74
Journal of Food Quality Natural Preservatives to Improve Food Quality and Safety Lead Guest Editor: Moreno Bondi Guest Editors: Simona de Niederhausern, Chrissanthy Papadopoulou, Andrea Laukova, and Patrizia Messi

Natural Preservatives to Improve Food Quality and Safety

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Page 1: Natural Preservatives to Improve Food Quality and Safety

Journal of Food Quality

Natural Preservatives to Improve Food Quality and Safety

Lead Guest Editor Moreno BondiGuest Editors Simona de Niederhausern Chrissanthy Papadopoulou Andrea Laukova and Patrizia Messi

Natural Preservatives to ImproveFood Quality and Safety

Journal of Food Quality

Natural Preservatives to ImproveFood Quality and Safety

Lead Guest Editor Moreno BondiGuest Editors Simona de NiederhausernChrissanthy Papadopoulou Andrea Laukova and Patrizia Messi

Copyright copy 2017 Hindawi All rights reserved

This is a special issue published in ldquoJournal of Food Qualityrdquo All articles are open access articles distributed under the Creative Com-mons Attribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Editorial Board

Encarna Aguayo SpainRiccarda Antiochia ItalyJorge Barros-Velaacutezquez SpainJoseacute A Beltraacuten SpainAacute A Carbonell-Barrachina SpainMarina Carcea ItalyMaria Rosaria Corbo ItalyEgidio De Benedetto ItalyAlessandra Del Caro ItalyAntimo Di Maro Italy

Rossella Di Monaco ItalyHuumlseyin Erten TurkeySusana Fiszman SpainAndrea Galimberti ItalyEfstathios Giaouris GreeceVicente M Goacutemez-Loacutepez SpainElena Gonzaacutelez-Fandos SpainAlejandro Hernaacutendez SpainJesuacutes Lozano SpainSara Panseri Italy

Mariacutea B Peacuterez-Gago SpainWitoon Prinyawiwatkul USAEduardo Pueacutertolas SpainJuan E Rivera MexicoFlora V Romeo ItalyJordi Rovira SpainAmy Simonne USAGiuseppe Zeppa Italy

Contents

Natural Preservatives to Improve Food Quality and SafetyMoreno Bondi Andrea Laukovaacute Simona de Niederhausern Patrizia Messi and Chrissanthy PapadopoulouVolume 2017 Article ID 1090932 3 pages

Natural Food Additives and Preservatives for Fish-Paste Products A Review of the Past Present andFuture States of ResearchKhawaja Muhammad Imran Bashir Jin-Soo Kim Jeong Hyeon An Jae Hak Sohn and Jae-Suk ChoiVolume 2017 Article ID 9675469 31 pages

Development of a Chemically Defined Medium for Better Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31Wenli Liu Lanwei Zhang and Huaxi YiVolume 2017 Article ID 9017452 8 pages

Lipid Oxidation Color Changes and Microbiological Quality of Frozen Beef Burgers Incorporatedwith ShiraziThyme Cinnamon and Rosemary ExtractsHadi Hashemi Gahruie Seyed Mohammad Hashem HosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan ShadVolume 2017 Article ID 6350156 9 pages

Optimization of Ultrasound Extraction of Cactus Pear (Opuntia ficus indica) Seed Oil Based onAntioxidant Activity and Evaluation of Its Antimicrobial ActivityMariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-Cansino Ernesto Alaniacutes-GarciacuteaLuis Delgado-Olivares Joseacute Alberto Ariza-Ortega Esther Ramiacuterez-Morenoand Joseacute de Jesuacutes Manriacutequez-TorresVolume 2017 Article ID 9315360 9 pages

Antioxidant and Antimicrobial Properties of Cactus Pear (Opuntia) Seed OilsEsther Ramiacuterez-Moreno Raquel Carintildeo-Corteacutes Nelly del Socorro Cruz-Cansino Luis Delgado-OlivaresJoseacute Alberto Ariza-Ortega Vanessa Yelina Montantildeez-Izquierdo Mariacutea Manuela Hernaacutendez-Herreroand Tomaacutes Filardo-KerstuppVolume 2017 Article ID 3075907 8 pages

EditorialNatural Preservatives to Improve Food Quality and Safety

Moreno Bondi1 Andrea Laukovaacute2 Simona de Niederhausern1

Patrizia Messi1 and Chrissanthy Papadopoulou3

1Department of Life Sciences University of Modena and Reggio Emilia Via G Campi 287 Modena Italy2Institute of Animal Physiology Slovak Academy of Sciences Soltesovej 4-6 040 01 Kosice Slovakia3Microbiology Department Faculty of Medicine School of Health Sciences University of Ioannina Ioannina Greece

Correspondence should be addressed to Moreno Bondi morenobondiunimoreit

Received 12 October 2017 Accepted 12 October 2017 Published 12 December 2017

Copyright copy 2017 Moreno Bondi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Food products can be contaminated by a variety of path-ogenic and spoilage microbiota the former causing food-borne diseases and the latter causing significant economiclosses for the food industry due to undesirable effects onthe food properties According to the Centers for DiseaseControl and Prevention (CDC) each year in the UnitedStates 48 million people get sick 128000 are hospitalizedand 3000 die because of foodborne infections Howeveralthough foodborne outbreaks are well recorded sporadiccases are not because not all patients visit the doctor orenter the hospital and the causative agent is not alwaysidentified A considerable number of foodborne pathogens ofgreat public health importance (eg VTEC E coli serotypesCampylobacter jejuni Listeria monocytogenes and Yersiniaenterocolitica) have emerged during the recent two decadescausing severe illness and foodborne outbreaks worldwide

Microbial food spoilage is also an area of immenseconcern for the food industry It is estimated that as much as25 of all food produced is lost after harvest due to microbialactivity While the growth of spoilage microbiota in foodsis not harmful for the human health it has negative impacton the shelf-life textural characteristics and overall qualityof the finished products affects the consumer choices andresults in significant commercial losses Thus prevention orinhibition of microbial growth in foods is of outmost impor-tance for the current globalized food production Hencethere is still the need for new processing methods to be usedeither alone or in combination with the already existing onesable to reduce or eliminate foodborne pathogens and spoilagebacteria

Chemical additives have been extensively used to preventthe survival and proliferation of microorganisms but their

safety and impact on human health are under discussionSince the reduction or elimination of pathogens and spoilagemicroorganisms in food is the foremost priority the currenttrends in food processing are focusing on the use of naturalcompounds which are considered as safe alternatives andsatisfy the consumer preferences for more ldquogreen foodsrdquoHence the increased awareness on the safety of food additivesand preservatives and the consumerrsquos trend to avoid foodscontaining chemicals which in the long-term may haveadverse impact on their health have generated a significantnumber of studies and publications on the potential useof various natural substances recognized as GRAS (Gener-ally Recognized as Safe) to be used as food preservativesChemical compounds added to foods as antioxidant agentsare also of concern particularly when important proteinsources (eg burgers steaks) are involved in the daily diet ofwesternized consumer living in the developed countries [1 2]Synthetic antioxidants such as BHT TBHQ and BHA havedemonstrated various adverse effects on the human healthincluding allergy headache asthma and dermatitis Recentstudies on the utilization of natural antioxidants (eg herbalessential oils and extracts) indicate their capacity and safety[3 4] Also the antimicrobial properties of natural substancessuch as plant essential oils and extracts have been extensivelystudied with promising results [5] The proper recycling anduse of fruit-processing plants by-products like fruit seedsor skins discarded and piling up in huge amounts everyyear are of great interest for the food industry particularlytheir potential to be a useful source of oil and meal [6]Additionally the oil from plant seeds can be used by thefood industry for manufacturing more ldquonaturalrdquo or ldquogreenrdquofoods and also can sufficiently extend the shelf-life of the

HindawiJournal of Food QualityVolume 2017 Article ID 1090932 3 pageshttpsdoiorg10115520171090932

2 Journal of Food Quality

food product [7] The oils derived from fruit seeds oils mayalso have some more useful properties beyond being justldquoediblerdquoThe oil derived from the seed extract of twoMexicanvarieties of cactus pear (Opuntia albicarpa and Opuntia ficusindica) has been found to have sufficient antioxidant andantimicrobial properties [8] Furthermore some biologicalactive compounds produced by microorganisms are widelyused in the food industry as well A good alternative toconventional chemically synthesized food preservatives is theuse of natural antimicrobials such as bacteriocins producedby lactic acid bacteria (LAB) with Nisin being officiallyemployed by the food industry and thus the most widelyused Bacteriocins are peptides actually microbial toxinsproduced from various microorganisms and so far someof them (eg enterocins produced mostly by enterococci)have shown remarkable antimicrobial potential and theirapplication as a natural barrier against pathogens and foodspoilage has been proven to be very efficient when used inthe form of purified or semipurified extracts or as protectivecultures [9 10] Therefore as the developments in foodpreservation are focusing on the implementation of naturalantimicrobials and antioxidants this special issue exploresthe potential of alternatives to currently used preserva-tives through the publication of five high-quality articleswhich aim to address recent advancements in the field ofnatural food preservatives and antioxidants The prospectto replace synthetic preservatives with natural substanceshas been demonstrated by comparing the effects of Shirazithyme cinnamon and rosemary extracts (denoted as naturalantioxidants) with those of the synthetic antioxidant BHT onprotein and lipid oxidations physicochemical microbial andsensory characteristics of frozen beef burgers during storageSpecifically the oxidative stability of the beef burgers contain-ing Shirazi thyme cinnamon and rosemary extracts was welldemonstrated and the antibacterial activitywas documentedas the total microbial counts of the tested burgers were wellbelow the maximum allowed limit Besides the evaluationof the antimicrobial and antioxidant properties of naturalsubstances it is important to optimize their recovery Withregard to bacteriocins to enhance Enterocin Y31 productionand simplify the steps of separation and purification a propersimplified and defined medium (SDM) has been developedfor the Enterococcus faecium Y31 growth and enhancementof the Enterocin Y31 production The bacterial growth didnot result in Enterocin Y31 production in MRS medium andtherefore both the growth rate and the EnterocinY31 produc-tion were set as the goal for the investigation Single omissionexperiments revealed that 5 gL NaCl five vitamins twonucleic acid bases MgSO4sdot7H2O MnSO4sdot4H2O KH2PO4K2HPO4 CH3COONa fourteen amino acids and glucosewere essential for the adequate strain growth and EnterocinY31 production As a result a novel simplified and definedmedium (SDM) was formulated containing 30 ingredientsin which the Enterocin Y31 production yield was higherwhen compared to either MRS or CDM The developmentof the SDM improved the Enterocin Y31 production andsimplified the steps of purification (only two steps) whichis very promising and increases its potential applicationsReferring to seedsrsquo oils the optimization of the extraction

conditions of cactus pear seed oil has been obtained usingultrasound in a closed system based on the antioxidantactivity and using response surface methodology The yieldextraction and antioxidant and antimicrobial activity werecompared with those obtained using both conventional andunconventional methods such as Soxhlet and macerationusing heat agitation or long extraction times microwavesupercritical fluids and ultrasound-assisted extraction inan open and in a closed system The results have shownthat ultrasound exhibited lower oil yield and antioxidantactivity but had the potential to achieve comparable resultsif multiple ultrasound extractions are performed in the timeneeded by conventional methods Seed oils showed similarantimicrobial activity despite the extraction method and canbe an alternative extraction method of seed oils from fruitssuch as cactus pear Lastly the replacement of chemicaladditives with natural compounds has been addressed for fishfoods as well Fish-paste products also known as fish cakes orsurimi-based products are worldwide favorites Surimi a wetprotein concentrate of fish muscle is used as an intermediateraw material to produce surimi seafood The flavor texturetaste shelf-life and market value of surimi-based productsdepend on several factors including the additives used toprepare the surimi While preparing surimi with chemicaladditives several problems have been observed such as alack of unique characteristics inferior acceptability and poorfunctionality In this context a systematic review of fish-paste products prepared using natural food additives (eganimal seafood and plant source additives herbs and orientalmedicines grains and roots and functional food materials)has been performed which summarizes the existing relevantknowledge in the production of new value-added foodstuffsof interest for the surimi industry

In conclusion this special issue offers to the readers thechance to be informed on the recent advancements relatedto the antimicrobial and antioxidant properties of naturalsubstances that are of interest for the contemporary foodindustry Their prospective use in the food production hasthe potential to lead towards the production of safer andhealthier foods not excluding their contribution to a moreefficient preservation of the environment when chemicalswill be replaced with natural substances

Moreno BondiAndrea Laukova

Simona de NiederhausernPatrizia Messi

Chrissanthy Papadopoulou

References

[1] G Comi E Tirloni D AndyantoMManzano and L IacuminldquoUse of bio-protective cultures to improve the shelf-life andthe sensorial characteristics of commercial hamburgersrdquo LWT -Food Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[2] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWT - FoodScience and Technology vol 68 pp 385ndash390 2016

Journal of Food Quality 3

[3] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[4] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[5] H Sakkas P Gousia V Economou V Sakkas S Petsios and CPapadopoulou ldquoIn vitro antimicrobial activity of five essentialoils on multidrug resistant Gram-negative clinical isolatesrdquoJournal of Intercultural Ethnopharmacology vol 5 no 3 pp212ndash218 2016

[6] B Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Fatty Acids in Foods and their Health ImplicationsThirdEdition vol 20073230 of Food Science and Technology pp 263ndash301 CRC Press 3rd Edition edition 2007

[7] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

[8] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research (Formerly Natural Product Letters)vol 27 no 14 pp 1305ndash1314 2013

[9] R Iseppi F Pilati M Marini et al ldquoAnti-listerial activity of apolymeric film coated with hybrid coatings doped with Ente-rocin 416K1 for use as bioactive food packagingrdquo InternationalJournal of Food Microbiology vol 123 no 3 pp 281ndash287 2008

[10] A Laukova and P Turek ldquoEffect of enterocin 4231 in Slovak fer-mented salami puchov after its experimental inoculation withListeria Innocua Lirdquo ACTA Scientiarum Polonorum TechnologiaAlimentaria vol 10 no 4 pp 423ndash431 2011

Review ArticleNatural Food Additives and Preservatives forFish-Paste Products A Review of the Past Present andFuture States of Research

Khawaja Muhammad Imran Bashir1 Jin-Soo Kim2 Jeong Hyeon An1

Jae Hak Sohn13 and Jae-Suk Choi13

1Seafood Research Center IACF Silla University 606 Advanced Seafood Processing Complex Wonyang-roAmnam-dong Seo-gu Busan 49277 Republic of Korea2Department of Seafood and Aquaculture Science Gyeongsang National University 38 Cheondaegukchi-gilTongyeong-si Gyeongsangnam-do 53064 Republic of Korea3Food Biotechnology Division of Bioindustry College of Medical and Life Sciences Silla University 140 Baegyang-daero700 beon-gil Sasang-gu Busan 46958 Republic of Korea

Correspondence should be addressed to Jae-Suk Choi jsc1008sillaackr

Received 9 June 2017 Revised 15 August 2017 Accepted 17 September 2017 Published 27 November 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Khawaja Muhammad Imran Bashir et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Fish-paste products also known as fish cakes or surimi-based products are worldwide favorites Surimi a wet protein concentrateof fish muscle is used as an intermediate raw material to produce surimi seafood The flavor texture taste shelf-life and marketvalue of surimi-based products depend on the source of the fish meat type of applied heat treatment and additives used toprepare the surimi While preparing surimi with chemical additives several problems have been observed such as a lack of uniquecharacteristics inferior acceptability and poor functionality Various types of fish-paste products have been developed by usingdifferent ingredients (eg vegetables seafood herbs and oriental medicines grains and roots including carrots and functionalfood materials) However a systematic review of fish-paste products prepared using natural food additives has not yet beenperformedTherefore the quality characteristics of fish-paste products and their functionalities were elucidated in this study Withthe increasing demand for surimi seafood products the functional properties physiochemical properties and shelf-life of surimi-based products need to be improved This review will aid the preparation of new value-added products in the surimi industry

1 Introduction

Fish-paste products popularly known as fish cakes areproduced from frozen surimi (ie they are a kind of surimi-based product) and are popular in Korea and Japan [1] Inthe Korean Food Standards Codex fish cakes are known asa processed marine product comprising salt-soluble proteinsisolated from fish meat [2] Fish muscle is mechanicallydeboned washed with water and blended with cryoprotec-tants to prepare a wet concentrate of proteins called surimiSurimi is a Japanese term that is also known as washed fishmince It is a refined fish myofibrillar protein manufacturedthrough numerous step-by-step processes including headinggutting filleting deboning (mincing) washing dewatering

refining mixing with cryoprotectants freezing and metaldetection for HACCP [3] The myofibrillar proteins make itan excellent ingredient for developing food products It hasexcellent gelling properties and forms strong and elastic gelsupon heating [4]

The setting and deformation are important to preparesurimi and surimi-based products Setting also known asldquosuwarirdquo in Japanese is a very important process which hasa significant influence on the physiological and rheologicalproperties of surimi-based products Setting is a vital processin the quality estimation of surimi because it helps to improvethe water-holding capacity as well as the gel texture of surimi-based productsWhen fishmince paste (sol) is heated at a lowtemperature (up to 50∘C) a loose network (suwari) is formed

HindawiJournal of Food QualityVolume 2017 Article ID 9675469 31 pageshttpsdoiorg10115520179675469

2 Journal of Food Quality

from myosin and actomyosin molecules this process isreferred to as setting Setting is species dependent and occursover a range of temperatures (up to 50∘C) and to a varyingextent As the temperature is increased to around 70∘Csuwari is partially disrupted to form a broken net structure(modori) a phenomenon attributed to the dissociation ofmyosin from actin and the possible fragmentation of the actinfilament [5ndash7]

Most of the surimi-based products are different types offish-paste products while less than 10 include fish burgersfish ham and fish sausages [3] Surimi-based products areprepared by mixing the raw or frozen surimi with saltsand other ingredients molded and heated to form the finalproduct in the specified shape and texture and pasteurizedbefore packaging The kind of heat treatment depends on theflavor texture and appearance of the desired final productand may include broiling steaming deep-fat frying andboiling [8] while fish-paste products in South Korea aremostly prepared by frying [9] Textural characteristics suchas gel strength are the major determinant of surimi priceand quality [10] Several studies have attempted to enhancethe textural quality of surimi or surimi-based products usingvarious protein additives [11ndash14]

Surimi quality and gelling property are mainly affectedby both intrinsic factors (effect of fish species seasonalitysexual maturity and freshness or rigor) and extrinsic fac-tors (harvesting handling water characteristics processingtime and temperature solubilization of myofibrillar proteinsduring processing the activity of the endogenous or addedprotein oxidants and proteolytic enzymes washing cyclessalinity and pH) [3 134] Surimi forms thermoirreversiblegels upon heating which do not deform with further changein the temperature This phenomenon of surimi and surimi-based products is similar to that observed in other proteinssuch as egg white milk-lactoglobulin and wheat glutenAdditionally surimi produces gels of very high deformabilityand strength This heat-induced gelation property of surimimakes it a very valuable food ingredient [134]

The gel-forming ability and capacity of surimi areadversely affected by the proteolytic degradation of myofib-rillar proteinsThe presence of indigenous proteinases causedgel softening in surimi made from fish species for examplethreadfin bream [135] arrow tooth flounder [136] Pacificwhiting [137] and lizard fish and bigeye snapper [20 59]Various active proteinases in fish muscle are responsible forsoftening of the surimi gels Nakamura and Ogawa and Anet al testified that cathepsins L and B were the most activecysteine proteinases in Pacific whiting surimi and fish filletsrespectively [7 138] The myofibril-associated proteinasesobserved in lizardfish surimi were serine proteinases andcysteine while a serine proteinase was reported in the bigeyesnapper surimi [20 59]

Seasonal analysis of the compositional properties ofAlaska pollock and Pacific whiting showed higher proteincontents in winter while the moisture contents were higherin summer [139 140] Surimi prepared from cold-water fishspecies with low thermostability of myofibrillar proteinsmakes setting easier Normally a myofibrillar protein withlow thermostability is optimum to do setting because its

reactivity is increased due to the loose internal structure bysodium chloride addition and heat denaturation In contrastthe myofibrillar protein of tropical fish species with high heatstability is difficult to denature and form the myofibrillarprotein network structure in surimi [3]

Several research groups have studied ways to enhance thequality of surimi-based products by investigating the changesin microbial content enzyme activity nutrient content andacceptability characteristics the use of raw materials thestandardization of the manufacturing process storage andmarketing Natural and chemical food-grade additives suchas konjac flour proteinase inhibitors egg white and hydro-colloids have been used to enhance the gelling properties ofsurimi [12 17 20 23 34 141ndash143] The trypsin inhibitor inegg white plays a major role in improving the gel strengthof surimi The addition of egg white inhibits the proteolyticactivity of the modori-inducing enzyme in fish meat andsuppresses the decrease of elasticity in surimi Serum pro-teins have strong inhibiting abilities against the action ofvarious proteases with different active centers such as SHgroups and serine groups In addition they also containtransglutaminases that accelerate the setting Egg white andserum proteins also play an important role in inhibiting theenzymatic activity of the parasites Apart from the use ofadditives gel strengthening can be achieved by treating thegels at low temperatures (0ndash40∘C) before cooking [144 145]Furthermore the gel quality of surimi and surimi-basedproducts can also be enhanced by using alternate fish speciesor by acid and alkali washing to increase the myofibrillarprotein concentrations [7 146 147]

Surimi production worldwide reached around800000MT by 2011-2012 [3] while South Korea alonecontributed approx 156000MT in 2013 Over the yearsthe size of the market for Korean fish-paste products hasgradually increased reaching sim350 million US dollars in2013 (based on the amount produced) [148] Howevermanufacturers have had several problems in producingsurimi-based products such as a lack of unique character-istics and inferior acceptability and functionality Thereforethere have been several attempts to develop new fish-pasteproducts with excellent acceptability and functionalityTo this end numerous types of fish-paste products havebeen developed using various natural ingredients such asvegetables seafood animals plants herbs and orientalmedicines seaweed and functional food materials It is ofworldwide interest to use these natural food preservativesinstead of chemical or synthetic ones However to date nosystematic review of fish-paste products supplemented withvarious food raw materials has been performed Thereforethe quality characteristics of fish-paste products and theirfunctionalities were elucidated in this study

2 Improvement of the Gel Properties ofFish-Paste Products

Various food additives derived from animals (eg beefswine and chicken) seafood (eg fish invertebrates) plants(eg legumes cereals) sugars polyols and functional mate-rials used in fish-paste products to improve their gelling

Journal of Food Quality 3

capabilities and strength are listed in Table 1 and describedbelow

21 Animal Source Additives Various food-grade proteaseinhibitors from animal sources are used to enhance thephysical properties of surimi-based products as well to pre-vent the protein degradation The ability of beef plasma andother food-grade additives in surimi and fishmince preparedfrom Pacific whiting (Merluccius productus) was studied byMorrissey et al [12] The strongest proteolytic inhibitionwas observed with beef plasma protein at a concentrationas low as 1 Reppond and Babbitt reported the increase ingel strength of gels prepared by arrow tooth flounder at aconcentration of 2 with a yellow hue color [16] Weeras-inghe et al characterized the inhibitory activity of these food-grade inhibitors and reported that the inhibitory activity wasmainly because of specific serine proteinase inhibitors [17]The addition of 2 dried bovine plasma to steamed fish-pasteslightly increased the chewiness and hardness but it showeda negative effect on the gel strength [18] Duangmal andTaluengphol reported that the higher levels of beef plasmaprotein unfavorably affected gel characteristics of red tilapiasurimi gels [19]

The effect of porcine plasmaprotein on the bigeye snapper(Priacanthus tayenus) surimi gel characteristics was investi-gated by Benjakul et al [14]The gels supplemented with 05porcine plasma protein had the highest level of deformationand breaking force Benjakul and colleagues later reportedthe effect of porcine plasma protein on the gel characteristicsof surimi from bigeye croaker (Pennahia macrophthalmus)bigeye snapper (P tayenus) barracuda (Sphyraena jello)and threadfin bream (Nemipterus bleekeri) [20] The porcineplasma protein was effective in increasing the deformationand breaking force of kamaboko gels Higher breaking forcesand levels of deformation occurred when chicken plasmaprotein was supplemented to sardine kamaboko gels at levelsup to 2 [21] The inhibitory activities of cysteine proteinaseinhibitor fraction from chicken plasma on Pacific whitingand arrow tooth flounder mince were reported by Rawdkuenet al [22] Furthermore similar results were observed intheir extended study onPacificwhiting surimi where chickenplasma at a level of 2 inhibited the degradation of myosinheavy chain proteins [23]

Ovomucoid is a mucoprotein obtained from egg whitethat has been tested for its potential as a gel-degradationinhibitor [24 25] The addition of 2 ovomucoid couldincrease the breaking strength and gel deformation [28]The autolytic activities of lizardfish (Saurida tumbil) surimiand mince under the application of protease inhibitors wereinvestigated by Yongsawatdigul and Piyadhammaviboon[26] At all preincubation conditions egg white enhancedthe gel-forming capability of S tumbil surimi to a greaterextent than did whey protein concentrateThe addition of 1egg white and preincubation at 25∘C increased the breakingforce by twofold Campo-Deano and Tovar [27] reportedthat the addition of egg albumen at 15 and 2 for Alaskapollock and Pacific whiting surimi respectively enhancedthe gel strength of crab sticks According to Hunt et al theincorporation of 2-3 special dried egg white improved

the gel textural characteristics of Alaska pollock and Pacificwhiting surimi [28]

Whey is the complete set of proteins isolated fromthe watery portion of milk Whey protein is comprisedof 20 milk protein and 80 casein [149] Whey proteinconcentrates have generally been used as an emulsifierfiller water binder protein supplement foam stabilizer andthickener as well as gelling agent [150] Rawdkuen andBenjakul investigated the effect of whey protein concentrateon the gelling characteristics of surimi prepared fromgoatfish(Mulloidichthys vanicolensis) bigeye snapper (P tayenus)lizardfish (S tumbil) and threadfin bream (N bleekeri) [29]All the tested surimi supplemented with 3 whey proteinconcentrate displayed inhibitory activity against autolysis andsignificantly reduced gel whiteness However better water-holding capacity was obtained by increasing concentrationsof whey protein concentrate

Plasma proteins produced from pig cow and chickenbyproducts are relatively affordable and easily collectiblesources [143 151 152] However outbreaks of foot-and-mouthdisease avian influenza andmad cow disease as well as a banonproteins frompig bone and skin in some states for religiouscauses have made it essential to search alternative sources[153 154] Various fish plasma proteins have been testedincluding those from rainbow trout and salmon [31 35 36]

22 Seafood Additives The effects of shrimp head proteinhydrolysate fromdifferent shrimp namely black tiger shrimp(Penaeus monodon) northern pink shrimp (Pandalus eous)and endeavour shrimp (Metapenaeus endeavouri) on thegelling properties of lizardfish (Saurida spp) surimi wereinvestigated by Ruttanapornvareesakul et al [30] It wasreported that the freeze-induced denaturation of lizardfishmuscle protein could be reduced by the supplementation ofshrimp head protein hydrolysate at a concentration of 5resulting in higher Ca-ATPase activity and gel strength Theeffects of rainbow trout plasma proteins on the gelling prop-erties of surimi prepared by Alaska pollock were investigatedby Li et al [31] Gel degradation deformation the breakingforce water-holding capacity and whiteness enhanced withincreasing amounts of rainbow trout plasma protein anddecreased at higher concentrationsThe rainbow trout plasmaprotein at a concentration of 075mgg could be used asa potential protease inhibitor to inhibit gel weakening inAlaska pollock surimi Li et al reported the higher inhibitoryactivities of the recombinant chum salmon cystatin againstautolysis of Alaska pollock surimi [155]

Fish gelatin is extracted from the collagen of fish skinand it is used as a food additive Hernandez-Briones et alstudied the functional and mechanical properties of Alaskapollock surimi gels while using fish gelatin as an additive[32] The increasing concentration of gelatin affected thewhiteness but the sensory panelists were unable to detect itThese results showed that fish gelatin was not effective as afunctional additive in Alaska pollock surimi Nevertheless itcould be added at up to 10 gkg without negatively affectingthe mechanical properties of surimi Yin et al reported asignificant improvement in the endogenous transglutaminaseactivity of Alaska pollock surimi prepared with nanoscaled

4 Journal of Food Quality

Table1Naturalfood

additiv

esused

toim

provethe

gelpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Animalsource

additiv

es

Beefplasma

hydrolysate

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Atlanticmenhaden

(Brevoortia

tyrann

us)

Alaskap

ollock

(Theragra

chalcogram

ma)

Moistu

recontentproteincontent

cook

inglossw

ater-holding

capacitytexturetorsio

ntest

05

ndash15

[15]

Bovine

plasma

Bostaurus

Heatedin

awater

bath

Powder

Arrow

toothflo

under

(Atheresthessto

mias)

Walleye

pollo

ck

Moistu

recontentpu

nchtorsion

colortest

2[16]

Beefplasma

protein

Bostaurus

mdashPo

wder

Pacific

whitin

g(M

erlucciusp

rodu

ctus)

Proteincontentinhibitory

assay

4[17]

Drie

dbo

vine

plasma

Bostaurus

Steaming

Powder

Alaskap

ollock

(Tchalco

gram

ma)

Nutrie

ntcontentpH

water-holding

capacitytexture

and

sensoryevaluatio

n2

[18]

Beefplasma

protein

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Redtilapia

(Oniloticus

xO

placidus)

Colortextureexpressiblewater

protein

totalsulfhydrylcon

tent

2gkg

[19]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Bigeye

snapper

(Pria

canthu

stayenus)

Expressib

ledrip

amou

ntcolor

texturesetting

cond

ition

s05

[14]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Threadfin

bream

(Nem

ipterus

bleekeri)Bigeyes

napp

er(Ptayenus)

Baracuda

(Sphyraena

jello)and

Bigeye

croaker

(Penna

hiamacrophthalmus)

Trichloroacetic

acid-solub

lepeptidescolortextureprotein

content

05

[20]

Chickenplasma

protein

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Sardine

(Sardinella

gibbosa)

Colortextureexpressiblemoistu

re

proteincontentautolysis

activ

ity2

[21]

Cyste

inep

roteinase

inhibitorfrom

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Arrow

toothflo

under

(Astomias)Pacific

whitin

g(M

produ

ctus)

Autolysis

andinhibitory

activ

ity

pHprotein

content

3[22]

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Pacific

whitin

g(M

produ

ctus)

Torsionandfracture

test

dynamic

rheologicalattribute

2[23]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[24]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[25]

Eggwhite(EW)

Gallusgallusd

omesticus

Heatedin

awater

bath

Powder

Lizardfish(Saurid

atumbil)

mince

andsurim

iAu

tolytic

activ

itytexturalattributes

EW1

[26]

Eggalbu

min

Gallusgallusd

omesticus

Heatedin

thec

ooking

roller

Eggwhite

itself

Surim

i-based

crab

sticksfrom

Alaskap

ollock

(AP)

Pacific

whitin

g(PW)

(Mprodu

ctus)

Transie

nttest

streng

thtest

texture

dynamicrheologicaland

physical

attributes

AP

15

PW2

[27]

Journal of Food Quality 5

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Regu

lard

riedegg

white(REW

)speciald

riedegg

white(SEW

)liq

uideggwhite

(LEW

)

Gallusgallusd

omesticus

Heatedin

awater

bath

Spray-dried

powder

Pacific

whitin

g(M

produ

ctus)

Totalsulfhydrylgroup

sfracture

test

dynamicrheologicalattribute

SEW2-3

[28]

Wheyprotein

concentrate

Bostaurus

Heatedin

awater

bath

Wheyprotein

concentrate

Bigeye

snapper(Ptayenu

s)Goatfish

(Mulloidich

thys

vanicolen

sis)

Threadfin

bream

(Nblee

keri)

and

Lizardfish(Stum

bil)

Water-holding

capacitycolor

autolytic

activ

ity3

[29]

Seafoo

dadditiv

esSh

rimphead

proteinhydrolysate

from

northern

pink

shrim

pendeavou

rshrim

pand

blacktig

ershrim

p

Pand

alus

eous

Metapenaeus

endeavouri

Pena

eusm

onodon

Heatedin

awater

bath

Drie

dmatter

Lizardfish

(Saurid

aspp)

Gelstr

engthcolorgel-forming

abilityC

a-AT

Pase

activ

ity5

[30]

Rainbo

wtro

utplasmap

rotein

Oncorhynchu

smykiss

Heatedin

awater

bath

Freeze-drie

dplasma

Alaskap

ollock

Proxim

atea

nalysisw

ater-holding

capacitycolortextureprotein

content

075

mgg

[31]

Fish

gelatin

Com

mercialfishgelatin

(Gelatin

Rousselot)

Heatedin

awater

bath

Powder

Alaskap

ollock

Colorm

echanicalfunctio

nal

sensoryattributes

10gkg

[32]

Nanoscaled

fish-bo

neof

Pacific

whitin

gMprodu

ctus

Heatedin

awater

bath

Powder

Alaskap

ollock

Texturescanning

electron

microscop

y1g10

0g[33]

Nanoscaled

fish-bo

ne(N

FB)+

driedeggwhite

(DEW

)

Mprodu

ctusGallus

gallu

sdom

esticus

Heatedin

awater

bath

Powder

Pacific

whitin

g(M

produ

ctus)

Rheologicaland

texturalattributes

DEW

1+

10mgNFB

Cag

surim

ipaste

[34]

Salm

onbloo

dplasma

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)

Scanning

electronmicroscop

yproteincontentdynamic

rheologicalattributes

1g10

0g[35]

6 Journal of Food QualityTa

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Freeze-drie

dchinoo

ksalm

onplasma(

FSP)

and

concentrate

salm

onplasma

(CSP

)

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)surim

iand

Salm

onmince

Proteolytic

inhibitio

nautolysis

proteincontent

Salm

onminceC

SPgt

FSP

Pacific

whitin

gsurim

iFSP

[36]

Partially

purifi

edtrypsin

inhibitor

from

ther

oeof

yello

wfin

tuna

fish

Thun

nusa

lbacares

Heatedin

awater

bath

Freeze-drie

dBigeye

snapper

(Pria

canthu

smacracanthu

s)Proteolysis

colorw

ater-holding

capacitygellin

gprop

ertie

s3g

100g

[37]

Squidink

tyrosin

ase(SIT)

+tann

icacid

(TA)

Todarodesp

acificus

Heatedin

awater

bath

Mixture

Sardine

(Sardinella

albella)

Tyrosin

asea

ctivityinvitro

oxidationassaycolortexturaland

sensoryattributes

SIT

500U

gprotein+

TA1

[38]

Plantsou

rcea

dditives

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soybean

protein

Wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[39]

Soyprotein

eggwhite(EW)

wheyprotein

concentrate

(WPC

)La

ctalbumin

(LA)

milk

proteiniso

late

(MPI)

Glycinem

ax

Gallusgallusd

omesticus

Bostaurus

Coo

kedin

aste

amcooker

Powder

AlaskaP

ollock

(Tchalco

gram

ma)

Textureexpressib

lemoistu

recontentwater

retentionprop

ertie

sEW

andMPI

[4041]

Legu

mes

eed

extractfrom

blackcowpea

whitecowpea

soybeanseeds

Mun

gbean

peanut

Vignaun

guicu

lata

Glycinem

axVignaradiata

Arachish

ypogaea

mdash

Freeze-drie

dproteinase

inhibitor

extracts

Threadfin

bream

(Nem

ipterid

ae)

ThermalstabilitypHprotein

contentproteinase

inhibitory

assay

Blackcowpea

soybeanseeds

30mgg

[42]

Legu

mes

eed

extractfrom

Cow

pea

pigeon

pea

bambara

grou

ndnu

ts

Vignaun

guicu

lata

Cajanu

scajan

Vo

andzeia

subterranea

mdashPartially

purifi

edTrypsin

Threadfin

bream

(Nem

ipterid

ae)

Sarcop

lasm

icmod

ori-ind

ucing

proteinase

activ

itycolor

30ku

nits

g[43]

bambara

grou

ndnu

tprotein

isolate

Vignasubterranea

Heatedin

awater

bath

Powder

Threadfin

bream

(Nblee

keri)

Colorautolysis

025

g100g

[44]

Soyproteiniso

late

Glycinem

axHeatedin

awater

bath

Com

mercial

soyprotein

isolate

(JinQ

ui1200)

Alaskap

ollock

(Tchalco

gram

ma)

Com

mon

carp

(Cyprin

uscarpio)

Totaln

itrogen

andmoistu

recontentgelstre

ngthcolor

10

[45]

Journal of Food Quality 7Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soyprotein

wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[46]

Dietary

fiber

(DF)

from

peaa

ndchicory+

microbial

transglutaminase

(MTG

ase)

Cichorium

intybu

sPisum

sativ

umHeatedin

awater

bath

Powder

Hake(Mcapensis)

Gilthead

seabream

(Sparusa

urata)

Seab

ass(Dice

ntrarchu

slabrax)

Meagre(Argyrosomus

regius)

Dyn

amicrheologicalattributes

MTG

ase100U

g[47]

Proteiniso

lates

from

Mun

gbean

(MBP

I)black

bean

(BBP

I)bam

bara

grou

ndnu

t(BG

PI)

Phaseolusa

ureus

Phaseolusv

ulgarisV

igna

subterranea

mdashFreeze-drie

dpo

wder

mdash

Scanning

electronmicroscop

yproteolytic

autolyticandtrypsin

inhibitory

activ

ityassaycolor

texturetrichloroacetic

acid-solub

lepeptidec

ontent

1g10

0g[48]

Partially

purifi

edtrypsin

inhibitor

from

adzukibean

Vignaangularis

Heatedin

awater

bath

Freeze-drie

dpo

wder

Threadfin

bream

(Nblee

keri)

Proteincontenttexturecolor

trypsin

inhibitory

activ

ityautolytic

activ

ityassay

3g10

0g[49]

Amylose(A)a

ndam

ylop

ectin

(AP)

mdashHeatedin

awater

bath

Powder

Walleye

pollo

ck(T

chalcogram

ma)

Gelationandbreaking

strength

Amylose70+

Amylop

ectin

4

[50]

Wheatsta

rch

Triticum

aestivum

Heatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Com

pressio

ntest

dynamic

viscoelasticityscann

ingele

ctron

microscop

y

Starch10g

+Surim

i10g

[51]

Natives

weetp

otato

starch(N

SPS)

and

Mod

ified

sweet

potato

starch

(MSP

S)

Ipom

oeabatatas

Heatedon

acontrolled

stress

rheometer

Powder

Alaskap

ollock

(T

chalcogram

ma)

Dyn

amicrheologicalattributes

5[52]

Potato

starch

Solanu

mtuberosum

Heatedin

the

Krehalon

ecasin

gfilm

Powder

Pacific

sand

lance(Am

modytes

personatus

Gira

rd)

Proxim

atea

nalysis

protein

compo

sition

colorfoldingtext

texturalandsensoryattributes

8[53]

Rice

flour

Oryza

sativa

Fried

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorrheologicaland

sensoryattributes

10ndash15

[54]

Rice

flour

Oryza

sativa

Fried

Powder

Threadfin

bream

(Nem

ipterid

ae)

Moistu

recontentpH

color

texturalandsensoryattributes

50

[55]

Rice

flour

Oryza

sativa

Fried

Powder

Goldenthreadfin

bream

(Nem

ipterusv

irgatus)

Gelstr

engthsensoryattributes

14

[56]

Cryoprotectantsa

ndhu

mectants

Xanthan(X)

locustbean

(LB)

gumsa

loneX

LB

ratio

Ceratoniasiliqua

Heatedin

awater

bath

Powder

Silver

carp

(Hypophthalm

ichthys

molitrix)

Torsiontest

gel-formingability

mechanicalattributes

XLB

025075

[57]

Pectin

gum

(HM

LM)+

CaCl2

mdashHeatedin

awater

bath

Gum

and

powder

Silver

carp

(Hm

olitrix)

Water-holding

capacitym

echanical

andtexturalattributes

Pectin

gum1+

CaCl202

[58]

8 Journal of Food Quality

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Chito

san7B

from

praw

nshell

Not

mentio

ned

Heatedin

awater

bath

Not

mentio

ned

Barred

garfish

(Hem

iramphus

far)

ProteincontentSE

Mtextural

attributes

1[59]

Konjac

glucom

annan

aqueou

sdisp

ersio

nAm

orphophallu

skonjac

Heatedin

awater

bath

Aqueou

sdispersio

n

Giant

squid(D

osidicu

sgigas)

Alaskap

ollock

(T

chalcogram

ma)

ProteinsolubilitypH

texturaland

viscoelasticrheologicalattributes

1[60]

Carrageenan+

NaC

lorK

Clmdash

Heatedin

awater

bath

Hydrocollo

idAlaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorcompressio

ntest

Carrageenan1+

KCl15

[61]

Amorphophallu

skonjac

flour

(AKF

)Am

orphophallu

skonjac

Heatedin

awater

bath

Flou

rGiant

squid(D

gigas)

Water

retentionabilitycolor

texturalandsensoryattributes

10

[62]

NaC

l+high

hydrostatic

pressure

(HHP)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Proxim

atea

nalysis

FTIR

SEM

colormechanicalrheologicaland

sensoryattributes

HHP

300MPa

+NaC

l03

[63]

Sodium

chlorid

esugarspolyols

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Larim

ichthys

polya

ctis)

Water

activ

ityV

BNcolor

moistu

recontent

Sodium

chlorid

e4

Glucose10

Glycerin

10

[64]

Starchglycine

sodium

lactate

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Lpolya

ctis)

Water

activ

ityV

BNcolorm

oistu

recontent

Sodium

lactate75

[65]

Glycerol

mdashSteamed

Liqu

idMackerel(Scom

berjaponicu

s)andBrazilian

sand

perch

(Pseud

opercis

semifa

sciata)

Water

activ

itytexturaland

sensory

attributes

20

[66]

Naa

ndCa

salts

ofpo

lyuron

ides

and

carboxym

ethyl

cellu

lose

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gel-

streng

theningeffects

2ndash6

[67]

L-ascorbicacid

(AsA

)and

dehydro-L-

ascorbicacid

(DAs

A)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthanalysis

DAsA

10120583

gg

[68]

Sodium

-L-

ascorbate

(SA)

mdash

Steamed

inNojax

cellu

lose

casin

g

Powder

Alaskap

ollock

(T

chalcogram

ma)

pHtexturaland

sensoryattributes

02

[69]

120596-3

fatty

acids

from

algae

Not

mentio

ned

Heatedin

awater

bath

Oil

Cod

(Gadus

morhu

a)TB

ARS

fattyacid

contentcolor

500m

g85

g[70]

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)

Microscop

icob

servation

viscosity

gel-formingability

10

[71]

Journal of Food Quality 9Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)Th

readfin

bream

(Nem

ipterid

ae)White

croaker(Ge

nyonem

uslin

eatus)

andJapanese

jack

mackerel(Trachu

rus

japonicus)

Proxim

atea

nalysis

color

water-holding

capacityphysic

alattributes

5ndash30

[72]

120596-3

PUFA

s-ric

hoils

Flaxseedalgae

menhaden

krillblend

(flaxseed

algae

krill

811)

Heatedin

awater

bath

Oil

Alaskap

ollock

(T

chalcogram

ma)

Torsiontest

andrheological

attributes

9g10

0g[73]

Ethano

licKiam

woo

dextract

(EKW

E)+

commercialtann

in(C

T)

Hopea

sp

Heatedin

awater

bath

Overdrie

dpo

wder

Strip

edcatfish

(Pangasiu

shypophthalmus)

pHV

BNT

BARS

color

TCA-

solublep

eptid

emoistu

re

proteincontents

texturalattributes

EKWE

008

CT002

ndash004

[74]

Cocon

uthu

skextractw

ithethano

l60(C

HE-E6

0)

80(C

HE-E8

0)

Cocosn

ucifera

Heatedin

awater

bath

Freeze-drie

dpo

wder

Sardine

(Salbella)

Totalpheno

licexpressible

moistu

reT

CA-solub

lepeptideand

proteincontents

colortextual

rheologicalandsensoryattributes

CHE-E6

00125

[75]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Solutio

nMackerel

(Rastre

lligerk

anagurta)

SEMexpressiblemoistu

reprotein

contentcolortexturalandsensory

attributes

OFA

040

OTA

050

OCF

050

OCT

010

[76]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Bigeye

snapper

(Ptayenus)

SEMexpressiblemoistu

reprotein

andfre

eaminoacid

contentcolor

texturalandsensoryattributes

OFA

020

OTA

005

OCF

015

OCT

005

[77]

Eggwhitepo

wder

(EW)whey

protein

concentrate(WPC

)

Gallusgallusd

omesticus

Triticum

aestivum

Heatedin

awater

bath

Powdera

ndconcentrate

Lizardfish

(Stum

bil)mince

andsurim

i

Autolytic

activ

ityT

CA-solub

leoligop

eptid

esprotein

content

texturalattributes

EW4

WPC

4

[26]

Zinc

sulfate

(ZnS

O4)sodium

tripolypho

sphate

(STP

P)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Yello

wstr

ipetrevally

(Sela

roideslep

tolep

is)

Expressib

lemoistu

relipid

phosph

olipidand

proteincontent

Ca-ATP

asea

ctivitycolortextural

attributes

ZnSO460120583

molkg+

STPP

05

[78]

SEMscann

ingelectro

nmicroscop

yFT

IRFou

rier-transfo

rminfrared

spectro

scop

yVBN

volatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stancesT

CAtric

hloroacetic

acid

10 Journal of Food Quality

fish bones [33] Furthermore a study on the rheologicaland textural attributes of Pacific whiting surimi showedthat slow heating and the addition of nanoscaled fish bonessignificantly enhanced gel strength [34]

Fowler and Park reported an enhanced gelling strengthand effectively inhibited proteinase activity in Pacific whitingsurimi gels heated ohmically [35] Fowler and Park laterstudied the effects of salmon plasma from Chinook salmonon proteolytic inhibition of surimi [36] Salmon plasmaeffectively inhibited both serine and cysteine proteases as wellas proteases isolated from Pacific whiting Salmon plasmaconcentrated by ultrafiltration performed slightly better thanfreeze-dried salmon plasma at inhibiting autolysis in salmonmince

Klomklao et al reported inhibitory activity of a par-tially purified trypsin inhibitor (TIYTR) from yellowfintuna (Thunnus albacores) on the gelling characteristics ofbigeye snapper (Priacanthus macracanthus) surimi [37] Theincorporation of TIYTR with a level of 30 g100 g resultedin the enhanced deformation and breaking force of surimigels suggesting that the TIYTR could be employed as anaffordable and alternative proteinase inhibitor to enhance thegel strength of surimi prepared by bigeye snapper

Vate and Benjakul investigated the effects of squid inktyrosinase mixtures of tannic acid and protein on the gellingcharacteristics of sardine surimi [38] The highest deforma-tion and breaking force were obtained when surimi gels wereallowed to react for 90min while being supplemented with1 tannic acid and 500Ug squid ink tyrosinase proteinHowever gels with an added squid ink tyrosinasetannicacid mixture were whiter than the control The surimi gelssupplemented with squid ink tyrosinasetannic acid mixtureshowed the maximum overall acceptance scores suggestingthat it could be used as an additive to increase the surimi gelproperties

23 Plant Source Additives The chicken plasma proteinegg white and beef plasma protein are considered as themost effective protease inhibitors for surimi [17 22 23156] However the use of chicken plasma and beef plasmaprotein has been forbidden because of the occurrence of avianinfluenza and mad cow disease respectively In additionhigher concentrations of beef plasma proteins have also beenassociated with off-flavors while egg white is expensive andhas an unwanted egg-like odor [29 156] Additionally veg-etarians would not want to consume surimi-based productsprepared with additives from animal or even seafood sourcesTherefore alternate food-grade additives are still desired toenhance the gel strength of surimi without affecting thecustomer demandVarious natural additives derived from theplant sources have been briefly described below

231 Legumes Theeffects of vegetable protein contentmois-ture heating and setting conditions on the physical attributesof kamaboko were examined by Yamashita [39] A firm gelwas obtained at 60∘C for kamaboko with soybean proteinand at 80∘C with wheat gluten When the kamaboko gelswere supplemented with 5 vegetable protein the changes injelly strength softness and expressiblewater of the kamaboko

with wheat gluten were somewhat greater than those of thekamaboko with soybean protein According to the results ofChung and Lee the addition of plant proteins including soyprotein isolate lactoalbumin and wheat gluten remarkablylessened the strength of non-animal protein-incorporatedsurimi gels [40] The textural and sensory attributes offiberized surimi gel products were categorized as an increasein overall textural desirability and an increase in gel strengthIn another study egg white and milk protein isolate showedhigher water retention ability than whey protein concentratesoy protein isolate and lactoalbumin [41]

Protein isolates from legume seeds can be used as alter-nate protein additives for the quality improvement of surimigels Legume seed isolates comprise trypsin inhibitors andhave been used as the protease inhibitor in the prepara-tion of surimi and surimi-based products [42 43] Ben-jakul et al reported higher protease inhibitory activities ofinhibitor extracts from soybean and black cowpea seeds[42] A reduced gel-degradation activity (modori) and ahigh thermal stability were reported In another study theyreported inhibitory effects of proteinase inhibitor extractsfrom Bambara groundnuts (Voandzeia subterranea) pigeonpea (Cajanus cajan) and cowpea (Vigna unguiculata) onautolysis and gel-degradation activity (modori) of threadfinbream surimi [43] The whiteness of surimi gels reducedslightly with the addition of proteinase inhibitor Similarresults were obtained by Oujifard and colleagues [44] TheBambara groundnut protein extracts at a level of 025 g100 gshowed improved autolytic inhibition deformation andbreaking force in surimi prepared by threadfin bream (Nbleekeri) [44] However a slight reduction in whiteness wasobserved at increasing levels of Bambara groundnut proteinisolates These studies show that the addition of Bambaragroundnut protein extracts at a suitable level could serve asan alternative food inhibitor to enhance the gelling propertiesof surimi

Plant protein isolates mainly soy protein isolates havebeen used in the surimi industry because of their safety andrational price [45] Luo et al indicated the legumin andvicilin two main legume seed storage proteins as bindersand cogelling agents in surimi gels [45] Protease inhibitorsisolated from legume seeds not only can help to reduce thegel-degradation process in surimi but can also improve thesurimi gel properties by acting as filler or binder Luo etal reported higher breaking force and quality characteristicsof silver carp surimi when supplemented at a ratio of 10soy protein isolate [46] Cardoso et al studied the effects ofdietary fiber and microbial transglutaminase from chicoryand pea on the rheological properties of protein paste fromgilthead sea bream hake meagre and seabass [47] It wasfound that a high degree of protein denaturation boosted gelhardness while a low degree of protein denaturation createdgels with high deformability It shows that the addition ofmicrobial transglutaminase could serve as a possible additivefor gels of those species having lesser protein unfoldingability

Kudre et al studied the effects of black bean (Phaseolusvulgaris) and mung bean (Phaseolus aureus) protein isolateson gelling properties and proteolysis of sardines (Sardinella

Journal of Food Quality 11

albella) surimi [48] An increase in deformation breakingforce and water-holding capacity as well as a lower levelof degradation was observed while the whiteness of kam-aboko gels reduced slightly Therefore mung bean or blackbean protein isolates could be effectively used to retardthe proteolysis in sardine surimi leading to improved gelstrength Klomklao and Benjakul studied the effects of thepartially purified trypsin inhibitor from adzuki bean on thegelling properties and proteolysis of threadfin bream (Nbleekeri) surimi [49] An increase in autolysis and inhibitoryactivity against sarcoplasmic proteinases aswell as an increasein deformation and breaking force of kamaboko gel wasobserved at increasing levels of trypsin inhibitor while gelwhiteness decreased slightly

232 Starch Starch is widely used to make fish-paste prod-ucts as it enhances elasticity and increases the weight ofthe products In attempts to control thermal stability stick-iness andor wetness under different serving and storageconditions the functional characteristics of surimi seafoodproducts have been widely studied using modified starchesStarch is the second most abundantly used ingredient in themanufacturing of fish-paste products because of its higherwater-holding ability and capacity to replace fish proteinspartially while preserving the desired gel features at a reducedcost [69 157ndash161]

Kim et al reported a positive correlation between theamount of added starch and the quality of the food products[162] Konoo et al studied the effects of adding starch andamylose to amylopectin contents of starch on the gela-tion properties of frozen walleye pollack surimi [50] Thebreaking strength of gel was not affected by the changein amylose amylopectin ratio However it increased as thecontent of amylose increased in pregelatinized starch [51]A lower packing effect was observed at 90∘C which hypoth-esized that the gelatinization of starch in fish meat can beprevented at this temperature A strong correlation betweenthe amylose to amylopectin contents and the textural andrheological properties of starch-containing surimi gels wasalso reported by Lanier et al [134]

The addition of normal and modified potato or sweetpotato starch resulted in reductions in the characteristicstorage modulus of surimi sols during heating [52] Surimigels supplemented with potato starch showed the highestfirmness and cohesiveness Yoo reported the best texturalproperties of the sand lance (Ammodytes personatus) fish-paste products at a level of 8 potato starch [53] Thesestudies show that potato or sweet potato starch can also beused as a potent food additive for the production of surimi

233 RiceRice Flour Fish meat and wheat flour are themajor ingredients used for the production of surimi-basedproducts Rice flour however can be an important ingredientto enhance the rheological properties of surimi-based prod-ucts Several attempts have been made to evaluate the poten-tial of rice flour as an alternate of wheat flour in the prepara-tion of surimi products [41] The effect of rice flour additionmethods and milling types on the sensory and rheologicalattributes of surimi products were studied by Cho et al [54]

Roll-mil rice at a concentration of 10ndash15 displayed highergel strength and sensory properties which show that roll-millrice had strong potential for replacing wheat flourThe surimiproducts containing rice flour showed similar rheological andsensory characteristics to those of a finest commercial surimiproduct Hence rice flour might be an effective alternative towheat flour for high-quality surimi products

To replace wheat flour Kwon and Lee examined thequality characteristics of fried fish cakes containing rice flour[55] The total content of corn starch and rice flour was2883 of the total content of fish cake doughThere were nonoteworthy differences in the pHmoisture level appearancecolor flavor taste and overall acceptance as compared tothe control group The addition of 50 rice flour to surimi-based products could be an effective way to increase thecontent of rice flour without decreasing texture acceptabilityYoon et al optimized the content of water and rice flourin surimi-based products [56] The surimi-based productsmanufactured under optimal environment were comparablein gel strength to the commercial products However highersensory evaluation scores were observed compared to thoseof the commercial products These studies advocate that therice flour not only can be employed as an alternative to wheatflour but can also be used to enhance the quality of surimiand surimi-based products

234 Potato Powder The food additives extracted frompotato and potato protease inhibitors used in the preparationof fish-paste products are discussed in Sections 21 232 and244

24 Cryoprotectants and Humectants To inhibit denatura-tion and to lessen the damage of gel quality during coldstorage cryoprotectants are usually added to surimi productsPolyunsaturated fatty acids protein additives polyols sugarsamino acids salts and plant extracts are frequently usedas cryoprotectants and humectants to avoid fluctuationsin myofibrillar proteins promoted by freezing storage orthawing [163] Mechanical properties of surimi gels can beimproved by the addition of numerous hydrocolloids such askonjac carrageenan locust bean xanthan gum and differentmicrobial transglutaminases during the preparation of surimiproducts [57 164ndash166] In contrast the addition of alginateshas been reported to weaken surimi gels [69]

241 Saccharides Xanthan is a nongelling polysaccharideproduced by the aerobic fermentation of Xanthomonascampestris [167] The property of xanthan to form highlyviscous and stable solution at low levels makes it acceptablein the food industry [168] Xanthan displays quite remarkablesynergistic interactions with other nongelling polysaccha-rides of the galactomannan family leading to increases in gelformation and viscosity [168 169] The three commerciallyavailable galactomannans are tara gum locust bean gum andguar gum

The impact of low methoxyl pectin on the mechanicalproperties of silver carp surimi gels was studied by Barreraet al [58] An increase in hardness shear stress and water-holding capacity of the surimi gel was observed while no

12 Journal of Food Quality

significant improvement in the mechanical properties wasobserved as compared to the control Benjakul et al reportedthe effects of prawn-shell chitosan on surimi prepared bybarred garfish (Hemiramphus far) [59] Prawn-shell chitosanat a level of 1 of the surimi gel showed an increase in gel-enhancing effect on the heat-induced gelation of myofib-rillar proteins The addition of microbial transglutaminasegenerally increases the deformation and breaking force ofsurimi gel However this effect was significantly retardedin the presence of prawn-shell chitosan resulting in lowermagnitudes of deformation and breaking force

The viscoelastic properties and the thermal stability oflow-grade squid (Dosidicus gigas) surimi were investigated byIglesias-Otero et al [60] The konjac glucomannan aqueousdispersion at a level of 1 expressed the best rheologicalproperties suggesting that the konjac glucomannan aqueousdispersion may be used to enhance the quality characteristicsof low-grade squid surimi gel Ramırez et al evaluated theeffect of protein-hydrochlorides on the gel-forming ability ofmyofibrillar proteins [142] The xanthanlocust bean gum ata ratio of 025075 showed a positive improvement in themechanical attributes of surimi gels Eom et al investigatedthe impact of carrageenan on the gelation property of salt-based Alaska pollock surimi [61] The addition of 15KCl rather than 2 NaCl significantly enhanced the gellingproperty of 120581-carrageenan-induced surimi gel and showedincreased gel strength breaking force and whiteness values

242 Salts Salts help in protein-protein interaction and theaddition of salt is critical during the processing of fish-pasteproducts However the high levels of sodium in foods andconsequently human consumption of sodium have becomea global issue The prime harmful effects of excess sodiumintake are hypertension and increased blood pressure Sub-sequently these conditions lead to cardiovascular diseasesincluding instances of stroke heart attack and relateddiseases as well as gastric cancer and osteoporosis [170ndash172] Therefore to reduce sodium intake levels in fish-pasteproducts Hwang et al prepared the sodium-reduced friedfish cakes containing potassium as a substitute for sodium [1]The quality characteristics of 30 sodium-reduced fried fishcakes were not notably different from those of full-sodiumfried fish cakes however the addition of potassium changedthe color and reduced consumer acceptance To increase theconsumer preference for sodium-reduced fried fish cakes theuse of different food additives might be advantageous

The weak gel-forming ability and the strong fishy smellof the giant squid (D gigas) make it undesirable for themanufacturing of surimi-based products To overcome theseproblems Choi and Kim used Amorphophallus konjac flourto enhance the quality characteristics of giant-squid surimiproducts [62]The increasing levels ofA konjac flour showedincreases in gel texture and water retention ability while areduction in color and taste was observed as compared tothe commercial surimi products The incorporation of theseasoning ingredients such as sweeteners might be helpfulin removing the fishy smell of D gigas ultimately improvingthe gel properties of giant-squid surimi Cando et al reportedthat the sensory and mechanical properties of surimi gels

with reduced-NaCl contents can be improved by the appli-cation of 300Mpa high hydrostatic pressures [63] The gelsmade with lower-NaCl contents revealed stronger and stablenetworks as showed by the ones with higher-NaCl contents

243 Water Activity It has been reported that humectantshad the greatest effect on lowering water activity (119886

119908) with

the efficiency of the reduction in 119886119908value decreasing in the

order of NaCl sodium lactate glycerin propylene glycoland sorbitol when each of them was combined with otherhumectants [173] Kim and Park reported the impact ofhumectants such as sodium chloride sugars and polyols tolower the water activity (119886

119908) of various model kamaboko gels

[64]The effect of sodium chloride on lowering water activity(119886119908) was the highest among all of the examined treatments

while glucose caused browning reaction on the surface ofkamaboko In another study they examined the effect ofstarch glycine and sodium lactate in lowering the wateractivity (119886

119908) of model kamaboko gels [65] Sanchez Pascua et

al reported that glycerol (15ndash50) was effective in reducingthe water activity (119886

119908) in Brazilian sand perch (Pseudopercis

semifasciata) and mackerel (Scomber japonicus marplatensis)[66] Among the tested humectants the efficiency of thereduction in water activity (119886

119908) was observed decreasing in

the order of sodium lactate glycine and starch

244 Polyuronides The effect of sodium and calcium salts ofcarboxymethyl and polyuronides cellulose on the strength-ening of kamaboko gels was investigated by Niwa et al [67]It was reported that the calcium salts of pectinic acid pecticacid alginic acid and carboxymethyl cellulose enhancedthe breaking force of Alaska pollock surimi whereas theirsodium salts except Na-pectinate failed to increase the break-ing force The increase in the breaking force induced by cal-cium carboxymethyl cellulose vanished upon increasing thedegree of substitution of hydroxyl groups to carboxymethylgroups Furthermore fine cellulose particles enhanced thebreaking strain and breaking force and reduced the amount ofexpressible water but were unsuccessful in the case of coarserparticlesThe addition of potato starch can increase the effec-tiveness even in the presence of coarse particles of cellulose

245 Ascorbic Acid The addition of dehydro-L-ascorbicacid and L-ascorbic acid to Alaska pollock surimi increasedthe gel strength [68] It was suggested that the positiveeffect of L-ascorbic acid on gel formation might be due tothe oxidation of sulfhydryl groups in fish proteins Lee etal studied the effects of sodium-L-ascorbate on the gel-forming abilities of surimi prepared by Alaska pollock [69]Sodium-L-ascorbate remarkably enhanced the gel firmnesscohesiveness strength and sensory properties of the fiber-ized products at a level of 02 It directly influenced thesurimi quality regardless of vacuum treatment indicatingthat airborne oxygen was not important Freeze-syneresisstimulated by ascorbate during frozen storage was lessenedby the application of hydroxypropylated-modified starch

246 Unsaturated Fatty Acids The addition of nutritionallybeneficial 120596-3 fatty acids during surimi preparation could

Journal of Food Quality 13

enhance the gel strength and stability [70] For the effectiveuse of highly unsaturated fatty acids such as docosahexaenoicacid (DHA) and eicosapentaenoic acid (EPA) in surimi-basedproducts Okazaki et al studied the gel-forming properties offrozen walleye pollock surimi containing DHA and EPA [71]They reported that to achieve a good quality product thevigorous agitation of surimi with fish oil is essential to allowthe heat-induced gelation of its emulsified product throughthe formation of fine oil droplets

Fukushima et al investigated changes in the physi-cal properties of heat-treated surimi gels prepared fromthreadfin breamwalleye pollock Japanese jackmackerel andwhite croaker [72] The breaking strain breaking strengthand water-holding capacity of the heat-treated gels becamegreater as the amount of fish oil increased Furthermoresurimi seafood was nutritionally enhanced with 120596-3 polyun-saturated fatty acid- (PUFA-) rich oils isolated from natu-ral sources such as algae flaxseed menhaden blend andkrill [73] The Alaska pollock surimi supplemented with120596-3 PUFA-rich oils showed improved protein fundamentaltextural properties heat-induced gelation and endothermaltransitions These studies show that the interaction of unsat-urated fatty acids and surimi proteins could contribute to theimprovement in gel properties without altering the texturalattributes

247 Plant Ethanol Extracts The effect of commercial tan-nin and ethanolic Kiam wood extract on the gelling char-acteristics of ice stored mackerel (Rastrelliger kanagurta)surimi was investigated by Balange et al [74] During12 d of iced storage pH TBARS TCA-soluble peptide andtrimethylamine (TMA) contents as well as total volatilebase (TVB) of mackerel mince increased while gel-formingability myosin heavy chain band intensity and whitenessdecreased consistently Deterioration lipid oxidation andprotein degradation proceeded as storage time increasedAn increase in deformation and breaking force of surimigel was observed with the addition of 030 commercialtannin or 015 ethanolic Kiam wood extract during the first6 d of storage Therefore commercial tannin and ethanolicKiam wood extract had not shown a gel-enhancing effecton mackerel surimi Furthermore Buamard and Benjakulinvestigated the effects of coconut husk ethanolic isolateson the gel-forming ability of sardine (S albella) surimi [75]Breaking force increasedwith the increasing levels of coconuthusk ethanolic isolates while a decrease in whiteness and nodetrimental effect on the sensory attributes of surimi gel wasobserved It was concluded that the addition of coconut huskextracts at a suitable concentration could enhance the gelstrength of sardine surimi with increased acceptability

25 Compound Additives The effect of different oxidizedphenolic compounds such as tannic acid OTA ferulic acidOFA caffeic acid OCF and catechin OCT on the gellingattributes of mackerel (R kanagurta) surimi was studied byBalange and Benjakul [76] Gels supplemented with 050OTA 040 OFA 010 OCT or 050 OCF showedincreases in deformation and breaking forces while a decreasein the expressible moisture content and myosin heavy chain

band intensity was observed In another study they inves-tigated the effects of oxidized phenolic compounds on thegel-forming abilities of bigeye snapper (P tayenus) surimi[77] An increase in breaking force and deformation witha decrease in expressible moisture contents was observedGels supplemented with the oxidized phenolic compoundshad a finer matrix with smaller strandsThe physicochemicalcharacteristics of natural actomyosin advocate that oxidizedphenolics could trigger the induction of disulfide bondformation or the conformational changes and cross-linkingthrough amino groups Therefore the addition of oxidizedphenolic compounds at an optimum concentration couldenhance the strength of surimi gel

Yongsawatdigul and Piyadhammaviboon reported aninhibition in autolysis of surimi and mince preparedby lizardfish (S tumbil) caused by p-tosyl-L-phenylalanylchloromethyl ketone and phenylmethanesulfonyl fluorideindicating the involvement of myofibrillar-associated serineproteinase Tropomyosin and myosin heavy chain proteinswere mainly hydrolyzed resulting in poor textural prop-erties [26] Arfat and Benjakul investigated the effect ofzinc chloride (ZnCl

2) and zinc sulfate (ZnSO

4) on the gel-

forming abilities of surimi produced by yellow stripe trevally(Selaroides leptolepis) [78] The kamaboko gels with ZnSO

4

added up to levels of 60120583molkg showed increased deforma-tion whiteness and breaking force as well as highly denserand interconnected gels Therefore ZnSO

4at a suitable

concentration could enhance gel strength and whiteness ofdark-fleshed fish surimi

3 Improvement in Quality andFunctionality of Fish-Paste Products

Various food additives from seafood (eg fish invertebratesand seaweed) plants (eg vegetables fruits and herbalmedicines) mushrooms animal sources and functionalmaterials used to improve the quality and functionality offish-paste products are listed in (Table 2) and describedbelow

31 Seafood Additives It has been reported that various typesof seafood namely fish including dried anchovy (Engraulisjaponicus) powder [79 80] pufferfish (Lagocephalus lunaris)powder [88] and skate (Raja kenojei) powder [81 82] andinvertebrates including warty sea squirt (Styela clava) groundflesh [83] its freeze-dried tunic powder [84] omandungi(Styela plicata) ground flesh [85] shrimp (Acetes japonicus)powder [86] and seaweed such as green laver (Ulva spp) [87]have been used to enhance the quality and functionality offish-paste

The boiled and dried Japanese anchovy (E japonicus)is a popular fisheries product in Korea and Japan As theflesh can be eaten together with bone boiled and driedanchovy products are regarded as good sources of calcium[174] Bae and Lee evaluated the properties of fried fish-paste with added anchovy (E japonicus) powder containinga high amount of calcium [79]The fish-paste containing 10anchovy powder displayed the highest values of adhesivenesshardness and strength In the overall acceptance of sensory

14 Journal of Food QualityTa

ble2Naturalfood

additiv

esused

toim

provethe

functio

nalpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Seafoo

dadditiv

es

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

1-2

[79]

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

5[80]

Skate

Rajakenojei

Fried

Hot

wind-dried

skin

and

cartilage

(64)p

owder

Seab

ream

Moistu

recontentcolortextural

andsensoryattributes

3[81]

Skate

Rajakenojei

Steamed

Ferm

ented

flesh

Nemipterusv

irgatus

Aminoacidand

moistu

recontentcolortexturaland

sensoryattributes

20

[82]

Wartyseas

quirt

Styelacla

vaFried

Groun

dflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

5[83]

Wartyseas

quirt

Styelacla

vaFried

Freeze-drie

dtunicp

owder

Frozen

Itoyori

Colortexturaland

sensory

attributes

1[84]

Pleatedseas

quirt

Styelaplica

taFried

Grin

dedflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

15

[85]

Shrim

pAc

etesjaponicus

Fried

Powder

Frozen

seab

ream

surim

iMoistu

recontentcolortextural

andsensoryattributes

5[86]

Green

laver

Ulva

spp

Fried

Powder

Frozen

seab

ream

surim

iColorsensory

attributes

5[87]

Pufferfish

Lagocephalus

luna

risFried

Powder

Nemipterusspp

Moistu

recrude

protein

lipid

colortexturalandsensory

attributes

5[88]

Maesaengi

Capsosiphon

fulve

scens

Fried

Freeze-drie

dpo

wder

Frozen

seab

ream

surim

iColortexturaland

sensory

attributes

5[89]

Redsnow

crab

Chionoecetes

japonicus

Fried

Leg-meat

powder

Frozen

Alaskap

ollock

(Tchalco

gram

ma)

Physiochem

icalandsensory

attributes

6[90]

Plantsou

rcea

dditives

Mulberryleaf

Morus

alba

Fried

Powder

Seab

ream

Colortexturesensory

attributes

05

[91]

Onion

Alliu

mcepa

Fried

Ethano

lextract

Cutla

ssfishpaste

Moistu

recontentTB

CVBN

colorsensoryattributes

3[70]

Lotusleaf

Nelumbo

nucifera

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

05

[92]

Beetroot

andSpinach

Beta

vulga

risand

Spinaciaoleracea

Microwave

inkamaboko

shape

mold

Freshbeet

rootspinach

dish

Not

mentio

ned

Moistu

retexture

analysis

Beetroot10

Spinach15

[93]

Citrus

fruits

Citru

slim

onC

junosC

unshiu

Fortun

ellajaponica

varmargarita

Steamed

Groun

dflesh

pulpwith

out

seeds

Min

Daegu

flesh

Colortexturaland

sensory

attributes

Cumqu

at[94]

Journal of Food Quality 15

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Oatbran

+SiO2

Avenasativa

Boiled

Powder

Frozen

Alaskap

ollock

surim

iColortexturaland

physiochem

icalattributes

6gOatbran10

0gSiO2

[95]

Yam

Dioscorea

japonica

Fried

Powder

Pollo

cksqu

idshrim

pFo

ldingtest

colortexturaland

sensoryattributes

2[96]

WolfberryC

hinese

Goji

Fructuslycii

Fried

Powder

Seab

ream

Texturalandsensoryattributes

3[97]

Redginseng

Pana

xginsengCA

Meyer

Fried

Powder

Not

describ

edColorlipid

oxidation

sensory

attributes

1[98]

Korean

angelicar

oot

Angelicae

gigantis

Radix

Fried

Powder

Seab

ream

Texturalandsensoryattributes

05

[99]

Turm

eric

Curcum

alongaL

Fried

Powder

Pollo

cksqu

idshrim

pColorrheologicalandsensory

attributes

3[100]

Wasabi

Wasabiajaponica

Fried

Freeze-drie

dpo

wder

Silver

pomfre

t(Pam

pusa

rgenteus)

ColorT

BCviablec

ellcou

nt

texturalandsensoryattributes

18

[101]

Wolfip

oriaextensa

Poria

cocos

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

3[102]

Mushroo

madditiv

es

Butto

nmushroo

mAg

aricu

sbisp

orus

Fried

Chop

ped

fresh

Argyrosomus

argentatus

Texturalandsensoryattributes

10

[103]

Enok

imushroo

mFlam

mulina

velutip

esFried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

5[104]

Shiitakem

ushroo

mLentinus

edodes

Fried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

10

[105]

King

oyste

rmushroo

mPleurotuseryngii

Fried

Paste

Silver

whitecroaker(Penn

ahiaargentata)

Texturalandsensoryattributes

10

[106]

King

oyste

rmushroo

mPleurotuseryngii

Steamed

Paste

Cuttlefish

(Sepiaesculen

ta)

Texturalphysio

chem

ical

sensoryattributes

40

[107]

Animalsource

additiv

es

Poultrychicken

Gallusgallus

domesticus

Fried

Breastmeat

batte

r

Itoyori

Japanese

threadfin

bream(Ne

mipterus

japonicus)

Chem

icalcompo

sition

color

fatty

acid

compo

sition

TBARS

sensoryattributes

746

or1493

[108]

Functio

nalfoo

dadditiv

es

Long

-chain

cellu

lose

mdashBo

iled

Powdered

cellu

lose

Alaskap

ollock

surim

iTexturalandrheological

attributes

6[109]

Dietary

fiber

from

ascidian

tunic

Halocynthiaroretzi

Boiled

Refin

eddietaryfib

erAlaskap

ollock

surim

iColortexturalph

ysiological

andsensoryattributes

5[110]

16 Journal of Food Quality

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Fibera

nd120596-3

oil

mdashHeatedin

awater

bath

Powdered

fiber120596

-3oil

Alaskap

ollock

surim

iTexturalandrheological

attributes

Fiber6ndash

10g

and120596-3100

g[111]

Flaxseed

orsalm

onoil

Not

describ

edCoo

kedin

awater

bath

Oil

Frozen

Alaskap

ollock

surim

i(Tchalco

gram

ma)

TBARS

colortexturaland

sensoryattributes

2g10

0gfranks

[112]

Soybeanoil

Glycinem

axHeatedin

awater

bath

Oil

Frozen

silverc

arpsurim

iColortexturalattributes

Soybeanoilgt3

[113]

Calcium

powdero

fcuttlefish

bone

treated

with

aceticacid

Sepiaesculen

taHeatin

gin

awater

bath

Calcium

powder

Alaskap

ollock

surim

iMoistu

recontentcolortextural

andsensoryattributes

009

[114]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Alaskap

ollock

meatp

aste

Colortexturaland

sensory

attributes

017

[115]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Sand

lance

(Hypoptychus

dybowskii)

Acid

andperoxide

valueVBN

sensoryattributes

02

[116]

Cheong

gukjang

Ferm

entedGlycine

max

byBa

cillussp

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

2[117]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 17

evaluation small and large size fish-paste with 1 and 2respectively of added anchovy powder was preferred Thesimilar increasing trend of calcium intensity was observedby Bae et al [80] However the fried fish-paste productscontaining 20 anchovy powder displayed the highest valuesof adhesiveness hardness and strength Regarding overallacceptance in the sensory evaluation the fried fish-pastecontaining 5 anchovy was preferred The optimal amountsof added anchovy in the results from Bae and Lee and Bae etal were different which might have been due to the differentdrying methods and sizes of the anchovies used in each study[79 80] Despite the differences in the two studies the resultssuggest that anchovy powder could be applied to fried fish-paste products to achieve high calcium contents

Skate contains many essential fatty acids includinglinolenic acid linoleic acid arachidonic acid DHA andEPA [175] Skate skin contains high percentages of collagenprotein and calcium [176] while its cartilage is rich inchondroitin sulfate [177] To improve quality and nutrientlevels Cho and Kim prepared fried fish-paste with skate (Rkenojei) powder (hot wind-dried skin and cartilage powder[6 4]) [81] According to Park et al preference testingusing steamed fish-paste product with different levels ofadded 14-day-fermented flesh of skate showed significantincreases in brownness smoothness and skate flavor scores[82] The amino acid contents of fish cake samples with20 skate added had the highest overall preference scoresConsequently the addition of 20 skate powder was optimalfor the steamed fish cake to improve its quality characteristicswith higher protein contents

Warty sea squirt (S clava) aquaculture in the Masanarea of Korearsquos south coast contains abundant unsaturatedfatty acids and essential amino acids in its flesh [178] andglycosaminoglycan in its tunic [179] Warty sea squirt has aunique taste and distinct antioxidant and anticancer activities[180] Fried fish-paste supplemented with 20 warty seasquirt (Korean name miduduk) displayed improved qualityand functionality [83] Choi et al reported a fried fish-paste containing freeze-dried byproduct of warty sea squirt(S clava tunic) [84] The hardness and strength of fish-paste increased with increasing amounts of tunic powderFor overall acceptance in sensory evaluation a fish-pastesupplemented with 1 S clava tunic obtained a relativelyhigher score The results suggested that S clava flesh andtunic could be used for fish-paste products to improve theirquality and functionality Park et al reported improvementin the functional properties of fish-paste by adding S plicata(Korean name omandungi) [85] Fried fish-paste containing20 S plicata indicated the highest values of adhesivenesshardness and strength For overall acceptance in sensoryevaluation a fish-paste containing 15 S plicata obtained thehighest score

Seo and Cho reported the preparation of fish-paste withadded shrimp (A japonicus) powder [86] The hardnessspringiness and cohesiveness increased with the increasingconcentration of shrimp powder However the brittlenessand gumminess reduced In the sensory evaluation the fish-paste prepared with 5 shrimp powder was most preferredCho and Kim reported the preparation of fish-paste with

added green laver (Ulva spp) powder [87] The hardnessspringiness and cohesiveness increased with the increasingconcentration of green laver powder However the brittlenessand gumminess decreased upon the addition of green laverpowder In the sensory evaluation a fish-paste prepared with5 green laver powder was preferred over other fish-pastesThese results suggest that green laver powder could be appliedto fish-paste to improve its quality and functionality

Pufferfish containing taurine hydroxyproline lysine andglycine impart a characteristic taste to food [181] To improvethe taste of fish-paste products Park prepared a fish-pasteby adding green rough-backed pufferfish (L lunaris) pow-der [88] The hardness strength gumminess springinessand chewiness of the fish-paste increased depending onpufferfish powder contentThe preparation of fish-paste withadded Capsosiphon fulvescens powder was reported by Park[89] The hardness springiness strength and cohesivenessincreased with the increasing concentrations of C fulvescenspowder However the brittleness and gumminess reducedwith the addition of C fulvescens powder In the sensoryevaluation overall the fish-pastes prepared with 5 Cfulvescens powderwere preferred over other fish-pastesThusthe results show that C fulvescens powder could be used tocreate fish-paste products with high quality and functionality

Kim et al reported the changes in the sensory and physic-ochemical properties of a fish-paste containing red snow crab(Chionoecetes japonicus) leg-meat powder [90] Hardnessgumminess springiness and cohesiveness increased withincreasing levels of red snow crab leg-meat powder Based onthe sensory evaluation it was concluded that the addition ofred snow crab leg-meat powder at a level of 6 could improvethe quality characteristics of fish-paste products

32 Plant Source Additives It has been reported that variousplant sources namely vegetables (eg mulberry beetrootand spinach) fruits (eg citrus) and herbal medicines (egChinese matrimony vine Korean Angelica root) have asignificant effect in improving the quality and functionalityof fish-paste products

Mulberry (Morus alba) leaf has been used traditionallyto treat a disease symptomized by thirst and stroke [182]Ever since mulberry leaf was included as a food material inthe Food Codex in 1988 by the Ministry of Food and DrugSafety (MFDS Osong Chungju South Korea) Mulberry leafpowder has been used in various processed food productsand health functional foods Shin and Park reported theuse of mulberry leaf powder in the preparation of fish-pasteproducts [91] In a texture meter test the hardness increasedbut the cohesiveness springiness gumminess and brittlenessdecreased with increasing levels of mulberry leaf powder Insensory evaluation the fish-paste with 05 mulberry leafpowder revealed the highest acceptance scores in terms offlavor texture and overall quality

Garden onion (bulb onion Allium cepa) is a perennialplant belonging to Liliaceae and is widely used as a spice andseasoning vegetable in both the East and the West Park etal investigated the quality characteristics of fried fish-pastesupplemented with flavonol-rich ethanol extract of onion[183] In the sensory evaluation as the amount of ethanol

18 Journal of Food Quality

extract of onion increased so did the favorability in termsof flavor and taste Notably 3 ethanol extract of onion hadthe best score in overall acceptance The results indicate thatethanol extract of onion can be used to prepare fried fish-paste products with high quality and functionality

Shin reported the production of fish-paste with addedlotus (Nelumbo nucifera) leaf powder [92] The flavor adhe-siveness and hardness increased with the increasing levels oflotus leaf powder The fish-paste with 05 lotus leaf powderdisplayed the highest acceptance scores in terms of springi-ness pleasant taste appearance texture flavor and overallquality Thorat et al prepared kamaboko containing greenchili coriander ginger garlic spice mixture and groundbeetroot or a spinach dish and then subjected the preparationto microwave cooking [93] Kamaboko prepared with 10beetroot and a 15 spinach dish was found to be superior tothe others

Yang and Cho developed a steamed fish cake with added5 ground citrus fruits with skin [94] The addition of citrusfruits did not disturb the flexibility of surimi The pH ofsurimi samples increased in the following order lemon (Cit-rus limon) citron (Citrus junos) tangerine (Citrus unshiu)kumquat (Fortunella japonica var margarita) and controlThe hardness of surimi was highest for lemon followed bycitron tangerine kumquat and control surimi In the sensoryevaluation surimi containing kumquat demonstrated higherscores in terms of color taste and textural properties Theseresults suggest that surimi could be prepared by adding citrusfruits to improve the quality and functionality

Oat bran is a gluten-free dietary fiber that may decreasethe risk of diabetes and heart diseases The physicochemicalproperties of surimi gels supplemented with oat bran werestudied by Alakhrash et al [95] The oat bran and SiO

2

incorporation (6 g100 g) greatly improved water-holdingcapacity and gel texture while a reduction in whiteness wasobserved Kim and Byun conducted tests on the sensoryand physicochemical characteristics of fish-paste with addedyam (Dioscorea japonica) powder [96] The addition of yampowder increased gumminess strength springiness andcohesiveness In the sensory evaluation the addition of 2yam powder had the best scores in terms of taste color andoverall preference

Fructus lycii is a fruit produced by Lycium barbarumL that has been used for nourishment tonicity and nour-ishment of the blood it has antibacterial anticancer andantioxidant properties [182ndash186] Shin et al prepared friedfish-paste containing dried F lycii powder [97] In the texturalanalysis cohesiveness increased while brittleness and gum-miness decreased with increasing levels of F lycii powderThe 3 F lycii powder sample had the highest acceptancescores in terms of appearance texture taste flavor andoverall acceptability

Red ginseng-based fried fish-pastes containing differentsizes and amounts of red ginseng powder were preparedand their biological properties including lipid oxidation toimprove fish-paste quality were investigated [98] The fish-paste products containing red ginseng powder showed asignificant increase in hardness and chewiness Furthermorean inhibitory effect on lipid oxidation and reduced number

of total microbes during storage were observedThese resultssuggest that high-quality fish-pastes could be achieved withthe addition of 1 red ginseng powder which effectivelyimproved both sensory evaluation and physicochemicalproperties

Angelicae Gigantis Radix (the dried root ofAngelica gigasNikai) more popularly known as Korean Angelica is one ofthe widely used herbal medications [187] It has been usedin Korean medicine as an important medication for anemiaand blood circulatory disorders It has also been used formenstrual pains and postmenopausal syndromes Shin et alreported the development of fish-paste with A gigas powder[99] In a texture test hardness chewiness and brittlenessincreasedwith increasing concentrations of AngelicaeGigan-tis powderHowever cohesiveness and springiness decreasedIn the sensory evaluation the fish-paste with 05 AngelicaeGigantis powder showed the highest acceptance scores forappearance flavor taste texture and overall quality

Turmeric (Curcuma longa) has been used in Ayurvedicmedicine from ancient times as a treatment for inflammatoryconditions It has been reportedly used for its various bio-logical activities including antibacterial antiviral antifungalantioxidative and antiatherogenic effects [188] Turmeric hasbeen grown as a special crop in the central and southern areasaround Jindo in South Korea [189] Choi et al investigatedthe sensory and rheological properties of fish-paste preparedwith turmeric powder [84] In terms of textural attributesthe addition of C longa powder decreased springiness andimproved strength In the sensory evaluation the addition of3 C longa powder was associated with the best scores fortaste and overall preference

Wasabi (Wasabia japonica) has various beneficialhealth properties including antioxidative antimicrobialand antimutagenic activities [190 191] Jang et al reporteda high-quality fried fish-paste product made with silverpomfret (Pampus argenteus) which is one of the savorysoft and delicious types of fish prepared by adding wasabipowder [101] Notably hardness gumminess and chewinessincreased significantly with the addition of wasabi powderIn the sensory evaluation 18 wasabi powder showed thebest score in overall acceptability These results show thatwasabi could be used as a food additive or preservative infish-paste products

White Poria cocos wolf is the inner white part of P cocosa parasite found on Pinus densiflora It is used to treat edemachronic gastritis gastric atony nephrosis acute gastroentericcatarrh emesis dizziness and vomiting [192 193] Shin et alprepared a fried fish cake with added white P cocos powderand studied the textural and sensory characteristics [102]In texture tests brittleness was observed to increase whilespringiness decreased with increasing concentrations of Pcocos powder The fish-paste product containing 3 whitePoria cocos powder showed the highest acceptance scores forflavor appearance texture taste and overall quality

Milk-vetch root is one of the most produced herbalmedicines in Korea It is a peeled and dried root of the herba-ceous perennial herb known as Astragalus membranaceuswhich belongs to the Fabaceae family [194] It has been

Journal of Food Quality 19

reported that milk-vetch root exerts diuretic tonic anti-hypertensive hypoglycemic immune-enhancing antitumorand antiviral effects [195] Kim investigated the sensoryand physicochemical properties of fish-paste prepared withmilk-vetch root powder [196] The strength cohesivenessbrittleness and gumminess of the fish-paste increased whileits springiness decreased with an increasing amount of milk-vetch root powder In the sensory evaluation the addition of10 milk-vetch root powder indicated best scores for tastetexture color and overall preference

33 Mushroom Additives Mushroom is a nutritional andfunctional food as well as a vital source of physiologicallybeneficial medicines Mushrooms have been used as tradi-tional medicines in Korea Japan China and other Asiancountries for curing various diseases including lymphaticdisease gastroenteric disorder oral ulcer and various can-cers [197] It has been reported that edible mushrooms inKorea number approximately 350 species [198] Several ediblemushrooms that are highly preferred have been added to fish-paste to enhance their quality and functionality

Ha et al prepared a fried fish-paste product with addedAgaricus bisporus which is a product described as having aracy flavor and taste [103]The elasticity hardness brittlenessand gumminess of fish-paste with the added mushroomincreased however no significant difference in strengthwas observed Regarding overall acceptance in a sensoryevaluation a fish-paste supplemented with 10 A bisporusmushroom showed the highest scores

Enoki mushroom (Flammulina velutipes) is well knownfor its anticarcinogenic and blood pressure-reducing prop-erties To utilize its functional properties enoki mushroomwas added to fried fish cake [104] The sample containing15 mushroom received the highest values for strengthgumminess and brittleness In the sensory evaluation thefish cakes with 5 mushroom obtained favorable scores foroverall acceptance

Shiitake mushroom (Lentinus edodes) is known for itshigh level of 120573-glucans Son et al investigated the effectsof shiitake mushroom on the textural properties of friedfish cake [105] The fish cake containing shiitake mushroomreceived the highest values for strength hardness gummi-ness and brittleness In the sensory evaluation the fish cakeswith 10 shiitake mushroom sample obtained the best scorefor overall acceptance

Kim et al prepared a fried fish cake using cultured kingoyster mushroom (Pleurotus eryngii) and silver white croaker(Pennahia argentata) surimi to enhance its physiologicaleffects [106] In assessing its quality properties fish cake towhich 10 mushroom was added received the highest valuesfor strength hardness gumminess and brittlenessThe effectof king oyster mushroom on the textural and physicochem-ical properties of steamed cuttlefish (Sepia esculenta) fishcake was investigated by Chung et al [107] The fish-pastewith added king oyster mushroom paste revealed significantdecreases in gumminess cohesiveness and hardness whilethe springiness increased with increasing concentrations ofking oystermushroompasteOn the sensory evaluation basisthe cuttlefish-paste supplemented with 30ndash50 king oyster

mushroom showed higher overall acceptability In the studiesby Kim et al and Chung et al the optimal amounts of kingoyster mushroom differed which might have been due tothe different cooking methods and surimi used in each study[106 107]

34 Animal Source Additives Jin et al investigated the effectof chicken meat on the quality characteristics of Itoyori(Japanese threadfin bream Nemipterus japonicus) surimi[108] The physicochemical properties such as fatty acidcomposition shear force and gel characteristics were affectedby substitution with spent laying hen meat batter Howeversensory characteristics were less affected by this substitutionA huge amount of waste in the processing of grass carp isdiscarded To deal with this waste Gao et al studied theprocessing technology used for fish and mushroom pastewith salted fish cubes mushroom soybean and fermentedsoybeans [199]

35 Functional Food Additives Functional food additivesincluding dietary fiber 120596-3-rich oil calcium additives andpropolis have been used in the preparation of fish-pasteproducts to increase their quality and functionality Westernpopulations have an inadequate quantity of health beneficialdietary fiber in their diets Besides fiber most Western pop-ulations also consume an insufficient amount of 120596-3 PUFAswhile their sodiumconsumption greatly surpasses the recom-mended maximum Debusca et al prepared Alaska pollocksurimi fortified with commercial long-chain cellulose as asource of dietary fiber [109] Fiber fortification up to a level of6 improved both texture and color a slight decline in thesevalues was observed at levels of 8 fiber An increase in gelelasticity and thermal gelation of the fish cake was observed

Yook et al prepared a fish-paste by adding dietaryfiber extracted from ascidian (Halocynthia roretzi) tunic toenhance its physiological properties [110] The hardnessgumminess adhesiveness shear force and chewiness of thefish-paste improved with the incorporation of the ascidiandietary fiber The fish-paste with 5 ascidian dietary fiberscored the highest and was generally preferred by sensorypanels Tolasa et al reported that the oxidative stability andthe uniform dispersion of 120596-3 unsaturated fatty acids can beattained in a highly consistent surimi gel system without theuse of antioxidants [200]

Surimi and surimi-based products are famous through-out the world In fact US consumption increased in the1980s while the rate leveled off thereafter The nutrificationof food products with 120596-3 PUFAs increases the health ben-efits of food consequently increasing their market demandPietrowski et al prepared surimi seafood products nutrition-ally enhanced with 120596-3 PUFAs [201] Although the nutrifica-tion of 120596-3 PUFAs indicated an increase in lipid oxidationit was within limits acceptable to consumers The color ofsurimi seafood nutrified with 120596-3 PUFAs generally improvedbut no effect on textural characteristics was observed

Debusca et al reported that the fortification of Alaskapollock surimi with either 120596-3 oil or dietary fiber alone orin combination improved both the textural and rheologicalproperties [111]The120596-3 oil and fiber in combination revealed

20 Journal of Food Quality

greater gelation of surimi and a slight reduction in color prop-erties indicating their interaction with myofibrillar proteinsThus it was suggested that the 120596-3 oils and fiber could beeffectively used as a fortifying agent to prepare high-qualitysurimi products with nutritional benefits Sell et al preparedsurimi franks fortified with salmon oil or flaxseed [112]The textural properties showed differences between franktypes with the flaxseed franks being cohesive less gummysofter and chewy while the sensory evaluation showed nosignificant differences

Chang et al determined the effects of soybean oil andmoisture contents on the physical properties of surimi gels[113] The increasing levels of soybean oil and moisturecontents resulted in an increase in whiteness and reductionin the chewiness hardness and breaking force Setting incombination with soybean oil improved the textural andcolor parameters of surimi gels indicating that soybean oilcould be used to improve the color and textural properties ofsurimi seafood products

Kim et al prepared boiled fish cake using acetic acid-treated cuttlefish bone as a calcium additive agent [114] Theresults of sensory evaluation of texture and whiteness weresimilar to those without this supplementation In the mineralcontent analysis of heat-induced surimi gel calcium contentincreased depending on the increasing concentration ofacetic acid-treated cuttlefish bone powder while phosphoruscontent did not change The optimal concentration of aceticacid-treated cuttlefish bone powder for the preparation ofhigh-quality heat-induced surimi gel was 009

Kim et al prepared Alaska pollock fried fish-pastesupplemented with propolis [115] The addition of propolisenhanced the antispoiling and antioxidative ability as well asgel strength of fried fish-paste In the sensory evaluation theaddition of 017 propolis showed the best score in overallacceptability In another study Kim et al later studied sand-lance (Hypoptychus dybowskii) meat paste prepared withpropolis [116] Similar to the previous report the addition ofpropolis on the fried fish-paste showed higher antioxidativeand antispoiling activities The fried sand-lance meat pasteprepared with 02 added propolis was the most acceptableFurthermore the bitter taste of the sand-lancemeat paste wasreduced by adding 2 sweet amber powder

Cheonggukjang is an ancient Korean food prepared byfermented soybean It contains high levels of dietary fiberoligosaccharides isoflavones saponin lecithin phytic acidand phenolic compounds among others Its many benefi-cial properties have been reported such as thrombolyticanticancer antimicrobial hepatoprotective antioxidant andcholesterol-lowering effects [202] Park et al reported theuse of fish-paste containing cheonggukjang powder [117]Theincreasing concentrations of cheonggukjang resulted in anincreased value of springiness cohesiveness and hardnesshowever a reduction in brittleness and gumminess values offish-paste was observed

4 Shelf-Life Extension of Fish-Paste Products

Fish-paste products may easily spoil due to residualmicrobes that are not removed by sterilization during the

manufacturing process or by contamination in packagingor the distribution process For such reasons even vacuum-packed fried fish-paste products have a shelf-life of fewerthan 10 days during cold storage which is relatively short[121 122] Various efforts have been made to develop long-term storage solutions for fish-paste products via physicaland chemical methods [118ndash122] Although these methodswere found to be very effective for the long-term storageof fish-paste products they require sensitive and complexmanipulation and are costly

The addition of appropriate food additives to fish-pasteproducts as an effective preservation protocol is anotherstrategy Potassium sorbate is a typical synthetic food preser-vative and is commonly used in processed foods includingfish-paste productsThis material is effective in inhibiting thegrowth of variousmicroorganisms as it has a slight sterilizingeffectThe use of this material is permitted to a concentrationof less than 20 gkg in processed fish meat products (FoodCode Ministry of Food and Drug Safety Republic of Korea)According to the results of Walker sorbates and sorbic acidexert a very low level of mammalian toxicity even in chronicstudies as up to 10 of the diet did not show any carcinogenicactivity [203] In addition Thakur and Patel summarizedthe application of sorbates in the shelf-life extension of fishand fish-based products [204] The physical and chemicalmethods along with natural food preservatives for the long-term storage of fish-paste products are listed in Table 3 andbriefly described below

41 Physical and Chemical Methods Various efforts havebeen focused on developing long-term storage solutions forfish-paste products via physical methods including highpressurization [118] microwave pasteurization [93] highhydrostatic pressure treatment [119] and even irradiation[118 121] In addition it has also been reported that treatmentwith chlorine dioxide solution at an appropriate concentra-tion which is harmless to humans could be used to preventspoilage and to extend the shelf-life [122]

High hydrostatic pressure technology has graduallygained popularity in the food industry over the last twodecades [205] In 2013 the worldwide market for highhydrostatic pressure equipment was estimated to be $350million and it is expected to grow Besides high hydrostaticpressure technologies several types of radiation have alsobeen tested including ultraviolet microwaves and gammairradiation treatments Radiation is generally used to controlbiological hazards in the production of fish-paste productsand to prolong the shelf-life of such products [206 207]Gamma radiation exerts potent antimicrobial effects whereasultraviolet rays are effective for the surface but not interiorsterilization of porous dried fish products (eg fish-pasteproducts) However gamma irradiation treatment demandslarge-scale facilities and higher costs [207 208]

Miyao et al reported that growth of the majority of thepathogenic microorganisms present in surimi was inhibitedat a high pressure of between 300 and 400Mpa [118] Severalpressure-resistant strains were isolated from surimi and wereidentified as Moraxella sp Acinetobacter sp Streptococcusfaecalis and Corynebacterium sp It was suggested that

Journal of Food Quality 21

Table3Naturalfood

additiv

esandph

ysicochemicalmetho

dsused

toim

provethe

shelf-life

offish-paste

prod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Physicalandchem

icalmetho

ds

Highhydrostatic

pressure

mdash

High-pressure

treatmento

rheattre

atment

insampletub

ewith

vacuum

packaging

mdashFrozen

Alaskap

ollock

Microbialactiv

ity40

0MPa

[118]

Highhydrostatic

pressure

mdashNot

cooked

mdash

Tuna

fishpaste

Mackerelp

astewith

paprika

mackerelp

astewith

garlic

mackerelp

astealon

eand

salm

onpaste

Microbialactiv

ity200M

Pa[119]

Co-60

Gam

mar

ays

mdashGrilled

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

texturalsensorym

icrobial

physiochem

icalattributes

75kG

y[120]

Co-60

Gam

mar

ays

mdashFried

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

pHtexturalmicrobial

physiochem

icalattributes

3kGy

[121]

Chlorin

edioxide

(ClO2)

mdashSteamed

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

VBN

TBA

RSpHm

icrobial

physicochemicalsensory

attributes

50pp

m[122]

Naturalfood

additiv

esRe

dpepp

erethano

lextract(RP

EE)

andchop

pedfre

shredpepp

er(C

FRP)

Capsicu

mannu

umFried

Ethano

lextract

andchop

ped

fresh

one

Frozen

Alaskap

ollock

TBC

sensoryattributes

RPEE

10

CF

RP5

[123]

Ethano

lextract(EE)

andwater

extract

(WE)

Phellodendron

amurense

Eugenia

caryophyllu

sPinu

srigida

Bletillastr

iata

andPa

eonia

albiflora

mdashmdash

mdashAntim

icrobialattributes

onpu

trefactiveisolatesfrom

fish

meatp

asteprod

ucts

EE2000

ppm

[124]

Eggwhitelysozyme

(EWL)

andor

sodium

hexametapho

sphate

(SHMP)sod

ium

pyroph

osph

ate(SP

P)

Gallusgallus

domesticus

Fried

Powder

Frozen

Alaskap

ollock

Viablecellcoun

tpH

VBN

biochemicalattributes

EWL5

+SP

P05

+SH

MP

01

[125]

Grapefruitseed

extract

Citru

sparadisi

mdashSolutio

nCom

merciallyavailablefi

shmeat

paste

prod

ucts

Proxim

atec

ompo

sition

textural

biochemicalrheologicalsensory

attributes

1000

ppm

[126]

22 Journal of Food Quality

Table3Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Cinn

amon

bark

extract

Cinn

amom

umcassia

Fried

Extracted

solutio

nFrozen

Alaskap

ollock

Antim

icrobialactiv

itySprayeddiluted

extract(11)

[127]

Alginicacid

hydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Relativev

iscositypHcolor

rheologicalattributes

03

[128]

Chito

sanhydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Viablecellcoun

tsrheological

sensoryattributes

03

[129]

Nisin(N

)and

or

sucrosefattyacid

esters(SFE

)mdash

Steamed

Powdera

ndsolutio

nFrozen

Alaskap

ollock

Viablecellcoun

tantim

icrobial

activ

ityN125120583

gg+

SFE10mg

[130]

Piscicolin

KH1

Carnobacteriu

mmaltalomaticu

mSteamed

Solutio

nCod

fish

Inhibitory

assayproteincontent

antim

icrobialactiv

ity50

AUg

[131]

Zein

andsoyprotein

isolate(SPI)fi

lms

containing

greentea

extract(GTE

)

Zeamays

Glycinem

axCa

melliasin

ensis

Fried

Ediblefilm

(GC-WPI)w

ithGTE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

TBARS

colorm

icrobial

physicalattributes

GTE

1

[132]

Gelidium

corneum

(GC)

-Wheyprotein

isolate(G

C-WPI)

blendfilm

containing

grapefruitseed

extract(GSE

)

Gelidium

corneum

Citru

sparadisiBo

staurus

Not

mentio

ned

Ediblefilm

(GC-WPI)w

ithGSE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

Water

vapo

rpermeability

microbiologicalanalysis

sensory

attributes

GSE

01

[133]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 23

damage to the cell membrane and degradation of ribonucleicacids occurred in the high-pressure-treated cells Malickiet al investigated the use of high hydrostatic pressure toprolong the shelf-life of traditionallymanufactured fish-pastestored under refrigeration (4∘C) for 6 weeks [119] Neitherbacteria nor molds or yeasts were detected in the highhydrostatic pressure-treated fish-paste samples at any timepoint analyzed irrespective of the pressurization conditionsIn conclusion these studies revealed the effectiveness of highhydrostatic pressure to prolong the shelf-life of traditionallymanufactured fish-paste stored under refrigerated conditionsfor up to 6 weeks

Kim et al reported a reduction in the total aerobicbacterial counts in the grilled fish-paste stored at 5∘C andirradiated by gamma rays at a level of 25 kGy or more[120] Additionally the treatment of gamma rays at a levelof 75 KGy at 30∘C showed a significant inhibition in aerobicbacterial growth Cho et al investigated the effect of Co-60 gamma irradiation on fried fish-paste and studied thephysicochemical properties of fish-paste products stored atlow temperature (3 plusmn 1∘C) and room temperature (10ndash20∘C)[121] There was no obvious difference between the vacuum-and air-packed groupsThe irradiation of 3 KGy extended theshelf-life of fish-paste up to 2 times at room temperature and3-4 times at low temperature In both studies the irradiationtreatment caused very little textural degradation and no effecton the sensory characteristics of the samples was observed

Shin et al investigated the effects of chlorine dioxide(ClO2) treatment on the physiochemical andmicrobial prop-

erties of fish-paste products [122] After ClO2treatment

fish-paste samples were individually packed and stored at4∘C The pH and VBN values of fish-paste decreased withincreasing ClO

2concentration ClO

2treatment significantly

reduced the populations of total bacteria yeast and moldduring storage In particular treatment with 50 ppm ClO

2

significantly decreased the total bacterial count the mostamong all ClO

2-treated fish-pastes showing that 50 ppm

chlorine dioxide was the optimum concentration to prolongthe shelf-life of fish-paste products

42 Natural FoodAdditives Theuse of natural food preserva-tives rather than chemical and synthetic food preservatives isofworldwide interest It has been reported that several naturalfood additives could extend the shelf-life of cooked fish andfish products Some examples include onion ethanol extract[183] egg white lysozyme [125] grapefruit seed extract [126]chitosan hydrolysate [129] cinnamon bark extract [127] andred pepper extract [123] as well as mixtures of lysozymessodium hexametaphosphate and sodium pyrophosphate

The shelf-life of fried fish-paste products prepared byadding red pepper ethanol extract was estimated by Yoonet al [123] The shelf-life of the fried fish-paste with added10 red pepper ethanol extract and 5 chopped fresh redpepper was 2 to 3 days longer than that of the commercialfish-paste product thus demonstrating the most effectivepreservation effects According to Ahn et al the extractsof Eugenia caryophyllus Pinus rigida Bletilla striata andPaeonia albiflora exerted strong inhibitory effects on thegrowth of microorganisms isolated from putrefied fish-paste

[124] Notably the ethanol extract was more effective thanwater extract in all tested microorganisms The inhibitionlevel of each extract was evident at 2000 ppm ethanol in thefish-paste

Kim et al investigated the inhibitory effects of lysozymesmixtures of lysozymes and other antibacterial substancessuch as sodium pyrophosphate and sodium hexametaphos-phate on bacterial growth in surimi products [125] Thelysozymes inhibited growth in most of the tested isolatesand themixture of antibacterial substances showed increasedeffects compared with those when they were used individ-ually A mixture of 05 sodium hexametaphosphate 05sodium pyrophosphate and 005 lysozyme in imitationcrab and kamaboko showed the highest inhibitory activ-ity

The stabilizing effects of grapefruit seed extract on fish-paste products were investigated by Cho et al [126] Texturalproperties decreased with increasing storage period Thetreatment of fish products with grapefruit seed extract pro-longed the deterioration of fish-paste product proteins duringstorage up to 4-5 daysThe chemical sensory and rheologicalevaluation revealed that the grapefruit seed extract could beused as an effective additive to extend the shelf-life of fish-paste products

The predominant bacterium in most of the isolatedmicroorganisms from packed and unpacked spoiled fish-paste products is Bacillus sp [127] Notably yeast andmolds are not reported in the vacuum-packed products Ahydrolysate of alginic acid has antimicrobial activity but ithas not been used at industrial scale The alginic acid ata concentration of 03 prolonged shelf-life of fish-pasteproducts by 4 days at 15∘Cand inhibited the growth ofBacillussp isolated from fish-paste products [128] According to theresults of Cho et al the chitosan hydrolysate made withchitosanase from Aspergillus oryzae ATCC 22787 revealedthe strongest antimicrobial activity and inhibited the growthof Bacillus sp isolated from fish-paste products [129] Theaddition of chitosan hydrolysate at a concentration of 03resulted in extended shelf-life of up to 6 days at 15∘C Jeonget al reported that spraying cinnamon bark extract on thesurface of the fried fish-paste products could inhibit thegrowth of spoilage bacteria and mold at room temperatureand resulted in prolonged shelf-life [127]

Yamazaki et al investigated the effects of nisin andsucrose fatty acid esters on the growth of spoilage bacteria infish-paste products [130] Nisin exerted antibacterial activityagainst Bacillus subtilis and Bacillus licheniformis in a liquidmedium at 20∘C and resulted in a longer shelf-life forfish-paste products It was concluded that the addition ofnisin could be used as a potential alternative method toprevent spoilage caused by spore-forming bacteria in fish-paste productsThe bacteriocin produced byCarnobacteriummaltalomaticum had the ability to inhibit both Enterococcussp and Leuconostoc sp which reduce the shelf-life of fish-paste products during preservation [131] The results showedthat the purified bacteriocin piscicolin KH1 andor nisin sig-nificantly inhibited the growth of Leuconostoc mesenteroidesand Enterococcus faecium and could be used as a food-gradepreservative for kamaboko gels

24 Journal of Food Quality

Sakai and Yamaguchi examined the possibility of inhibit-ing lipid oxidation in boiled fish-paste by adding yuzu skinto the surimi [209] The heat-treated control kamabokoand yuzu skin-added kamaboko (citron kamaboko) wererefrigerated at 0∘C for 2 days and after heating the surimithe malonaldehyde content in both kamabokos was reducedThese results suggest that the addition of citron skin sup-pressed lipid oxidation in fish-paste products

Various packing materials and wrapping techniques havealso been employed to keep fish-paste products fresh and freeof contaminants for a longer period of time Lee et al investi-gated the processing conditions and quality stability of retortpouched fried-mackerel fish-paste during storage [210] Themackerel fish-paste was ground with added ingredients friedin soybean oil cooled vacuum-packed in a laminated plasticfilm and finally sterilized at 120∘C for 20min in a hotwater circulating retortThe reported method showed a goodpreservation for 100 days at 25 plusmn 3∘CThe sensory evaluationshowed no significant differences between the prepared fish-paste products and that of products in the market Ha et alexamined the optimum storage conditions for maintainingthe quality of the fried fish-paste in retort pouches [211]Both hardness and gel strength increased with increasingsterilization temperature On the other hand no differenceswere observed in elasticity and water-holding capacity

Lee et al elucidated the antioxidative effects of soyandor zein protein films containing green tea extract on thephysiological properties of fish-paste products during storage[132]The soy protein films showed an increase in yellownesswhile a decrease in yellowness was observed with the zeinfilms The lipid oxidation was retarded at day 2 of storageby wrapping the fried fish-paste products with soy and zeinprotein films containing green tea extract Lim et al prepareda Gelidium corneum whey protein isolate (GC-WPI) blendfilm containing grapefruit seed extract and studied the effectof this film on pathogenic bacterial inhibition during storage[133]TheGC-WPI blend was effective in decreasing the pop-ulations of Salmonella typhimurium Listeria monocytogenesand Escherichia coli on films treated with 01 grapefruitseed extract These studies suggest that packaging fish-pasteproducts in plant-based protein films containing green tea orgrapefruit seed extract could be beneficial to prolong shelf-life

5 Conclusion

The production of surimi dates back to ancient times How-ever advancement in surimi processing technology startedin 1960 with the discovery of cryoprotectants which werehelpful in maintaining the gel quality and functionality offish-paste for relatively longer periods of frozen storage [3]As themarket share of quality-conscious consumers rises thedemand for the use of natural additives rather than chemicalingredients for surimi products will continue to increaseAccording to Park et al the worldwide production of surimi-related products reached around 800000MT by 2011-2012while the main fish sources for surimi products includePacificwhitingAlaska pollock jackmackerel Atkamackerelsouthern blue whiting northern blue whiting and hoki [3]

Surimi is subdivided into high-grade (FA SA and A) andlow-grade (KA KB and RA) types based on the quality ofthe raw fish sources Most of the high-grade surimi is soldin Japan for the production of kamaboko and other high-quality surimi products and in Korea for the production ofpremium crabsticks Low-grade surimi is sold in Europe andthe United States for the manufacturing of crab sticks andin Korea and Japan for the preparation of other fried fishproducts [3] With the technological advancements in thesurimi processing industry it has been possible to use low-grade surimi for the production of fish cakes fish balls andother surimi products

With increasing demand and new processing techniques(eg the pH-shift method) the use of other seafoodresources such as small pelagic species and giant squid forthe production of surimi and surimi products was possible[212] Notably the production of surimi products is cheaperinKorea than elsewhere but industry professionals are alwayssearching for the most inexpensive surimi seafood sourcesHence the production of surimi from aquaculture fish suchas catfish and carp is growing in demand

Food additives from animal and seafood sources suchas fish chicken beef plasma proteins and egg white areconsidered the most effective protease inhibitors for surimiHowever with the outbreak of avian influenza mad cow dis-ease undesirable resulting characteristics and some religiousconstraints there is limited use of these food additives Addi-tionally vegetarians in some parts of the world would notwish to consume surimi-based products containing additivesderived from animals or even from seafood sources Hencethere is a need to identify more effective and alternative food-grade ingredients (eg plant sources seaweed and microal-gae) to be used in the preparation of fish-paste products

Surimi is mainly used for human consumption As suchthe challenges of production cost composition nutritionalvalue and the shelf-life of surimi products can never beneglected This review has provided an overview of nat-ural and synthetic food additives and preservatives usedto enhance the quality functionality and shelf-life of fish-paste products In addition the improvements in the fish-paste product quality and functionality by various foodadditives from seafood plants mushrooms animal sourcesand functional materials were discussed

For decades surimi and surimi-based products have beenwell known in East Asian countries such as Japan and KoreaHowever with advancements in technology they are attract-ing attention in other Asian as well as European countriesWith the increasing consumption worldwide the manufac-turing and processing of fish-paste products may requirenew and improved additives to enhance their acceptability inthe market Continuous scientific innovations and improvedprocessing technology will aid in further advancements andimprovements in this area

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article and regarding thefunding received

Journal of Food Quality 25

Authorsrsquo Contributions

Khawaja Muhammad Imran Bashir and Jin-Soo Kim con-tributed equally to this work

Acknowledgments

This research was a part of the Project no PJT200885entitled ldquoDevelopment andCommercialization of TraditionalSeafood Products Based on the Korean Coastal MarineResourcesrdquo funded by the Ministry of Oceans and FisheriesSouth Korea

References

[1] H-J Hwang S-Y Choi and S-C Lee ldquoPreparation andquality analysis of sodium-reduced fried fish cakesrdquo PreventiveNutrition and Food Science vol 18 no 3 pp 222ndash225 2013

[2] KFDA Food code Article 1-5-12 Korea Food and Drug Admin-istration Seoul Korea 2012

[3] J W Park H Nozaki T Suzuki and J-L Beliveau ldquoHistoricalreview of surimi technology and market developmentsrdquo inSurimi and Surimi seafood J W Park Ed pp 3ndash24 CRC PressNew York NY USA 2013

[4] J A Ramırez R Dıaz-Sobac O G Morales and M VazquezldquoEvaluation of freeze-dried surimi from tilapia and fat sleeper asemulsifiers [Evaluacion de surimi liofilizado de tilapia y dormi-dor como emulsificantes evaluacion de surimi liofilizado detilapia e dormidor como emulsificantes]rdquo Ciencia y TechnologiaAlimentaria vol 2 no 4 pp 210ndash214 1999

[5] J M Aguilera and D W Stanley ldquoFood structuringrdquo inMicrostructural Principles of Food Processing and Engineeringvol 12 p 246 AN Aspen Publishers Gaithersburg MarylandUSA 1999

[6] A P Stone and D W Stanley ldquoMechanisms of fish muscle gela-tionrdquo Food Research International vol 25 no 5 pp 381ndash3881992

[7] S Nakamura and M Ogawa ldquoBiomolecular strategies forpreparation of high quality surimi-based productsrdquo PreventiveNutrition and Food Science vol 10 no 2 pp 191ndash197 2005

[8] M Okada ldquoHistory of surimi technology in Japanrdquo in Surimitechnology T C Lanier and C M Lee Eds pp 3ndash22 MarcelDekker Inc New York NY USA 1992

[9] MIFAFF ldquoStatistics of fisheries processingrdquo Ministry of FoodAgriculture Forestry and Fisheries Seoul Korea 2011

[10] T C Lanier ldquoMeasurement of surimi composition and junc-tional propertiesrdquo in Surimi technology T C Lanier and C MLee Eds pp 123ndash166 Marcel Dekker Inc New York NY USA1992

[11] K-H Chung and C-M Lee ldquoRelationships between physico-chemical properties of nonfish protein and textural propertiesof protein-incorporated surimi gelrdquo Journal of Food Science vol55 pp 972ndash975 1990

[12] M TMorrissey JWWuD Lin andHAn ldquoProtease inhibitoreffects on torsionmeasurements and autolysis of Pacific whitingsurimirdquo Journal of Food Science vol 58 no 5 pp 1050ndash10541993

[13] J W Park ldquoFunctional protein additives in surimi gelsrdquo Journalof Food Science vol 59 no 3 pp 525ndash527 1994

[14] S Benjakul W Visessanguan and C Srivilai ldquoGel propertiesof bigeye snapper (Priacanthus tayenus) surimi as affected by

setting and porcine plasma proteinsrdquo Journal of Food Qualityvol 24 no 5 pp 453ndash471 2001

[15] D D Hamann P M Amato M C Wu and E A FoegedingldquoInhibition of modori (gel weakening) in surimi by plasmahydrolysate and egg whiterdquo Journal of Food Science vol 55 pp665ndash669 1990

[16] K D Reppond and J K Babbitt ldquoProtease inhibitors affectphysical properties of arrowtooth flounder and walleye pollocksurimirdquo Journal of Food Science vol 58 pp 96ndash98 1993

[17] V C Weerasinghe M T Morrissey and H An ldquoCharacteriza-tion of active components in food-grade proteinase inhibitorsfor surimi manufacturerdquo Journal of Agricultural and FoodChemistry vol 44 no 9 pp 2584ndash2590 1996

[18] C-Y Yang ldquoEffect of the addition of bovine plasma on thequality properties of steamed fish pasterdquo The Korean Journal ofFood and Nutrition vol 21 pp 518ndash523 2008

[19] K Duangmal and A Taluengphol ldquoEffect of protein additivessodium ascorbate and microbial transglutaminase on the tex-ture and colour of red tilapia surimi gelrdquo International Journalof Food Science amp Technology vol 45 no 1 pp 48ndash55 2010

[20] S BenjakulW Visessanguan and C Chantarasuwan ldquoEffect ofporcine plasma protein and setting on gel properties of surimiproduced from fish caught inThailandrdquo LWT- Food Science andTechnology vol 37 no 2 pp 177ndash185 2004

[21] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoCysteine proteinase inhibitor from chicken plasma Fractiona-tion characterization and autolysis inhibition of fish myofibril-lar proteinsrdquo Food Chemistry vol 101 no 4 pp 1647ndash1657 2007

[22] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoEffect of chicken plasma protein and some protein additiveson proteolysis and gel-forming ability of sardine (SardinellaGibbosa) surimirdquo Journal of Food Processing and Preservationvol 31 no 4 pp 492ndash516 2007

[23] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoRheological and textural properties of pacific whiting surimigels as influenced by chicken plasmardquo International Journal ofFood Properties vol 11 no 4 pp 820ndash832 2008

[24] M Sugiyama T Mishiro Y Tsukamasa T Suzuki and KTakama ldquoPuncture properties of kamaboko with ovomucoidpasteurized at several temperaturesrdquo Nippon Suisan Gakkaishivol 64 no 1 pp 76ndash81 1998

[25] M Sugiyama T Mishiro Y Tsukamasa et al ldquoPhysical prop-erties of Kamaboko with ovomucoid pasteurized at severaltemperaturesrdquo Nippon Suisan Gakkaishi vol 64 no 1 pp 82ndash87 1998

[26] J Yongsawatdigul and P Piyadhammaviboon ldquoInhibition ofautolytic activity of lizardfish surimi by proteinase inhibitorsrdquoFood Chemistry vol 87 no 3 pp 447ndash455 2004

[27] L Campo-Deano and C Tovar ldquoThe effect of egg albumen onthe viscoelasticity of crab sticks made from Alaska pollock andPacific whiting surimirdquo Food Hydrocolloids vol 23 no 7 pp1641ndash1646 2009

[28] A Hunt J W Park and A Handa ldquoEffect of various types ofegg white on characteristics and gelation of fish myofibrillarproteinsrdquo Journal of Food Science vol 74 no 9 pp C683ndashC6922009

[29] S Rawdkuen and S Benjakul ldquoWhey protein concentrateAutolysis inhibition and effects on the gel properties of surimiprepared from tropical fishrdquo Food Chemistry vol 106 no 3 pp1077ndash1084 2008

26 Journal of Food Quality

[30] Y Ruttanapornvareesakul K Somjit A Otsuka et al ldquoCry-oprotective effects of shrimp head protein hydrolysate on gelforming ability and protein denaturation of lizardfish surimiduring frozen storagerdquo Fisheries Science vol 72 no 2 pp 421ndash428 2006

[31] D K Li H Lin and SM Kim ldquoEffect of rainbow trout (Oncor-hynchus mykiss) plasma protein on the gelation of Alaska pol-lock (Theragra chalcogramma) surimirdquo Journal of Food Sciencevol 73 no 4 pp C227ndashC234 2008

[32] A Hernandez-Briones G Velazquez M Vazquez and J ARamırez ldquoEffects of adding fish gelatin onAlaska pollock surimigelsrdquo Food Hydrocolloids vol 23 no 8 pp 2446ndash2449 2009

[33] T Yin Z H Reed and J W Park ldquoGelling properties of surimias affected by the particle size of fish bonerdquo LWT- Food Scienceand Technology vol 58 no 2 pp 412ndash416 2014

[34] T Yin and J W Park ldquoTextural and rheological properties ofPacific whiting surimi as affected by nano-scaled fish bone andheating ratesrdquo Food Chemistry vol 180 pp 42ndash47 2015

[35] M R Fowler and J W Park ldquoEffect of salmon plasma proteinon Pacific whiting surimi gelation under various ohmic heatingconditionsrdquo LWT- Food Science and Technology vol 61 no 2pp 309ndash315 2015

[36] M R Fowler and J W Park ldquoSalmon blood plasma Effectiveinhibitor of protease-laden Pacific whiting surimi and salmonmincerdquo Food Chemistry vol 176 pp 448ndash454 2015

[37] S Klomklao S Benjakul H Kishimura K Osako and BK Simpson ldquoTrypsin inhibitor from yellowfin tuna (Thunnusalbacores) roe Effects on gel properties of surimi from bigeyesnapper (Priacanthus macracanthus)rdquo LWT- Food Science andTechnology vol 65 pp 122ndash127 2016

[38] N K Vate and S Benjakul ldquoEffect of the mixtures of squid inktyrosinase and tannic acid on properties of sardine surimi gelrdquoJournal of Food Science and Technology vol 53 no 1 pp 411ndash420 2016

[39] T Yamashita ldquoEffects of commercial soybean protein andwheat gluten as subsidiary materials on physical properties ofkamabokordquo Nippon Shokuhin Kogyo Gakkaishi vol 38 no 12pp 883ndash890 1991

[40] K H Chung and C M Lee ldquoFunction of nonfish proteins insurimi-based gel productsrdquo Korean Journal of Society of FoodScience vol 10 pp 146ndash150 1994

[41] K-H Chung and C-M Lee ldquoEvaluation of wheat gluten andmodified starches for their texture-modifying and freeze-thawstabilizing effects on surimi based-productsrdquo Journal of FoodScience and Nutrition pp 190ndash195 1996

[42] S Benjakul S Karoon and A Suwanno ldquoInhibitory effects oflegume seed extracts on fish proteinasesrdquo Journal of the Scienceof Food and Agriculture vol 79 no 13 pp 1875ndash1881 1999

[43] S Benjakul W Visessanguan and P Thummaratwasik ldquoInhi-bition of gel weakening of threadfin bream surimi using Thailegume seed proteinase inhibitorsrdquo Journal of Food Biochem-istry vol 24 no 5 pp 363ndash380 2000

[44] A Oujifard S Benjakul M Ahmad and J Seyfabadi ldquoEffect ofbambara groundnut protein isolate on autolysis and gel prop-erties of surimi from threadfin bream (Nemipterus bleekeri)rdquoLWT- Food Science and Technology vol 47 no 2 pp 261ndash2662012

[45] Y Luo RKuwaharaMKaneniwa YMurata andMYokoyamaldquoEffect of soy protein isolate on gel properties of Alaska pollockand common carp surimi at different setting conditionsrdquoJournal of the Science of Food and Agriculture vol 84 no 7 pp663ndash671 2004

[46] Y Luo H Shen D Pan and G Bu ldquoGel properties of surimifrom silver carp (Hypophthalmichthys molitrix) as affected byheat treatment and soy protein isolaterdquo Food Hydrocolloids vol22 no 8 pp 1513ndash1519 2008

[47] C Cardoso B Ribeiro and R Mendes ldquoEffects of dietary fibreandmicrobial transglutaminase addition on the rheological andtextural properties of protein gels from different fish speciesrdquoJournal of Food Engineering vol 113 no 4 pp 520ndash526 2012

[48] T Kudre S Benjakul and H Kishimura ldquoEffects of proteinisolates from black bean and mungbean on proteolysis and gelproperties of surimi from sardine (Sardinella albella)rdquo LWT-Food Science and Technology vol 50 no 2 pp 511ndash518 2013

[49] S Klomklao and S Benjakul ldquoEffect of trypsin inhibitor inadzuki bean (Vigna angularis) on proteolysis and gel propertiesof threadfin bream (Nemipterus bleekeri)rdquo LWT- Food Scienceand Technology vol 63 no 2 pp 906ndash911 2015

[50] S Konoo H Ogawa and N Iso ldquoEffects of addition of amyloseand amylopectin on the breaking strength of fish meat gelrdquoNippon Suisan Gakkaishi vol 64 no 1 pp 69ndash75 1998

[51] C-S Kong H Ogawa and N Iso ldquoRheological analysis of theeffect of gelatinization of starch added to fish-meat gel based onvolume changesrdquo Fisheries Science vol 65 no 6 pp 930ndash9361999

[52] B-Y Kim W-W Kim and B Yoo ldquoEffect of native and acety-lated sweet potato starch on rheological properties of compositesurimi solrdquo Journal of Food Science and Nutrition vol 13 no 3pp 245ndash248 2008

[53] B-J Yoo ldquoThe effects of alkaline treatment and potato-starchcontent on the quality of fishmeat paste products prepared fromPacific sandlance Ammodytes personatus Girardrdquo Fisheries andAquatic Sciences vol 14 no 3 pp 161ndash167 2011

[54] S M Cho M S Yoon and S-B Kim ldquoEffects of rice flourmilling types and addition methods on rheological and sensoryproperties of surimi productsrdquo Korean Journal of Fisheries andAquatic Sciences vol 46 no 2 pp 139ndash146 2013

[55] Y-M Kwon and J-S Lee ldquoA study on the quality characteristicsof fish cakes containing rice flourrdquo Korean Journal of HumanEcology vol 22 no 1 pp 189ndash200 2013

[56] M Yoon J-S Kim D Kim J Jo and S Cho ldquoOptimization ofthe processing conditions for the preparation of surimi productscontaining rice flourrdquo Fisheries and Aquatic Sciences vol 17 no2 pp 167ndash173 2014

[57] J A Ramırez M Barrera O G Morales and M VazquezldquoEffect of xanthan and locust bean gums on the gelling prop-erties of myofibrillar proteinrdquo Food Hydrocolloids vol 16 no 1pp 11ndash16 2002

[58] A M Barrera J A Ramırez J J Gonzalez-Cabriales and MVazquez ldquoEffect of pectins on the gelling properties of surimifrom silver carprdquo Food Hydrocolloids vol 16 no 5 pp 441ndash4472002

[59] S Benjakul W Visessanguan S Phatchrat and M TanakaldquoChitosan affects transglutaminase-induced surimi gelationrdquoJournal of Food Biochemistry vol 27 no 1 pp 53ndash66 2003

[60] M A Iglesias-Otero J Borderıas and C A Tovar ldquoUse ofKonjac glucomannan as additive to reinforce the gels from low-quality squid surimirdquo Journal of Food Engineering vol 101 no3 pp 281ndash288 2010

[61] S-H Eom J-A Kim B-Y Son et al ldquoEffects of carrageenanon the gelatinization of salt-based surimi gelsrdquo Fisheries andAquatic Sciences vol 16 no 3 pp 143ndash147 2013

Journal of Food Quality 27

[62] S H Choi and S M Kim ldquoQuality properties of giant squid(Dosidicus gigas) surimi-based product manufactured withAmorphophallus konjac flourrdquo Korean Journal of Food Scienceand Technology vol 44 no 4 pp 422ndash427 2012

[63] D Cando B Herranz A J Borderıas and H M MorenoldquoEffect of high pressure on reduced sodium chloride surimigelsrdquo Food Hydrocolloids vol 51 pp 176ndash187 2015

[64] D-S Kim and Y-H Park ldquoEffect of food humectants onlowering water activity of casing kamaboko 1 Effect of loweringwater activity of sodium chloride sugars and polyolsrdquo Bulletinof the Korean Fisheries Society vol 14 pp 139ndash147 1981

[65] D-S Kim and Y-H Park ldquoEffect of food humectant on lower-ingwater activity of casing kamaboko 2 Effect of loweringwateractivity of starch glycine and sodium lactate and prediction ofthe water activity lowing ability of humectantsrdquo Bulletin of theKorean Fisheries Society vol 15 pp 74ndash82 1982

[66] G L Sanchez Pascua M R Casales and M I Yeannes ldquoInflu-ence of water and glycerol contents on the aw of fish pastesrdquoJournal of Aquatic Food Product Technology vol 10 no 1 pp89ndash100 2001

[67] E Niwa K Tsujimoto and S Kanoh ldquoKamaboko gel-strength-ening effect of polyuronides and other polysaccharidesrdquoNipponSuisan Gakkaishi vol 58 pp 85ndash88 1992

[68] R Yoshinaka M Shiraishi and S Ikeda ldquoEffect of AscorbicAcid on theGel Formation of FishMeatrdquoBulletin of the JapaneseSociety for the Science of Fish vol 38 no 5 pp 511ndash515 1972

[69] H G Lee C M Lee K H Chung and S A Lavey ldquoSodiumascorbate affects surimi gel-forming propertiesrdquo Journal of FoodScience vol 57 pp 1343ndash1347 1992

[70] Y Park S D Kelleher D J McClements and E A DeckerldquoIncorporation and stabilization of omega-3 fatty acids insurimi made from cod Gadus morhuardquo Journal of Agriculturaland Food Chemistry vol 52 no 3 pp 597ndash601 2004

[71] E Okazaki Y Yamashita and Y Omura ldquoEmulsification of fishoil in surimi by high-speed mixing and improvement of gel-forming abilityrdquo Nippon Suisan Gakkaishi vol 68 no 4 pp547ndash553 2002

[72] H Fukushima E Okazaki S Noda and Y Fukuda ldquoChangesin physical properties water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oilrdquoNippon Shokuhin Kagaku Kogaku Kaishi vol 54 no 1 pp 39ndash44 2007

[73] B N Pietrowski R Tahergorabi and J Jaczynski ldquoDynamicrheology and thermal transitions of surimi seafood enhancedwith 120596-3-rich oilsrdquo Food Hydrocolloids vol 27 no 2 pp 384ndash389 2012

[74] A K Balange S Benjakul and S Maqsood ldquoGel strengtheningeffect of wood extract on surimi produced frommackerel storedin icerdquo Journal of Food Science vol 74 no 8 pp C619ndashC6272009

[75] N Buamard and S Benjakul ldquoImprovement of gel properties ofsardine (Sardinella albella) surimi using coconut husk extractsrdquoFood Hydrocolloids vol 51 pp 146ndash155 2015

[76] A K Balange and S Benjakul ldquoEffect of oxidised phenolic com-pounds on the gel property of mackerel (Rastrelliger kanagurta)surimirdquo LWT- Food Science and Technology vol 42 no 6 pp1059ndash1064 2009

[77] A Balange and S Benjakul ldquoEnhancement of gel strength ofbigeye snapper (Priacanthus tayenus) surimi using oxidisedphenolic compoundsrdquo Food Chemistry vol 113 no 1 pp 61ndash702009

[78] Y A Arfat and S Benjakul ldquoEffect of zinc sulphate on gellingproperties of phosphorylated protein isolate from yellow stripetrevallyrdquo Food Chemistry vol 141 no 3 pp 2848ndash2857 2013

[79] M-S Bae and S-C Lee ldquoQuality characteristics of fried fishpaste containing anchovy powderrdquo Journal of the Korean Societyof Food Science and Nutrition vol 36 no 9 pp 1188ndash1192 2007

[80] M-S Bae J-U Ha and S-C Lee ldquoQuality properties of highcalcium fish paste containing anchovyrdquo Korean Journal of Foodand Cookery Science vol 23 pp 561ndash566 2007

[81] H-S Cho and K-H Kim ldquoQuality characteristics of fish pastecontaining skate (Raja kenojei) powderrdquo Journal of the EastAsian Society of Dietary Life vol 21 pp 808ndash813 2011

[82] Y H Park E Y Bum E R Jeon and LH Jung ldquoEffect of addedskate (Raja kenojei) on the quality characteristics of steamedfishmeat pasterdquo Food Science and Biotechnology vol 23 no 5 pp1453ndash1458 2014

[83] S-M Park B-B Lee Y-M Hwang and S-C Lee ldquoQualityproperties of fish paste containing Styela clavardquo Journal of theKorean Society of Food Science and Nutrition vol 35 pp 908ndash911 2006

[84] S-Y Choi E-Y Choi K-E Lee A-S Song S-H Park and S-C Lee ldquoPreparation and quality analysis of fish paste containingStyela clava tunicrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 41 no 11 pp 1591ndash1595 2012

[85] S-M Park H-K Seo and S-C Lee ldquoPreparation and qualityproperties of fish paste containing Styela plicatardquo Journal of theKorean Society of Food and Nutrition vol 35 pp 1256ndash12592006

[86] J-S Seo and H-S Cho ldquoQuality characteristics of fish pastewith shrimp powderrdquo Korean Journal of Food Preservation vol19 pp 519ndash524 2012

[87] H-S Cho and K-H Kim ldquoQuality properties of fish pastecontaining green laver powderrdquo Journal of the Korean Societyof Food Culture vol 29 pp 421ndash427 2014

[88] I-D Park ldquoQuality characteristics of fish paste containingLagocephalus lunaris powderrdquo Journal of the Korean Society ofFood Culture vol 28 pp 657ndash663 2013

[89] I Park ldquoQuality properties of fish paste containingCapsosiphonfulvescens powderrdquo Journal of The Korean Society of FoodCulture vol 31 no 4 pp 357ndash363 2016

[90] B-M Kim J-H Jung M-J Jung D-S Kim J-Y Jun and I-H Jeong ldquoThe quality characteristics and processing of fishpaste containing red snow crabChionoecetes japonicus leg-meatpowderrdquo Korean Journal of Fisheries and Aquatic Sciences vol49 pp 1ndash6 2016

[91] Y-J Shin and G-S Park ldquoQuality characteristics of fish-pastecontaining mulberry leaf powderrdquo Journal of the East AsianSociety of Dietary Life vol 15 pp 738ndash745 2005

[92] Y-J Shin ldquoQuality characteristics of fish paste containing lotus(Nelumbo nucifera) leaf powderrdquo Korean Journal of Food andCookery Science vol 23 pp 947ndash953 2007

[93] A D Thorat V R Joshi A U Pagarkar and A K BalangeldquoMicrowave pasteursation of fish paste product-Kamabokowith Beetroot and Spinachrdquo Ecology Environment and Conser-vation vol 13 no 1 pp 113ndash118 2007

[94] M-O Yang and E-J Cho ldquoQuality properties of surimi withadded citrus fruitsrdquo Journal of East Asian Society of Dietary Lifevol 17 pp 58ndash63 2007

[95] F Alakhrash U Anyanwu and R Tahergorabi ldquoPhysicochemi-cal properties of Alaska pollock (Theragra chalcograma) surimigels with oat branrdquo LWT- Food Science and Technology vol 66pp 41ndash47 2016

28 Journal of Food Quality

[96] J-S Kim and G-I Byun ldquoMaking fish paste with yam (Dios-corea japonica Thumb) powder and its characteristicsrdquo KoreanJournal of Culinary Research vol 15 pp 57ndash69 2009

[97] Y-J Shin J A Lee and G-S Park ldquoa Quality characteristics offish pastes containing Lycii fructus powderrdquo Journal of the EastAsian Society of Dietary Life vol 18 pp 22ndash28 2008

[98] D-W Shim J Jiang J-H Kim et al ldquoEffects of size adjustedwith red ginseng powders on quality of fish pastesrdquo Journal ofthe Korean Society of Food Science and Nutrition vol 41 no 10pp 1448ndash1453 2012

[99] Y-J Shin J A Lee and G-S Park ldquoQuality characteristics offish paste containing Angelicae gigantis Radix powderrdquo KoreanJournal of Food and Cookery Science vol 24 pp 699ndash705 2008

[100] S Choi ldquoQuality characteristics of fish paste containing Cur-cuma longa L powderrdquo The Korean Journal of Food and Nutri-tion vol 25 no 4 pp 833ndash841 2012

[101] J-A Jang H-A Kim and S-K Choi ldquoQuality characteristicsof fish cake made with silver pomfret (Pampus argenteus) withadded wasabi powderrdquo Journal of the East Asian Society ofDietary Life vol 20 pp 103ndash112 2010

[102] Y-J Shin K-S Kim and G-S Park ldquoTexture and sensorycharacteristics of fish paste containing white Poria cocos wolfpowderrdquo Korean J Food Cookery Sci vol 25 pp 119ndash125 2009

[103] J-U Ha S-G Koo H-Y Lee Y-M Hwang and S-C LeeldquoPhysical properties of fish paste containing Agaricus bisporusrdquoKorean Journal of Food Science and Technology vol 33 pp 451ndash454 2001

[104] S-G Koo Y-K Ryu Y-M Hwang J-U Ha and S-C LeeldquoQuality properties of fish-paste containing enoki mushroom(Flammuilna velutipes)rdquo Journal of the Korean Society of FoodScience and Nutrition vol 30 pp 288ndash291 2001

[105] M-H Son S-Y Kim J-U Ha and S-C Lee ldquoTexture prop-erties of surimi gel containing shiitake mushroom (Lentinusedodes)rdquo Journal of the Korean Society of Food Science andNutrition vol 32 pp 859-853 2003

[106] S-Y Kim M-H Son J-U Ha and S-C Lee ldquoPreparationand characterization of fried surimi gel containing king oystermushroom (Pleurotus eryngii)rdquo Journal of the Korean Society ofFood Science and Nutrition vol 32 pp 855ndash858 2003

[107] S I Chung S Y Kim Y J Nam andM Y Kang ldquoDevelopmentof surimi gel from king oyster mushroom and cuttlefish meatpasterdquo Food Science and Biotechnology vol 19 no 1 pp 51ndash562010

[108] S K Jin J H Park and S J Hur ldquoEffect of substituting surimiwith spent laying hen meat on the physicochemical character-istics of fried fish pasterdquo Food and Bioprocess Technology vol 7no 3 pp 901ndash908 2014

[109] A Debusca R Tahergorabi S K Beamer K E Matak and JJaczynski ldquoPhysicochemical properties of surimi gels fortifiedwith dietary fiberrdquo Food Chemistry vol 148 pp 70ndash76 2014

[110] H-S Yook J-W Lee H-J Lee B-S Cha S-Y Lee and M-W Byun ldquoQuality properties of fish paste prepared with refineddietary fiber from ascidian (Halocynthia roretzi) tunicrdquo Journalof the Korean Society of Food Science and Nutrition vol 29 pp642ndash646 2000

[111] A Debusca R Tahergorabi S K Beamer S Partington andJ Jaczynski ldquoInteractions of dietary fibre and omega-3-rich oilwith protein in surimi gels developed with salt substituterdquo FoodChemistry vol 141 no 1 pp 201ndash208 2013

[112] C Sell S Beamer J Jaczynski and K E Matak ldquoSensorycharacteristics and storage quality indicators of surimi franks

nutritionally enhanced with omega-3 rich flaxseed oil andsalmon oilrdquo International Journal of Food Science amp Technologyvol 50 no 1 pp 210ndash217 2015

[113] T Chang C Wang X Wang L Shi H Yang and M CuildquoEffects of soybean oil moisture and setting on the textural andcolor properties of surimi gelsrdquo Journal of Food Quality vol 38no 1 pp 53ndash59 2015

[114] J-S Kim M-L Cho and M-S Heu ldquoQuality improvement ofheat-induced surimi gel using calcium powder of cuttle Sepiaesculenta bone treated with acetic acidrdquo Journal of the KoreanFisheries Society vol 36 pp 198ndash203 2003

[115] G-W Kim G-H Kim J-S Kim et al ldquoQuality characteristicsof fried fish paste of Alaska pollack meat paste added withpropolisrdquo Journal of the Korean Society of Food Science andNutrition vol 37 no 4 pp 485ndash489 2008

[116] G-W Kim G-H Kim J-S Kim et al ldquoQuality of fried fishpaste prepared with sand-lance (Hypoptychus dybowskii) meatand propolis additiverdquo Journal of the Korean Fisheries Societyvol 41 pp 170ndash175 2008

[117] B Park H Cho and S Park ldquoStudy on quality characteristicsof fish paste containing cheonggukjang powderrdquo Journal of TheKorean Society of Food Culture vol 30 no 2 pp 213ndash219 2015

[118] SMiyao T Shindoh KMiyamori and T Arita ldquoEffects of highpressurization on the growth of bacteria derived from surimi(fish paste)rdquo Nippon Shokuhin Kogyo Gakkaishi vol 40 pp478ndash484 1993

[119] A Malicki Z Sysak S Bruzewicz J Zrodłowska-Danek andM Szpak ldquoApplication of high hydrostatic pressure to extendthe shelf-life of traditionally produced fish pasterdquo MedycynaWeterynaryjna vol 66 pp 695ndash698 2010

[120] J-H Kim J-Y Jeon S-R Ryu et al ldquoMicrobial quality andphysiochemical changes of grilled fish paste in a group-mealservice affected by gamma-irradiationrdquo Korean Journal of FoodPreservation vol 11 pp 522ndash529 2004

[121] H-O Cho J-H Kwon M-W Byun and M-K Lee ldquoPreserva-tion of fried fish-paste by Irradiationrdquo Korean Journal of FoodScience and Technology vol 17 pp 474ndash481 1985

[122] H-Y Shin Y-J Lee I-Y Park J-Y Kim S-J Oh and K BSong ldquoEffect of chlorine dioxide treatment onmicrobial growthand qualities of fish paste during storagerdquo Journal of the KoreanSociety for Applied Biological Chemistry vol 50 pp 42ndash47 2007

[123] S S YoonH Kim YM Lee E J Jeong andY J Cha ldquoShelf-lifeextension effects of fish paste product by adding pepper extractrdquoin Proceedings of the Korean Nutrition Society Conference p 216Seoul Korea 2001

[124] E-S Ahn M-S Kim and D-H Shin ldquoScreening of natu-ral antimicrobial edible plant extract for dooboo fish pastemakkoli spoilage microorganismrdquo Korean Journal of FoodScience and Technology vol 26 pp 733ndash739 1994

[125] Y-M Kim B-H Lee S-H Lee I-S Shin and T-S LeeldquoThe preservative effect of egg white lysozyme added surimiproductsrdquo Bulletin of the Korean Fisheries Society vol 21 pp269ndash275 1988

[126] S-H Cho I-S Joo I-W Seo and Z-W Kim ldquoPreservativeeffect of grapefruit seed extract on fish meat productrdquo Journalof Food Hygiene and Safety vol 6 pp 67ndash72 1991

[127] E-T Jeong M-Y Park E-W Lee U-T Park and D-S ChangldquoAntimicrobial characteristics against spoilage microorganismsand food preservative effect of cinnamon (Cinnamomum cassiaBlume) bark extractrdquo Korean Journal of Life Science vol 8 pp648ndash653 1998

Journal of Food Quality 29

[128] D-S Chang H-R Cho H-S Lee M-Y Park and S-M LimldquoDevelopment of alginic acid hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 823ndash826 1998

[129] H-R Cho D-S Chang W-D Lee E-T Jeong and E-WLee ldquoUtilization of chitosan hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 817ndash822 1998

[130] K Yamazaki T Tashiro S Shirahama J-Y Jun and Y KawaildquoGrowth inhibition of spore-forming bacteria in fish-pasteproducts by Nisinrdquo Nippon Shokuhin Kagaku Kogaku Kaishivol 61 no 2 pp 70ndash76 2014

[131] K Hashimoto M L Bari Y Inatsu S Kawamoto and J ShimaldquoBiopreservation of kamaboko (steamed surimi) using pisci-colin KH1 produced by Carnobacteriummaltalomaticum KH1rdquoJapanese Journal of FoodMicrobiology vol 28 pp 193ndash200 2011

[132] S H Lee M S Lee S K Park D H Bae S D Ha and K BSong ldquoPhysical properties of protein films containing green teaextract and its antioxidant effect on fish paste productsrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1063ndash1067 2004

[133] G-O Lim Y-H Hong and K B Song ldquoIncorporating grape-fruit seed extract into Gelidium corneum-whey protein isolateblend packaging film increases the shelf life of fish paste -Research noterdquo Journal of Food Science and Nutrition vol 13no 4 pp 370ndash374 2008

[134] T C Lanier J Yongsawatdigul and P Carvajal-RondanellildquoSurimi gelation chemistryrdquo in Surimi and Surimi Seafood J WPark Ed pp 101ndash139Marcel Dekker NewYork NYUSA 2013

[135] M Kinoshita H Toyohara and Y Shimizu ldquoPurification andproperties of a novel latent proteinase showing myosin heavychain-degrading activity from threadfin-bream musclerdquo TheJournal of Biochemistry vol 107 no 4 pp 587ndash591 1990

[136] D H Wasson J K Babbitt and J S French ldquoCharacterizationof a heat stable protease from arrowtooth flounder Atheresthesstomiasrdquo Journal of Aquatic Food Product Technology vol 1 no3-4 pp 167ndash182 1993

[137] T A Seymour M T Morrissey M Y Peters and H An ldquoPuri-fication and characterization of pacific whiting proteasesrdquoJournal of Agricultural and Food Chemistry vol 42 no 11 pp2421ndash2427 1994

[138] H An V Weerasinghe T A Seymour and M T MorrisseyldquoCathepsin degradation of Pacific whiting surimi proteinrdquoJournal of Food Science vol 59 pp 1013ndash1017 1994

[139] AFDF Ground fish quality chart Alaska fisheries departmentfoundation Anchorage Alaska 1992

[140] G Sylvia S Larkin and M T Morrissey ldquoQuality and resourcemanagement bioeconomic analysis of the Pacific whitingindustryrdquo in Recent Advances inMarine Science and TechnologyO Bellwood H Choat and N Saxena Eds James CookUniversity Townsville QS Australia 1994

[141] S H Choi and S M Kim ldquoDevelopment of giant squid(Ommastrephes bartrami) surimi-based products with gel tex-ture enhancers and the effects of setting on gel qualityrdquo Journalof the Korean Society of Food Science and Nutrition vol 41 no7 pp 975ndash981 2012

[142] J A Ramırez R M Uresti G Velazquez and M VazquezldquoFood hydrocolloids as additives to improve the mechanicaland functional properties of fish products A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1842ndash1852 2011

[143] S-K Kim H-G Byun P-J Park and F Shahidi ldquoAngiotensinI converting enzyme inhibitory peptides purified from bovine

skin gelatin hydrolysaterdquo Journal of Agricultural and FoodChemistry vol 49 no 6 pp 2992ndash2997 2001

[144] I Kimura M Sugimoto K Toyoda N Seki K-I Arai andT Fujita ldquoA study on the cross-links reaction of myosin inkamaboko rsquosuwarirsquo gelsrdquo Nippon Suisan Gakkaisi vol 57 pp1386ndash1396 1991

[145] H An M Y Peters and T A Seymour ldquoRoles of endogenousenzymes in surimi gelationrdquo Trends in Food Science amp Technol-ogy vol 7 no 10 pp 321ndash327 1996

[146] R Nopianti N Huda andN Ismail ldquoA review on the loss of thefunctional properties of proteins during frozen storage and theimprovement of gel-forming properties of Surimirdquo AmericanJournal of Food Technology vol 6 no 1 pp 19ndash30 2011

[147] A M Martın-Sanchez C Navarro J A Perez-Alvarez and VKuri ldquoAlternatives for efficient and sustainable production ofsurimi A reviewrdquo Comprehensive Reviews in Food Science andFood Safety vol 8 no 4 pp 359ndash374 2009

[148] Korea Agro-Fisheries and Food Trade Corporation Processedfood segmented market survey-fish cake market Korea Agro-Fisheries and Food Trade Corporation Seoul Korea 2014

[149] D Kraft and A DerMarderosian The A-Z guide to food asmedicine CRC Press Boca Raton Fla USA 2016

[150] C V Morr and E A Foegeding ldquoComposition and function-ality of commercial whey and milk protein concentrates andisolates a status reportrdquo Food Technology vol 44 pp 100ndash1121990

[151] A Saiga T Okumura T Makihara et al ldquoAngiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chickenbreast muscle extractrdquo Journal of Agricultural and Food Chem-istry vol 51 no 6 pp 1741ndash1745 2003

[152] B Li F Chen X Wang B Ji and Y Wu ldquoIsolation and iden-tification of antioxidative peptides from porcine collagenhydrolysate by consecutive chromatography and electrosprayionization-mass spectrometryrdquo Food Chemistry vol 102 no 4pp 1135ndash1143 2007

[153] A Trampuz R M Prabhu T F Smith and L M BaddourldquoAvian Influenza A New Pandemic Threatrdquo Mayo ClinicProceedings vol 79 no 4 pp 523ndash530 2004

[154] M C Gomez-Guillen B Gimenez M E Lopez-Caballeroand M P Montero ldquoFunctional and bioactive properties ofcollagen and gelatin from alternative sources A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1813ndash1827 2011

[155] D Li X Fu and S M Kim ldquoProduction of chum salmoncystatin from the recombinant Saccharomyces cerevisiae opti-mized using response surface methodologyrdquo Biotechnology andBioprocess Engineering vol 15 no 2 pp 314ndash323 2010

[156] H Akazawa Y Miyauchi K Sakurada H Wasson and K DReppond ldquoEvaluation of protease inhibitors in Pacific whitingsurimirdquo Journal of Aquatic Food Product Technology vol 2 no3 pp 79ndash95 1994

[157] A Hunt K J K Getty and J W Park ldquoRoles of starch in surimiseafood A reviewrdquo Food Reviews International vol 25 no 4 pp299ndash312 2009

[158] T Suzuki Fish and Krill Protein Processing Technology AppliedScience Publishers London UK 1981

[159] C M Lee ldquoSurimi process technologyrdquo Food Technology vol38 pp 69ndash80 1984

[160] M C Wu D D Hamann and T C Lanier ldquoRheological andcalorimetric investigations of starch-fish protein systems duringthermal processingrdquo Journal of Texture Studies vol 16 pp 53ndash74 1985

30 Journal of Food Quality

[161] M C Wu T C Lanier and D D Hamann ldquoRigidity and vis-cosity changes of croaker actomyosin during thermal gelationrdquoJournal of Food Science vol 50 no 1 pp 14ndash19 1985

[162] S-K Kim S-T Yang and E-H Lee ldquoThe starch content of fish-paste products onmarketrdquo Journal of the Korean Society of FoodScience and Nutrition vol 7 pp 41-42 1978

[163] G AMacDonald T C Lanier and P A Caruajal ldquoStabilizationof protein in surimirdquo in Surimi and Surimi Seafood J W ParkEd pp 91ndash125 Marcel Dekker Inc New York NY USA 2000

[164] J A Ramırez I A Santos O G Morales M T Morrisseyand M Vazquez ldquoApplication of microbial transglutaminaseto improve mechanical properties of surimi from silver carputilizacionde transglutaminasa microbiana paramellora-las-propiedades mecanicas de surimide carpaplateada utiliza-cionde transglutaminasamicrobiana paramejorarlaspropieda-des mecanicas de surimide carpaplateadardquo Ciencia y TecnologıaAlimentaria vol 3 no 1 pp 21ndash28 2000

[165] M C Gomez-Guillen A J Borderıas and P MonteroldquoSalt nonmuscle proteins and hydrocolloids affecting rigiditychanges during gelation of giant squid (Dosidicus gigas)rdquoJournal of Agricultural and Food Chemistry vol 45 no 3 pp616ndash621 1997

[166] J W Park ldquoIngredient technology and formulation develop-mentrdquo in Surimi and Surimi Seafood J W Park Ed pp 91ndash125Marcel Dekker Inc New York NY USA 2000

[167] F Garcıa-Ochoa V E Santos J A Casas and E Gomez ldquoXan-than gum production recovery and propertiesrdquo BiotechnologyAdvances vol 18 no 7 pp 549ndash579 2000

[168] A I Rodrıguez-Hernandez and A Tecante ldquoDynamic vis-coelastic behavior of gellan- 120580 -carrageenan and gellan-xanthangelsrdquo Food Hydrocolloids vol 13 no 1 pp 59ndash64 1999

[169] J A Casas and F Garcıa-Ochoa ldquoSophorolipid production byCandida bombicola Medium composition and culture meth-odsrdquo Journal of Bioscience and Bioengineering vol 88 no 5 pp488ndash494 1999

[170] H J Lim ldquoA study on the calcium and sodium intakes andurinary calcium excretion of preschool children in BusanrdquoKorean Journal of Nutrition vol 34 pp 786ndash796 2001

[171] WHO ldquoDiet nutrition and the prevention of chronic diseasesReport of a joint WHOFAO expert consultationrdquo Tech RepWHO World Health Organization Geneva Switzerland 2003

[172] L K Dahl ldquoPossible role of salt intake in the development ofessential hypertensionrdquo International Journal of Epidemiologyvol 34 no 5 pp 967ndash972 2005

[173] H-K Jeong D-S Kim S-J Chun K-S Jo and Y-H ParkldquoEffect of food humectant on lowering water activity of casingKamaboko 3rdquo Bulletin of the Korean Fisheries Society vol 16 pp88ndash96 1983

[174] J Han E Kim M Cheong S Chee and K Chee ldquoBioavailabil-ity and digestibility of organic calcium sources by bone healthindexrdquo Journal of Nutrition and Health vol 43 no 1 pp 12ndash252010

[175] M K Lee ldquoA study of the bio-functional evaluation of Rajaskates caught in Huksando areardquo Journal of the Kwangju HealthCollege vol 21 pp 253ndash265 1996

[176] S H Cho Extraction and characterization of gelatin andantimicrobial peptide from skate (Raja kenojei) skins ChonnamNational University Gwangju Korea 2003

[177] J H Choi ldquoIsolation and purification of in chondroitin sulfatefrom skate cartilagerdquo Tech Rep Pukyong National UniversityBusan Korea 2004

[178] Y G Jo ldquoThe sterol composition of Styela clavardquo Journal of theKorean Fisheries Society vol 11 pp 97ndash101 1978

[179] S H Ahn ldquoExtraction of glycosaminoglycans from Styela clavatunicrdquo Biotechnology and Bioprocess Engineering vol 18 pp180ndash185 2003

[180] J J Kim S J Kim S H Kim H R Park and S C LeeldquoAntioxidant and anticancer activities of extracts from Styelaclava according to the processing methods and solventsrdquoJournal of the Korean Society of Food Science and Nutrition vol35 pp 278ndash283 2006

[181] T Aoki K Takata and N Kunisaki ldquoComparison of nutrientcomponents of six species of wild and cultured fishesrdquo Bulletinof the Japanese Society for the Science of Fish vol 57 pp 1927ndash1934 1991

[182] Committee Donguibogam Translated Donguibogam Bubin-munwha Press Seoul Korea 1999

[183] Y-K Park H-J Kim and M-H Kim ldquoQuality characteristicsof fried fish paste added with ethanol extract of onionrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1049ndash1055 2004

[184] G L Dong J J Hyun and E-R Woo ldquoAntimicrobial prop-erty of (+)-lyoniresinol-3120572-O-120573-D- glucopyranoside isolatedfrom the root bark of Lycium chinense Miller against humanpathogenic microorganismsrdquo Archives of Pharmacal Researchvol 28 no 9 pp 1031ndash1036 2005

[185] C C Wang S C Chang B S Inbaraj and B H ChenldquoIsolation of carotenoids flavonoids and polysaccharides fromLycium barbarum L and evaluation of antioxidant activityrdquoFood Chemistry vol 120 no 1 pp 184ndash192 2010

[186] Z Zhang X Liu T Wu et al ldquoSelective suppression of cervicalcancer Hela cells by 2-O-120573-d- glucopyranosyl-l-ascorbic acidisolated from the fruit of Lycium barbarum Lrdquo Cell Biology andToxicology vol 27 no 2 pp 107ndash121 2011

[187] J S Kil M G Kim H M Choi et al ldquoInhibitory effects ofAngelicae GigantisRadix on osteoclast formationrdquo PhytotherapyResearch vol 22 no 4 pp 472ndash476 2008

[188] ANiranjan andD Prakash ldquoChemical constituents and biolog-ical activities of turmeric (Curcuma longa L) - a reviewrdquo Journalof Food Science and Technology vol 45 pp 109ndash116 2008

[189] K S Kim M G Choung and S H Park ldquoQuantitativedetermination and stability of curcuminoid pigments fromturmeric (Curcuma longaL) rootrdquo Korean Journal of CropScience vol 50 pp 211ndash215 2005

[190] I S Shin and J M Lee ldquoStudy on antimicrobial and antimuta-genic activity of horseradish (Wasabia japonica) root extractsrdquoJournal of the Korean Fisheries Society vol 31 pp 835ndash841 1998

[191] Y J ChoA study on the antioxidative and antimicrobial activitiesof wasabi (Wasabia koreana Cruciferae) extracts [PhD thesis]Sungshin Womens University Seoul Korea 2008

[192] A-S Kang T-S Kang H-R Shon et al ldquoStudies on improve-ment of artificial cultivation and antioxidative activity of Poriacocosrdquo The Korean Journal of Mycology vol 27 pp 378ndash3801999

[193] J-H Lee Y J Lee J-K Shin et al ldquoEffects of triterpenoidsfrom Poria cocos Wolf on the serotonin type 3A receptor-mediated ion current in Xenopus oocytesrdquo European Journal ofPharmacology vol 615 no 1ndash3 pp 27ndash32 2009

[194] K R Im M J Kim T K Jung and K S Yoon ldquoAnalysisof isoflavonoid contents in Astragalus membranaceus Bungecultivated in different areas and at various agesrdquo The KoreanSociety for Biotechnology and Bioengineering vol 25 pp 271ndash276 2010

Journal of Food Quality 31

[195] Y E Lee and S H Hong Oriental Medicine Food MaterialsKyomunsa Seoul Korea 2003

[196] D H Kim ldquoQuality characteristics of fish paste prepared withAstragalus membranaceus powderrdquo Food Engineering Progressvol 15 pp 362ndash369 2011

[197] S-E Kim B S Hwang J-G Song S W Lee I-K Lee andB-S Yun ldquoNew bioactive compounds from Korean nativemushroomsrdquoMycobiology vol 41 no 4 pp 171ndash176 2013

[198] National Institute of Agricultural Science The Mushrooms inKorea Dongbang Media Co Ltd Seoul Korea 2004

[199] Y-J Gao M Zhang and W-P Chen ldquoStudy on processing offish paste with waste of grass carprdquo Journal of Food Science andBiotechnology vol 31 pp 1031ndash1038 2012

[200] S Tolasa C M Lee and S Cakli ldquoPhysical and oxidativestabilization of omega-3 fatty acids in surimi gelsrdquo Journal ofFood Science vol 75 no 3 pp C305ndashC310 2010

[201] B N Pietrowski R Tahergorabi K E Matak J C Tou andJ Jaczynski ldquoChemical properties of surimi seafood nutrifiedwith 120596-3 rich oilsrdquo Food Chemistry vol 129 no 3 pp 912ndash9192011

[202] S H Kim J L Yang and Y S Song ldquoPhysiological function ofcheonggukjangrdquo Food Industry and Nutrition vol 4 pp 40ndash461999

[203] R Walker ldquoToxicology of sorbic acid and sorbatesrdquo Food Addi-tives amp Contaminants Part A vol 7 no 5 pp 671ndash676 1990

[204] B R Thakur and T R Patel ldquoSorbates in fish and fish productsmdasha reviewrdquo Food Reviews International vol 10 no 1 pp 93ndash1071994

[205] C-Y Wang H-W Huang C-P Hsu and B B Yang ldquoRecentadvances in food processing using high hydrostatic pressuretechnologyrdquo Critical Reviews in Food Science and Nutrition vol56 no 4 pp 527ndash540 2016

[206] J H Kwon M W Byun and J S Kim ldquoMicrobiological andorganoleptic qualities of boiled-dried anchovies during post-irradiation periodrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 25 pp 283ndash287 1996

[207] J Noh and J H Kwon ldquoThe quality and thermoluminescenceproperties of dried pollack during storage following irradia-tionrdquo Korean Journal of Food Science and Technology vol 36pp 711ndash716 2004

[208] I Tukenmez M S Ersen A T Bakioglu A Bicer and VPamuk ldquoDose dependent oxidation kinetics of lipids in fish dur-ing irradiation processingrdquo Radiation Physics and Chemistryvol 50 no 4 pp 407ndash414 1997

[209] T Sakai and T Yamaguchi ldquoEffects of yuzu peel addition onthe lipid oxidation in kamaboko Effects of yuzu peel additionon the lipid oxidation in kamabokordquo Bulletin of the Faculty ofAgriculture Miyazaki University vol 57 pp 101-102 2011

[210] E-H Lee K-S Oh J-G Koo H-S Park S-Y Cho and Y-J Cha ldquoStudies on processing and keeping quality of retortpouched foods (3) Preparation and keeping quality of retortpouched fried mackerel meat pasterdquo Bulletin of the KoreanFisheries Society vol 17 pp 373ndash382 1984

[211] J-H Ha E-H Lee J-S Kim S-G Ji and J-G Koo ldquoA study onthe thermal treatment conditions of retort pouched fried fish-paste 1 Influence of thermal treatment conditions on qualityrdquoBulletin of the Korean Fisheries Society vol 20 pp 573ndash581 1987

[212] P Guenneugues and J Ianelli ldquoSurimi resources and marketrdquoin Surimi and surimi seafood J W Park Ed pp 25ndash53 MarcelDekker Inc New York NY USA 2013

Research ArticleDevelopment of a Chemically Defined Medium forBetter Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31

Wenli Liu12 Lanwei Zhang23 and Huaxi Yi3

1College of Chemistry and Environmental Engineering Shenzhen University Shenzhen Guangdong 518060 China2School of Food Science amp Technology Harbin Institute of Technology 73 HuangHe Avenue Harbin Heilongjiang 150090 China3College of Food Science and Engineering Ocean University of China Yushan Road 5 Qingdao Shandong 266100 China

Correspondence should be addressed to Lanwei Zhang zhanglwhiteducn and Huaxi Yi yihxouceducn

Received 31 March 2017 Revised 17 July 2017 Accepted 2 August 2017 Published 6 September 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Wenli Liu et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The macro- and micronutrients in traditional medium such as MRS used for cultivating lactic acid bacteria especially forbacteriocin production have not been defined preventing the quantitative monitoring of metabolic flux during bacteriocinbiosynthesis To enhance Enterocin Y31 production and simplify steps of separation and purification we developed a simplifiedchemically definedmedium (SDM) for the growth of Enterococcus faeciumY31 and production of its bacteriocin Enterocin Y31Wefound that the bacterial growthwas unrelated toEnterocinY31 production inMRS therefore both the growth rate and theEnterocinY31 production were set as the index for investigation Single omission experiments revealed that 5 gL NaCl five vitamins twonucleic acid basesMgSO

4sdot7H2OMnSO

4sdot4H2OKH

2PO4 K2HPO4 CH3COONa fourteen amino acids and glucosewere essential

for the strainrsquos growth and Enterocin Y31 production Thus a novel simplified and defined medium (SDM) was formulated with30 components in total Consequently Enterocin Y31 production yield was higher in SDM as compared to either MRS or CDMSDM improved the Enterocin Y31 production and simplified the steps of purification (only two steps) which has broad potentialapplications

1 Introduction

Bacteriocins are ribosomally synthesised antimicrobial pro-teins or protein complexes that inhibit other bacteria andthey either have a narrow antimicrobial spectrum (againstthe same species) or broad antimicrobial spectrum (againstacross genera) [1 2] Bacteriocin produced by lactic acidbacteria (LAB) is generally regarded as safe (GRAS) andQualified Presumption of Safety (QPS) status [3 4] andit is a desirable trait as a food additive for extending theshelf-life of the fermented food and controlling the safetyof foods [5 6] Based on their molecular structure bac-teriocins can be divided into four groups class I bacte-riocins contain posttranslational modifications (lantibioticsand molecular weight le 5 kDa) class II bacteriocins areunmodified and include small heat-stable nonlanthionine-containing peptides [7] The third class includes large

heat-labile bacteriocins Finally the fourth class comprisescomplex bacteriocins containing a protein moiety with oneor more other lipids or carbohydrates [8] Most bacteriocinsproduced by the Enterococcus faecium group of LAB are classII bacteriocins One subgroup class IIa contains bacteriocinswith certain sequence motifs in their N-terminal halves andis active against the food pathogen Listeria monocytogenes[9] Class IIa bacteriocins have become a focus of researchowing to their low molecular weight good dispersity andhigh thermostability This is also a case of Enterocin Y31produced by E faecium Y31 in the current work [10]

Enterocin Y31 is a class IIa bacteriocin produced byE faecium Y31 [11] Previous research results showed thatEnterocin Y31 had broad spectrum inhibition activity againstBacillus subtilis ATCC 6633 Escherichia coli ATCC 25922Listeria monocytogenes ATCC 19111 Bacillus cereus CICC20463 Staphylococcus aureus and Salmonella enterica serovar

HindawiJournal of Food QualityVolume 2017 Article ID 9017452 8 pageshttpsdoiorg10115520179017452

2 Journal of Food Quality

TyphimuriumATCC 14028The isoelectric point of EnterocinY31 was 825 it was stable in both acidity and alkalescenceconditions hence Enterocin Y31 has a broad applicationprospect (not published) However two main drawbacks ofEnterocin Y31 with regard to application in foods are asfollows (1) bacteriocins are secreted in very small quan-tities in the production media and (2) the media used togrow the bacteriocin-producing strains are very complex[12] as the LAB are fastidious organisms requiring aminoacids B vitamins and various minerals for their growthThese components are normally provided by sources such assoybean meal yeast extract and meat extract All of thesesources contain proteins and peptides as sources of aminoacids which are often very closely related to the bacteriocinproduced Therefore purification of bacteriocin from sucha complex medium requires a series of steps At each stepthere is some loss and sometimes after the final purificationthe antimicrobial activity may be completely lost Complexmedia do not allow the examination of all individual mediumfactors [13 14] affecting bacteriocin production

Ricciardi reported a modified chemically defined med-ium to promote the growth of Lactobacillus casei and Lacto-bacillus plantarum groups [15] In the present study weimproved the chemically defined medium to improve theyield of Enterocin Y31 produced by E faecium Y31 Thereare four objectives of this study (1) to develop a newand improved production method for Enterocin Y31 (pro-duced by E faecium Y31) (2) to determine the macro- andmicronutrients necessary for cultivating E faecium Y31 andimproving Enterocin Y31 production (3) to develop a noveland simple separation and purificationmethod for EnterocinY31 (avoiding a series of chromatography steps and the lossof Enterocin Y31 activity) and (4) to compare Enterocin Y31production in a defined medium with that in a complexmediumThis is feasible using a completely defined mediumand a minimal medium for bacteriocin production can thusbe established

2 Materials and Methods

21 Strains and Growth Conditions The bacteriocin-pro-ducer strain E faecium Y31 isolated from Chinese traditionalfermented foods (fermented vegetable juice from Lanzhou)was previously found to produce class IIa bacteriocin [10]which wasmaintained as stock cultures inMRSmediumwith18 glycerol at minus80∘C

Escherichia coli ATCC 25922 was selected as a sensitivestrain for antimicrobial activity assays because the bacte-riocin produced by E faecium Y31 has the highest activityagainst E coli ATCC 25922 in gram-negative bacteria

22 Medium The growth of E faecium Y31 and productionof Enterocin Y31 in a defined medium in a fermenter werecompared with those in MRS (reference medium) used forthe optimisation of the growth of E faecium Y31 and theproduction of Enterocin Y31 This medium CDM consistedof 44 components described by Khan et al [12] (listed inTable 1) All chemicals used for the preparation of the definedmedium were of analytical grade and obtained from either

Sigma-Aldrich (St Louis MO USA) or BDH ChemicalsLtd (Poole UK) For all the experiments aqueous stocksolutions of the individual components were prepared inthe appropriate concentrations and sterilized by autoclav-ing with the exception of the heat-sensitive componentsThe heat-sensitive amino acids (asparagine glutamine andtryptophan) all of the B vitamins and FeSO

4were filter-

sterilized (pore size 022120583m membrane Millipore CorpBillerica MA USA) All the stock solutions were then storedat 4∘C except FeSO

4which was freshly prepared before each

experiment because it is prone to oxidation during storage Inaddition to the defined medium MRS medium was used asa reference for comparison with the defined medium beforeeach experiment

23 Determination of the Antimicrobial Activity of EnterocinY31 The antimicrobial activity of bacteriocin was monitoredusing the agar well diffusion assay (AWDA) as describedpreviously [16] with some modifications E faecium Y31 wascultured for two or three generations and then the cell-free supernatants (CFSs) of E faecium Y31 were preparedby centrifuging for 30min at 10000timesg Aliquots (80 120583L) ofthe cell-free supernatants (CFSs) of E faecium Y31 wereadded to the wells (6mm diameter) on double-layer agarplates previously inoculated with 02mL overnight cultureof the indicator strain E coli ATCC 25922 Plates were keptstatic at room temperature for 3 h to allow diffusion of theCFSs evenly in the agar and then the plates were incubatedfor 24 h at 37∘C The bacteriocin titre was determined byeliminating the effect of the organic acid eliminating theeffect of H

2O2 and protease verificationThe diameter of the

zone of inhibition (not including the wells) was measuredusing a Vernier caliper An arbitrary unit (AUmL) wasdefined as the reciprocal of the highest dilution that producedan inhibition zone Specific activity was expressed as that unitper milligram of protein

24 Protein Concentration Determination Protein concen-tration was determined by the BCA (bicinchoninic acid)microassay method (Pierce Rockford IL USA) [17]

25 Monitoring of the Growth of E faecium Y31 The ODvalue of the fermentation liquid of E faecium Y31 wasmonitored with UV spectrophotometry at 600 nm each hourSterile culture medium was used as blanks to subtract thebackground value Samples having an OD600 nm value ofmore than 07 were diluted with the sterile culture mediumand the corrected OD value was obtained by multiplying thedilution factor ODmax (600 nm) represents the maximumOD value of the growth of E faecium Y31 ODmax (600 nm)was calculated before any centrifugation

26 Determination of the Relative Growth Rate The relativegrowth rate was calculated according to Monod [18] Thefollowing equation was used to calculate the growth rate

120583 = [(lnOD2minus lnOD

1) divide (1199052minus 1199051)] divide 120583CDM (1)

where 120583 is the relative growth rate (hminus1) ln is the symbol fornatural logarithm and OD

1and OD

2are the corrected OD

Journal of Food Quality 3

Table 1 Composition of CDM and SDMmedium

Constituent ContentCDM SDM

Amino acids (g Lminus1)L-Asparagine 100 100L-Aspartic acid 100 mdashL-Glutamic acid 100 100L -Glutamine 100 mdashL-Cys 100 100L-Alanine 100 mdashL-Arginine 100 100Glycine 100 100L-Histidine 100 100L-Isoleucine 100 100L-Leucine 100 100L-Lysine 100 100L-Methionine 100 100L-Phenylalanine 100 100L-Proline 100 mdashL-Serine 100 100L-Threonine 100 100L-Tryptophan 100 100L-Tyrosine 100 mdashL-Valine 100 mdash

Nucleic acid bases (g Lminus1)AdemomeSO

4002 002

Guanine 002 mdashInosine 002 mdashXanthine 002 mdashUracil 002 002Thymine 002 mdashOrotic acid 002 mdash

B vitamins (mgsdotLminus1)Biotin 2000 2000Para-aminobenzoic acid 1000 mdashNicotinic acid 200 200Ca-pantothenic acid 2000 2000Riboflavin 200 200Folic acid 200 200Cyanocobalamin 200 mdashThiamine 1000 mdashPyridoxal 2000 mdash

Minerals (gsdotLminus1)Manganese sulfate 005 005Magnesium sulfate 01 010Ferrous sulfate7H

2O 002 mdash

CaCl2

mdash mdashSodium citrate 500 500Potassium dihydrogen phosphate 200 200Dipotassium hydrogen phosphate 700 700

Table 1 Continued

Constituent ContentCDM SDM

Carbon source (gsdotLminus1)Glucose 1500 1500

Others (gsdotLminus1)Tween 80 100 100Glycerol mdash mdashNaCl mdash 500

27 Effects of NaCl CaCl2 and Glycerol on the Growth of Efaecium Y31 and Enterocin Y31 Production To determine theeffects of these components 5 gL 10 gL 15 gL and 20 gLNaCl 10 gL CaCl

2 and 50 gL glycerol were individually

added to 1000mLCDM andCDMmediumwith no addtionswas used as a control wherein the inoculum size was 2fermentation temperature was 37∘C and inoculum time was24 h The culturing liquid was then centrifuged for 20minat 10000timesg and then the CFSs were used to determineEnterocin Y31 activity and ODmax (24 h)

28 Effects of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth ofE faecium Y31 and Enterocin Y31 Production According tothe Leave One Out (LOO) technique each amino acid Bvitamin mineral and nucleic acid base was sequentially andindividually omitted from 1000mLCDMmedium andCDMwithout additions was used as a control The inoculum sizewas 2 fermentation temperature was 37∘C and inoculationtime was 24 h The culture liquid was then centrifugedfor 20min at 10000timesg and then the CFSs were used todetermine Enterocin Y31 activity and ODmax (24 h)

The following terms were used to describe the rela-tionship between each medium component and growth asdetermined by the single omission technique A constituentwas considered essential if its omission resulted in less thanhalf the maximum strain growth rate and production ofbacteriocin of the positive control stimulatory when itsabsence resulted in the fact that the growth rate and thebacteriocin production was between 50 and 80 of thatobserved in complete CDM and nonessential if the growthrate and Enterocin Y31 production was 80 (or more) of thatobtained in the complete CDM

29 Purification of Enterocin Y31 E faecium Y31 was allowedto grow in the SDM (Table 1) for 24 h The cells were thenremoved by centrifugation (11800timesg 25min) The CFSswere then filtered through a 022 120583m filter (low-protein-binding HVLP filter Millipore Corp) to remove any remain-ing cells These filtered CFSs were referred to as crude bacte-riocin The crude bacteriocin was subjected to ultrafiltrationof 1 kDa and 30 kDa The retentate from the 1 kDa step wasthen subjected to Tricine-SDS-PAGE

210 Statistical Analyses All experiments were preformedseparately three times and mean plusmn standard deviation (SD)values were calculated from triplicate determinations All

4 Journal of Food Quality

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 320002

0604

081012141618202224

ODpHInhibition zone diameter (mm)

Time (h)

OD

35404550556065707580

pH

0

2

4

6

8

10

12

14

Inhi

bitio

n zo

ne (

mm

)

Figure 1 Relationship between the growth of the bacteriocinogenicstrain and Enterocin Y31 production

data were subjected to one-way analysis of variance (one-way ANOVA) Comparison of means was performed withDuncanrsquos multiple range tests Statistical significance was setat 119875 lt 005

3 Results and Discussion

31 Relationship between the Growth of the Strain andEnterocin Y31 Activity The growth of E faecium Y31 wasunrelated to EnterocinY31 activity inMRSmedium as shownin Figure 1 The result was consistent with the result ofBacterocin J23 produced by Lactobacillus paracasei J23 asdescribed by Huaxi Yi in our research group (not published)whichwas inconsistentwith the result of Salivaricin producedby L salivarius CRL 1328 [19] thus the growth rate of EfaeciumY31 and Enterocin Y31 activity were used as detectionindexes for developing a novel chemical defined mediumEnterocin Y31 activity could be detected at the exponentialphase of the producing strain (9 h) and reached its highestvalue of 1126 plusmn 036mm at stationary phase of producingstrain (24 h) ODmax remained stable at 16 h of fermentationof strain Y31 thus ODmax (16 h) was used as an index of thestrain growth status

32 Effect of NaCl Concentration on the Growth of E faeciumY31 and Enterocin Y31 Production Theeffect of NaCl at 5 gL10 gL 15 gL and 20 gL was determined in CDMwith CDMwith no additives as the control The results indicated thatthe growth of E faecium Y31 and production of EnterocinY31 were not significant difference when adding 5 gL or10 gL NaCl and 0 gL and 15 gL NaCl had no effect onthe growth of strain Y31 and production of Enterocin Y31When the concentration of NaCl was 20 the growth of Efaecium Y31 and production of Enterocin Y31 reduced whichshowed the significant difference when compared to 0 gLand 15 gL NaCl We can conclude that 20 gL NaCl have anegative effect on the growth of strain Y31 and the productionof Enterocin Y31 When the adding concentration of NaClwas 5 gL the ODmax (16 h) of E faecium Y31 was highest

150

155

160

165

170

175

180

Enterocin Y31 production (AUmg protein)

CDM

(con

trol)

bc c

bc

ab

a

b b bab

a

GR

(16B

)

ODmax (16 B)

10A

L N

aCl

15A

L N

aCl

20A

L N

aCl

5A

L N

aCl 0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 2 Effect of NaCl concentration on the growth of Enterococ-cus faecium Y31 and Enterocin Y31 production Means not sharing acommon superscript letter are significantly different fromeach other(119875 lt 005)

172 plusmn 001 and the antibacterial activity also reached themaximum value 128364 plusmn 4140AUmg protein Based thesignificant difference analysis we could conclude that 5 gLNaCl stimulated the growth of strain Y31 (119875 lt 005) andhad no effect on the production of Enterocin Y31 (Figure 2)Similar results have been reported in a study of nutritionalrequirements of L salivarius CRL 1328 producing Salivaricin[19] Considering that the condition for the growth of Efaecium Y31 was crucial 5 gL NaCl was added to the novelchemically defined medium SDM (the medium ingredientsof SDM were listed in Table 1)

33 Effect of CaCl2 and Glycerol on the Growth of E faeciumY31 and Enterocin Y31 Production The results shown inTable 2 indicated that adding 10 gL CaCl

2to CDM had no

effect on the growth of E faecium Y31 but had a negativeeffect on the production of Enterocin Y31 (119875 lt 005) whereasadding 50 gL glycerol had a slight negative effect on thegrowth of E faecium Y31 (119875 lt 005) and a negative influenceon Enterocin Y31 production (119875 lt 005)

34 Effect of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth of Efaecium Y31 and Enterocin Y31 Production According to theLeaveOneOut (LOO) technique each amino acid B vitaminmineral and nucleic acid base was sequentially omitted ina series of prepared formulations along with CDM as acontrol The results shown in Table 3 indicated that L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser and L-Cys areessential amino acids which had an effect on the growth ofE faecium Y31 and Enterocin Y31 production and the stim-ulatory amino acids mainly included L-Asn L-Glu L-Iso L-Lys and L-Try Omitting the stimulatory amino acids resultedin the slow growth of E faecium Y31 and low production

Journal of Food Quality 5

Table 2 Effects of CaCl2and glycerol on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Added components ODmax (600 nm) after 16 h Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003b 124224 plusmn 4141c

10 gL CaCl2

170 plusmn 002b 28986 plusmn 4141a

50 gL glycerol 153 plusmn 003a 56591 plusmn 4181b

Note CDM is explained in Table 1 and means in the same row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

Table 3 Effect of omitting a single amino acid on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Omitted amino acid ODmax (16 h) Relative growth rate Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003h 100 124224 plusmn 4141cd

L-Ala 150 plusmn 005g 90 122843 plusmn 6325cd

L-Arg 076 plusmn 002c ng mdasha

L-Asp 143 plusmn 004g 93 117322 plusmn 6325cd

L-Asn 091 plusmn 003d 60 122843 plusmn 8225cd

L-Cys 100 plusmn 004de 44 mdasha

L-Glu 152 plusmn 004g 72 110420 plusmn 2391c

L-Gln 171 plusmn 004h 84 124224 plusmn 5686d

L-Gly 061 plusmn 003ab ng mdasha

L-His 066 plusmn 003bc ng mdasha

L-Iso 106 plusmn 004ef 79 66252 plusmn 8251b

L-Leu 071 plusmn 003bc ng mdasha

L-Lys 116 plusmn 004f 80 62111 plusmn 4140b

L-Met 053 plusmn 002a ng mdasha

L-Phe 077 plusmn 002c ng mdasha

L-Pro 181 plusmn 003h 71 110420 plusmn 6545cd

L-Ser 049 plusmn 003a ng mdasha

L-Thr 068 plusmn 002bc ng mdasha

L-Try 112 plusmn 003ef 80 57322 plusmn 2391b

L-Tyr 170 plusmn 007h 100 120082 plusmn 3487cd

L-Val 196 plusmn 008i 98 122843 plusmn 6582cd

Note ldquongrdquo represents that the strain did not grow and ldquomdashrdquo represents that there was no inhibition activity CDM is explained in Table 1 and means in thesame row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

of Enterocin Y31 Therefore the essential amino acids andstimulatory amino acids were included in the SDM (listedin Table 1) A previous study reported the similar results asZhang et al found that six amino acids (arginine histidineisoleucine leucine methionine and valine) were necessaryfor the lactococci enterococci and streptococci [20]

Pyridoxal and pantothenic acid are essential B vitaminswhich had an effect on the growth of E faeciumY31 and Ente-rocin Y31 production and the stimulatory B vitamins mainlyincluded niacin and riboflavin Wherein the stimulatory Bvitamins could not result in the growth arrest of E faeciumY31 and the biosynthesis arrest of Enterocin Y31 they couldcause low growth rate and low biosynthesis volume There-fore the essential and stimulatory B vitamins were neededin the SDM Omitting folic acid would cause a reduction of80 in the ODmax (16 h) of E faecium Y31 therefore folicacid is also needed for the growth of E faecium Y31 and theproduction of Enterocin Y31 (Figure 3) It has been reported

that nutritional requirements of L delbrueckii ssp lactis CRL581 growthwere nicotinic acid and pyridoxal and pantothenicacid whereas the growth of L delbrueckii ssp lactis CRL654 requires niacin and pantothenic acid and riboflavinand cyanocobalamin were found to be stimulatory for bothstrains [21] Research results about S thermophilus strains(ST1 ST7 ST8 ST11 ST18 and ST21) indicated that riboflavinwas essential for the growth of all strains whereas Ca-pantothenic acid and nicotinic acid were also required [22]

In the present study MgSO4sdot7H2O was an essential min-

eral andMnSO4sdot4H2OKH

2PO4 K

2HPO4 andCH

3COONa

were stimulatory minerals which had an effect on the growthof E faecium Y31 and Enterocin Y31 production (Figure 4)The necessity of magnesium and phosphate has previouslybeen reported by other researchers for various LAB species[20 23 24]

Adenine and uracil are stimulatory nucleic acids whichhad an effect on the growth of E faecium Y31 and Enterocin

6 Journal of Food Quality

Non

e (CD

M)

Pyrid

oxal

Thia

min

e

Nia

cin

D-B

iotin

Ribo

flavi

n

Cyan

ocob

alam

in

Folic

acid

p-A

min

oben

zoic

acid

Pant

othe

nic a

cid

02040608101214161820

Omitted vitamins

f

b

f

c

f

d

e ef

a

d

b

d

b

ccd

cdcd

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 3 Effect of individually omitting each B vitamin on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Y31 production (Figure 5) No nucleic acid was essential forthe growth of E faecium Y31 and Enterocin Y31 production

35 Comparison of Enterocin Y31 Production onMRSMediumand SDM A novel chemical defined medium (SDM) wasdeveloped (Table 1 and Figures 3 4 and 5) and SDMcontainedNaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

and uracil Strain Y31 grew better on SDM than on MRSmedium (Figure 6) As shown in Figure 7 Enterocin Y31production on SDM was 16 times than that on MRS

36 Purification and Characterization of Enterocin Y31 Afterthe removal of cells from the defined medium the cell-free supernatant was subjected to ultrafiltration through a30 kDa ultrafiltration membrane The active permeate liquorwas then subjected to a second ultrafiltration step using a1 kDa NMWL The antimicrobial activity was again foundin the retentate (10240AUL) Enterocin Y31 was purified byTricine-SDS-PAGE and its molecular weight was 674 kDa(showed in Figure 8)

4 Conclusion

When culturing E faecium Y31 using novel chemical definedmedium (SDM) Enterocin Y31 production increased 16times than that on MRS The ingredients were composedof NaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-ThrL-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

Non

e (CD

M)

Am

mon

ium

citr

ate d

ibas

ic

MnS

O4 middot 4

H2O

MgS

O4 middot 7

H2O

KH2P

O4

K2H

PO4

Sodi

um ac

etat

e

0204060810121416182022

Omitted minerals

d d

b

a

b

c ce e

b

a

c

d d

Enterocin Y31 production (AUmg protein)$

GR

(16B

)$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

Figure 4 Effect of individually omitting each a mineral on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Non

e (CD

M)

Aden

ine

Gua

nine

Inos

ine

Xant

hine

Oro

tic ac

id

Ura

cil

Thym

ine

14

15

16

17

18

19

20

Omitted nucleic acid bases

d

a

c

d d d

b

d

d

abbc

d d d

a

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

Figure 5 Effect of individually omitting each a nucleic acid baseon the growth of Enterococcus faecium Y31 and Enterocin Y31production Means not sharing a common superscript letter aresignificantly different from each other (119875 lt 005)

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

uracil and glucose which were the macro- and micronu-trients needed by biosynthesis of Enterocin Y31 SDM washelpful to the growth of E faecium Y31 and EnterocinY31 production improvement In addition SDM avoided aseries of chromatography steps and the loss of Enterocin Y31

Journal of Food Quality 7

0 5 10 15 20 25 30 3500020406081012141618202224

Time (h)

SDMMRS

GR

(16B

)

Figure 6 Growth of Enterococcus faecium Y31 on MRS and SDM

0 5 10 15 20 25 30 3502468

10121416182022

Time (h)

Inhi

bitio

n zo

ne d

iam

eter

(mm

)

SDMMRS

Figure 7 Enterocin Y31 productions on MRS and SDM

Enterocin Y31

M 140 +$

30+$

20 +$

10 +$

46 +$

17 +$

Figure 8 Tricine-SDS-PAGE of Enterocin Y31 M protein marker1 Enterocin Y31

activity only two steps of ultrafiltration and Tricine-SDS-PAGE were needed to separate and purify Enterocin Y31Therefore chemically defined medium has better potentialfor improving the bacteriocin production and reducing thesteps of separation and purification Chemically definedmedia is useful for purification of not only large bacteriocinssuch as Enterocin Y31 but also small peptide bacteriocinsThe alternative use of a chemically defined medium meetsthe nutritional requirements of strains producing bacteri-ocins and therefore is an excellent alternative to reduce theload of contaminating peptides from the medium therebydecreasing the purification steps To our knowledge no suchstudies have been conducted to improve class IIa bacteriocinEnterocin Y31 production and purify Enterocin Y31

Ethical Approval

This study complies with the research ethics guidelines and itdoes not contain any studies with human or animal subjects

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article

Acknowledgments

This work was financially supported by the 60th Finan-cial Grant from China Postdoctoral Science Foundation(Grant no 2016M602534) the Youth Innovation TalentsProject of General Higher School in Guangdong Province(2016KQNCX144) and theNationalNatural Science Founda-tion of China (Grants nos 31571850 31771988 and 31701621)

References

[1] R C R Martinez M Wachsman N I Torres J G LeBlancS D Todorov and B D G D M Franco ldquoBiochemical anti-microbial and molecular characterization of a noncytotoxicbacteriocin produced by Lactobacillus plantarum ST71KSrdquo FoodMicrobiology vol 34 no 2 pp 376ndash381 2013

[2] I M Aasen T Moslashretroslash T Katla L Axelsson and I StorroslashldquoInfluence of complex nutrients temperature and pH on bacte-riocin production by Lactobacillus sakei CCUG 42687rdquo AppliedMicrobiology andBiotechnology vol 53 no 2 pp 159ndash166 2000

[3] P Alvarez-Sieiro M Montalban-Lopez D Mu and O PKuipers ldquoBacteriocins of lactic acid bacteria extending thefamilyrdquo Applied microbiology and biotechnology vol 100 no 7pp 2939ndash2951 2016

[4] F A C Martinez E M Balciunas A Converti P D Cotterand R P De Souza Oliveira ldquoBacteriocin production by Bifido-bacterium spp A reviewrdquo Biotechnology Advances vol 31 no 4pp 482ndash488 2013

[5] E F OrsquoShea P D Cotter R P Ross and C Hill ldquoStrategiesto improve the bacteriocin protection provided by lactic acidbacteriardquo Current Opinion in Biotechnology vol 24 no 2 pp130ndash134 2013

[6] A-M Zouhir E Kheadr I Tahiri J Ben Hamida and IFliss ldquoCombination with plant extracts improves the inhibitoryaction of divergicin m35 against Listeria monocytogenesrdquo Jour-nal of Food Quality vol 31 no 1 pp 13ndash33 2008

8 Journal of Food Quality

[7] J Pei Y Yuan and T Yue ldquoPrimary characterization of bacteri-ocin paracin C - A novel bacteriocin produced by Lactobacillusparacaseirdquo Food Control vol 34 no 1 pp 168ndash176 2013

[8] D Drider and S Rebuffat ldquoClassification of Bacteriocins fromGram-Positive Bacteriardquo in Prokaryotic Antimicrobial Peptidespp 29ndash53 Springer New York NY USA 2011

[9] T Aymerich H Holo L S Havarstein M Hugas M Garrigaand I F Nes ldquoBiochemical and genetic characterization of ente-rocin A from Enterococcus faecium a new antilisterial bac-teriocin in the pediocin family of bacteriocinsrdquo Applied andEnvironmental Microbiology vol 62 no 5 pp 1676ndash1682 1996

[10] W Liu L Zhang H Yi et al ldquoQualitative detection of class IIabacteriocinogenic lactic acid bacteria from traditional Chinesefermented food using a YGNGV-motif-based assayrdquo Journal ofMicrobiological Methods vol 100 no 1 pp 121ndash127 2014

[11] W Liu L Zhang J Shi et al ldquoAssessment of the safety and appli-cations of bacteriocinogenic Enterococcus faecium Y31 as anadjunct culture in North-eastern Chinese traditional fermen-tation paocairdquo Food Control vol 50 pp 637ndash644 2015

[12] H Khan S H Flint and P-L Yu ldquoDevelopment of a chemicallydefined medium for the production of enterolysin A fromEnterococcus faecalis B9510rdquo Journal of Applied Microbiologyvol 114 no 4 pp 1092ndash1102 2013

[13] M Silva d M Andrade d S A Bauermeister et al ldquoA SimpleDefined Medium for the Production of True Diketopiperazinesin Xylella Fastidiosa and Their Identification by Ultra-FastLiquidChromatography-Electrospray Ionization IonTrapMassSpectrometryrdquoMolecules vol 22 no 6 p 985 2017

[14] E Texeira J Checa A Rıal et al ldquoA New Chemically DefinedMedium for Cultivation of Streptococcus Pneumoniae SerotyperdquoJournal of Biotech Research vol 6 p 54 2015

[15] A Ricciardi R G Ianniello E Parente and T Zotta ldquoModifiedchemically definedmedium for enhanced respiratory growth ofLactobacillus casei and Lactobacillus plantarum groupsrdquo Journalof Applied Microbiology vol 119 no 3 pp 776ndash785 2015

[16] U Schillinger and K Lucke F ldquoAntibacterial activity of Lacto-bacillus sake isolated from meatrdquo Applied and EnvironmentalMicrobiology vol 55 no 8 pp 1901ndash1906 1989

[17] P K Smith R I Krohn G Hermanson et al ldquoMeasurement ofprotein using bicinchoninic acidrdquo Analytical biochemistry vol150 no 1 pp 76ndash85 1985

[18] J Monod ldquoThe Growth of Bacterial Culturesrdquo Annual Reviewsin Microbiology vol 3 no 1 pp 371ndash394 1949

[19] E V Pingitore EMHebert F Sesma andM E Nader-MacıasldquoInfluence of vitamins and osmolites on growth and bacteriocinproduction by Lactobacillus salivarius CRL 1328 in a chemicallydefinedmediumrdquoCanadian Journal of Microbiology vol 55 no3 pp 304ndash310 2009

[20] G Zhang D AMills and D E Block ldquoDevelopment of chemi-cally defined media supporting high-cell-density growth ofLactococci Enterococci and Streptococcirdquo Applied and Environ-mental Microbiology vol 75 no 4 pp 1080ndash1087 2009

[21] E M Hebert R R Raya and G S De Giori ldquoNutritionalrequirements of Lactobacillus delbrueckii subsp lactis in achemically defined mediumrdquo Current Microbiology vol 49 no5 pp 341ndash345 2004

[22] C Letort and V Juillard ldquoDevelopment of a minimal chemi-cally-defined medium for the exponential growth of Streptococ-cus thermophilusrdquo Journal of AppliedMicrobiology vol 91 no 6pp 1023ndash1029 2001

[23] N Terrade and R Mira de Orduna ldquoDetermination of theessential nutrient requirements of wine-related bacteria fromthe genera Oenococcus and Lactobacillusrdquo International Journalof Food Microbiology vol 133 no 1-2 pp 8ndash13 2009

[24] F M Saguir and M C M De Nadra ldquoImprovement of a chem-ically definedmedium for the sustained growth of Lactobacillusplantarum nutritional requirementsrdquo Current Microbiologyvol 54 no 6 pp 414ndash418 2007

Research ArticleLipid Oxidation Color Changes and MicrobiologicalQuality of Frozen Beef Burgers Incorporated with ShiraziThyme Cinnamon and Rosemary Extracts

Hadi Hashemi Gahruie Seyed Mohammad HashemHosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan Shad

Department of Food Science and Technology School of Agriculture Shiraz University Shiraz Iran

Correspondence should be addressed to Mohammad Hadi Eskandari eskandarshirazuacir

Received 3 January 2017 Revised 17 March 2017 Accepted 11 April 2017 Published 21 May 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Hadi Hashemi Gahruie et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In this study the oxidative stability of beef burgers incorporated with Shirazi thyme cinnamon and rosemary extracts wascompared with that of BHT-incorporated and antioxidant-free samples The chemical composition TBARS metmyoglobin pHcolor and microbial and sensory characteristics were evaluated during storage at minus18∘C for 2 months The results indicated thatShirazi thyme and cinnamon extracts did not change the colorimetric properties significantly (119875 lt 005) Incorporating naturalantioxidants led to a significant (119875 lt 005) reduction in TBARS (3658ndash4634) and metmyoglobin (1625ndash1847) as compared tocontrol Except for the control sample total microbial counts of burgers were lower than the maximum allowed limit Burgersformulated with Shirazi thyme revealed the lowest amount of total count Regarding the sensory characteristics the overallacceptability of different samples decreased in the order of cinnamon gt BHT gt Shirazi thyme gt rosemary gt control Finally theresults showed that these plant extracts can be utilized as an alternative to synthetic antioxidants in formulation of burgers

1 Introduction

Meat and meat products are among the most importantprotein sources in the daily diet of people living in developedcountries Beef burger is almost the most popular meatproduct consumed by millions of people from all over theworld The common processes (such as mincing cookingand salt addition) applied in the production of burgersenhance the formation of reactive oxygen species thereforethe resultant product is highly vulnerable to oxidation [1]Lipid and protein oxidations have been reported as theprincipal reason for the decreased quality of burgers duringstorage resulting in decreasing the shelf life [2ndash4]

Application of antioxidants is the best strategy to pre-vent oxidation reactions [5] Synthetic antioxidants such asBHT TBHQ and BHA have various adverse human healtheffects including allergy headache asthma and dermatitis

Therefore the application of natural antioxidants (such asherbal essential oils and extracts) is of interest and canbe observed in a growing number of research works [6ndash8](Aliakbarlu et al 2016)Moreover consumers are increasinglydemanding for green-labeled food products such as thosecontaining natural antioxidant Natural compounds can beobtained from natural sources such as plants fruits vegeta-bles oil seeds spices team honey bee pollen and cereals[9] A lot of extracts have been approved as GRAS (GenerallyRecognized as Safe) that is the addition of these chemicals orsubstances into food is considered safe by experts and theirapplication is exempted from the usual Federal Food Drugand Cosmetic Act (FFDCA) [10]

The potential of natural antioxidants in preventing thelipid oxidation in different food products has been evaluatedby many researchers around the world [11] It has beenreported that the extracts of kinnow rind pomegranate rind

HindawiJournal of Food QualityVolume 2017 Article ID 6350156 9 pageshttpsdoiorg10115520176350156

2 Journal of Food Quality

Hamburger ingredients Extracts (20 g herb + 500 ml water)

Preparation of base batter

Formula 1without additives

(control)

Formula 2with BHT(100 ppm)

Formula 3with Shirazi thyme

(22 mlkg)

Formula 4with rosemary

(28 mlkg)

Formula 5with cinnamon

(73 mlkg)

Analysis (0 15 30 45 and 60 days)

Chemical analysis

Chemical compotation(i) Moisture

(ii) Protein(iii) Fat(iv) Carbohydrate(v) Ash

Deterioration criteria(i) TBARS

(ii) pH(iii) Metmyoglobin

Microbiological analysis(i) Total aerobic bacterial count

Sensory analysis(i) Appearance

(ii) Texture(iii) Taste(iv) Odor(v) Overall acceptance

Color analysis(i) Llowast

(ii) alowast

(iii) blowast

(iv) ΔE

Production and storage at minus18∘C

Figure 1 Schematic diagram of experimental design

and seed powders were significantly able to decrease the lipidoxidation in goat meat patties [12] The effects of natural(sage and rosemary) and synthetic (BHT) antioxidants onprotein oxidation discoloration and texture of refrigeratedpatties produced from pig liver have been studied by Estevezet al [13] Authors reported that the antioxidant propertiesof natural and synthetic antioxidants were similar In treatedsamples the increase in the carbonyl content as a result ofoxidation was significantly (P lt 005) lower than controlsamples Moreover antioxidants could successfully protectheme molecules from degradation Among different naturalantioxidants it has been reported that the extracts of Shirazithyme cinnamon and rosemary reveal substantial antioxi-dant capacity [14]

The main objective of the current study was to comparethe effects of Shirazi thyme cinnamon and rosemary extracts(denoted as natural antioxidants) with those of BHT on pro-tein and lipid oxidations and physicochemicalmicrobial andsensory characteristics of frozen beef burgers during storageThe results of this study may have potential implications

in substituting the synthetic antioxidants with nature-madeones

2 Materials and Methods

A schematic representation of beef burger production isshown in Figure 1

21 Materials Beef flanks (18 fat) from freshly slaughteredanimals (24 hours post slaughter)were purchased froma localmarket (Shiraz Iran) and transported to the laboratory ininsulated polystyrene ice-boxes The meat was ground (MeatGrinder Philips HR2743 AmsterdamNetherlands) througha perforated plate with a hole diameter of 5mm Thiobar-bituric acid (Sigma-Aldrich St Louis MO USA) 1133-tetraethoxypropane (Sigma-Aldrich St Louis MO USA)and diphenyl-2-picrylhydrazyl (DPPH∙) (Sigma-Aldrich StLouisMOUSA) soy protein isolate (SPI 90 protein SonicCo India) onions salt spices and ruskwere also used in thisstudy

Journal of Food Quality 3

22 Plant Extracts Shirazi thyme (Zatariamultiflora) cinna-mon (Cinnamomum zeylanicum) and rosemary (Rosmarinusofficinalis) were purchased from a local grocery The genusand species were certified by experts from the Herbariumof Biology Department (Shiraz University Shiraz Iran)Dried plants were powdered with a mill and then kept inpolyethylene bags at room temperature before extraction

221 Extract Preparation Plant powder (20 g) was thor-oughly mixed with boiling distilled water (500mL) for5min followed by filtration through Whatman grade No 1filter papers and concentration in rotary evaporator (BuchiRotavapor R Switzerland) at 50∘C [15]

222 DPPH Radical Scavenging Activity Antioxidant activ-ity of natural extracts and BHT was calculated using DPPHfree radicalmethod described by Cam et al [16]The amountsof extracts required to replace BHT were calculated basedon the IC50 of BHTThe required amounts of natural extractsshould have equal antioxidant activity to BHT

23 Beef Burger

231 Burger Preparation and Storage The formulation ofbeef burger used in this study was composed of beef (70)onions (134) rusk (4) water (8) SPI (3) salt (1)black (03) and red (02) peppers Ground meat saltwater and minced onion were mixed together After thatSPI was added and then mixed for 15min to obtain ahomogenousmixture Rusk and spices were added in the nextstep Finally natural extracts andor BHT were incorporatedinto the homogenate and thenmixing process was continuedThe concentration of BHT was 100 ppm A burger maker(9 cm internal diameter) was used to shape the mixture intopatties of approximately 90 g and 5mm thickness Burgers(15 patties per treatment) were then packed in light-resistantpolyethylene containers and frozen at minus18∘C Analyses wereperformed during 15-day intervals for two months Beforeanalysis the samples were thawed at +4∘C and then hand-mixed for 30 s

232 Chemical Analysis Moisture protein fat and ashcontents of burgers were determined according to the AOACmethods [17] Carbohydrate content was estimated by sub-tracting the total amounts of moisture protein fat and ashfrom 100

233 pH Measurement Meat sample (10 g) was homog-enized with 50mL deionized water for 1min pH wasmeasured at room temperature using a digital pH meter(Suntex TS-1 Taiwan) equipped with a probe-type combinedelectrode (Ingold) through direct immersion of electrode intothe mixture [17]

234 Instrumental Color Evaluation Color attributes of beefburgers were measured by 119871lowast119886lowast119887lowast method described byYam and Papadakis [18] The values of 119871lowast (brightness) 119886lowast(redness-greenness) and 119887lowast (yellowness-blueness) weremea-sured on the whole outer surfaces of beef burger A wooden

box (50 times 50 times 60 cm3) equipped with a natural daylightsource (6500K) and a digital camera (CanonPowershotA540of six megapixels resolution) in a vertical position and adistance of 25 cm from the samples was used for takingphotos Adobe PhotoshopCS6 was applied to determine theaverage surface color

235 Determination of Lipid Oxidation Lipid oxidationwas monitored by measuring thiobarbituric acid reactivesubstances (TBARS) Meat sample (4 g) was homogenizedwith 20mL trichloroacetic acid solution (20 wv) and thencentrifuged at 3000119892 for 10min The supernatant (2mL) wasmixed with 2mL thiobarbituric acid solution (01 wv indouble distillated water) followed by heating in a water bathat 100∘C for 30min and then cooling to room temperatureTherefore TBARS were extracted in chilled atmosphere Theabsorbance of each extract was measured at 520 nm in aspectrophotometer (spec 1650PC Shimadzu Japan) 1133-tetraethoxypropane was used to develop the standard curvefor TBARS assay TBARS values were reported as mg ofmalonaldehyde per kg of beef burger [7]

236 Metmyoglobin Measurement A modified method ofAn et al [19] was used to measure the metmyoglobincontent in raw beef burgers The sample (4 g) was mixedin a homogenizer with 20mL of phosphate buffer (004MpH 68) and then stored at 1∘C for 1 h The mixture wasthen centrifuged at 3500119892 and 4∘C for 30min Finally thesupernatant was filtered through Whatman grade No 1filter paper The absorbance of the solution was measuredat 525 572 and 700 nm Metmyoglobin () was calculatedaccording to the following equation

Metmyoglobin () = [1395 minus [(119860572 minus 119860700)(119860525 minus 119860700)]]times 100

(1)

Total Aerobic Bacterial Count Total aerobic bacteria werequantified every 15 days using the method described byAliakbarlu et al (2016) Beef burgers (10 g) were asepti-cally transferred into individual stomaching bags containing90mL of sterile saline (09) and homogenized for 2minSerial 10-fold dilutions were prepared in saline and 100 120583Lfrom appropriate dilutions was spread on the surface of platecount agar for total aerobic count (TMC) and then incubatedat 35∘C for 24 h

237 Sensory Evaluation Sensory analyses have been per-formed by 20 trained panelists from the Department of FoodScience and Technology (Shiraz University) Panelists wereboth male and female in the age range of 23ndash28 years oldPanelists were selected based on their previous experiences inconsuming traditional beef burgers Moreover they receivea preparatory session before the sensory test to train themhow to describe all evaluated factors completely Burgers werefried at 150∘C in a forced draft oven to a core temperatureof 72∘C and kept warm in the oven for 3ndash8min until thesensory testing [20] Rectangular pieces of approximately

4 Journal of Food Quality

2 cm were cut from the center of each burger and then servedat room temperature Each panelist randomly evaluated threepieces of all formulations and asked to give a numericalvalue between 1 and 9 for the following attributes taste 1(imperceptible) to 9 (extremely intense) texture attributesand juiciness 1 (extremely dry) to 9 (extremely moist)appearance 1 (extremely soft) to 9 (extremely tough) andodor 1 (imperceptible) to 9 (extremely intense) Tap waterwas provided for panelists to rinse their mouth betweendifferent samples At the end of evaluation each panelist wasasked to give an overall score from 1 (dislike very much) to9 (like very much) for the overall acceptability of differentformulations

24 Statistical Analysis A completely randomized blockdesign with five treatments (including antioxidant-free (con-trol) treatment and those incorporated with BHT cinnamonrosemary and Shirazi thyme extracts) was used in this studyExperiments were performed during a 60-day storage periodat 15-day intervals (0 15 30 45 and 60) Independent blocks(developed from three different batches) were replicatedthree times at each sampling point A two-way analysisof variance (ANOVA) and Duncanrsquos multiple range tests(SAS 80 software SAS Institute Inc Cary NC USA) wereperformed to analyze the effect of treatments storage periodand their interaction on the physicochemical microbial andsensory characteristics of beef burgers at a confidence levelof 005 In the analysis models the treatments storage timesand their interaction were assigned as fixed effects and thereplications as random effects

The given scores of different sensory attributes werecompared between the treatments using general linear model(GLM) Duncanrsquos multiple range tests were used for compar-ison of means at a confidence level of 005 Treatments andassessors were considered as main effects and the replicationsas random effects Data was reported as mean plusmn standarderror (SE)

3 Results and Discussion

31 Antioxidant Activity of Extracts The IC50 values (definedas the concentration of an antioxidant required to reduce theinitial DPPH concentration by 50 using DPPH free radicalmethod described by Cam et al [16]) of natural extracts(including Shirazi thyme cinnamon and rosemary) andsynthetic BHT were 0022 0373 0062 and 0107mgmLrespectively Therefore the amounts of Shirazi thyme cinna-mon and rosemary concentrated extracts required to replace100 ppm BHT in formulation were 22 73 and 28mL per kgof beef burger respectively Cinnamon is a source of bioactivecompounds such as cinnamaldehyde eugenol and coumarin[21] The effect of cinnamon extract as direct scavengersof free radicals has been studied by Roussel et al [22]Carnosic acid and carnosol are the main bioactive com-pounds present in the rosemary extract [23] According toSharififar et al [24] the major chemical compounds presentin Shirazi thyme were carvacrol (3365) thymol (3759) p-cymene (772) 120574-terpinene (388) and 120573-caryophyllene(206)

40

45

50

55

60

65

70

75

80

Met

myo

glob

in (

)

15 30 45 600Storage period (days)

ControlBHTCinnamon extract

Rosemary extractShirazi thyme extract

Figure 2 Effect of incorporating Shirazi thyme cinnamon androsemary extracts on the metmyoglobin () developed in raw beefburgers during frozen storage at minus18∘C

32 Physicochemical Properties of Beef Burger The resultsindicated that the samples contained 5913 moisture 19protein 12 fat 772 carbohydrate and 2 ash

33 Color Stability When assessing meat a consumer paysa great attention to its color which as a visual impressionis induced mainly by the presence of pigments but it alsodepends on tissue composition and meat structure Hencethe color of fresh meat is an important quality parameterthat determines a consumerrsquos response and decision to buyor not to buy that product at retail Changes in 119871lowast 119886lowast and119887lowast values of beef burgers during frozen storage are shown inTable 1 No significant difference (119875 gt 005) was observedbetween the samples incorporated with natural antioxidantsand those incorporated with BHT at production time (day 0)resulting in low Δ119864 values at early stages of storage All of theformulations showed significant decrease in 119886lowast during frozenstorage Formulation incorporated with rosemary extractshowed lower amounts of 119886lowast at the end of storage timeThe significant decrease in 119886lowast values indicated the red colorreduction of products during storage this is despite the factthat BHT- and extract-incorporated treatment significantlyreduced the Met-mb development ratio in comparison tocontrol one (Figure 2) During the first 30 days of storage119871lowast values increased significantly (119875 lt 005) then remainedconstant During frozen storage changes in the amountsof 119871lowast in cinnamon- (642) or Shirazi thyme-incorporatedsamples (597) were less than those in other formulationsSamples incorporated with rosemary extract showed the leastredness (433)

A significant decrease in 119886lowast values of raw pork pat-ties containing grape seed extract and bearberry has beenreported over a 12-day storage by Carpenter et al [25]however 119887lowast values (particularly of control samples) increasedsignificantly (119875 lt 005) Similarly Nunez de Gonzalez et al[26] reported that 119886lowast value of beefs stored under refrigeration

Journal of Food Quality 5

Table 1 Effect of addition of Shirazi thyme cinnamon and rosemary extracts and BHT on 119871lowast 119886lowast 119887lowastand Δ119864 values of raw beef burgersduring frozen storage at minus18∘CParameter Sample Storage period (days)

0 15 30 45 60

119871lowastControl 6033 plusmn 088 glowastlowast 5800 plusmn 058 hi 7133 plusmn 034 abc 7167 plusmn 034 ab 7267 plusmn 067 aBHT 5867 plusmn 088 ghi 5733 plusmn 034 i 6833 plusmn 034 de 6933 plusmn 034 cd 7067 plusmn 067 abc

Cinnamon extract 6033 plusmn 067 g 5433 plusmn 034 j 5967 plusmn 067 gh 6533 plusmn 067 f 6800 plusmn 058 deRosemary extract 5733 plusmn 034 i 5433 plusmn 082 i 6967 plusmn 088 bcd 7133 plusmn 088 abc 7167 plusmn 034 ab

Shirazi thyme extract 5733 plusmn 146 i 5667 plusmn 067 i 5700 plusmn 058 i 6700 plusmn 058 ef 6833 plusmn 067 de

119886lowastControl 1133 plusmn 034 a 833 plusmn 034 de 833 plusmn 034 de 767 plusmn 034 ef 667 plusmn 034 fghBHT 1100 plusmn 058 ab 667 plusmn 034 fgh 767 plusmn 067 ef 700 plusmn 058 fg 667 plusmn 034 fgh

Cinnamon extract 933 plusmn 034 cd 733 plusmn 034 efg 667 plusmn 034 fgh 567 plusmn 034 hij 533 plusmn 034 ijkRosemary extract 1167 plusmn 034 a 533 plusmn 034 ijk 533 plusmn 034 ijk 467 plusmn 034 jk 433 plusmn 034 k

Shirazi thyme extract 1000 plusmn 058 667 plusmn 034 fgh 633 plusmn 034 ghi 567 plusmn 034 hij 533 plusmn 034 ijk

119887lowastControl 2333 plusmn 034 kl 2500 plusmn 058 ij 3233 plusmn 034 bc 3267 plusmn 067 b 3400 plusmn 058 aBHT 2233 plusmn 034 lmn 2333 plusmn 034 kl 3100 plusmn 058 cd 3133 plusmn 067 bcd 3167 plusmn 067 bcd

Cinnamon extract 2167 plusmn 034 mno 2267 plusmn 034 lm 2533 plusmn 034 ij 2600 plusmn 058 i 2767 plusmn 034 hRosemary extract 2033 plusmn 0340 2100 plusmn 058 no 2900 plusmn 058 fgh 3067 plusmn 034 de 3133 plusmn 067 bcd

Shirazi thyme extract 2300 plusmn 000 klm 2433 plusmn 034 jk 2833 plusmn 034 gh 2933 plusmn 034 efg 3033 plusmn 034 def

Δ119864lowastlowastlowastControl 000 plusmn 000 f 1700 plusmn 025 aBHT 272 plusmn 069 e 1409 plusmn 018 bc

Cinnamon extract 282 plusmn 072 e 1078 plusmn 095 dRosemary extract 442 plusmn 104 e 1559 plusmn 102 ab

Shirazi thyme extract 354 plusmn 030 e 1229 plusmn 080 cdlowastlowastData represent averages of three independent repeats plusmn standard errorslowastlowastMeans with different letters are significantly different (119875 le 005)lowastlowastlowastFor each storage time the color difference (Δ119864) was calculated by comparing the color attributes of different formulations with those of control sample

for 10 weeks decreased significantly (119875 lt 005) The resultsof the current study showed that high antioxidant activity ofnatural extracts can be potentially used to develop naturalcolor stabilizers particularly for controlling 119871lowast and 119887lowast valuesin frozen beef burger

As mentioned already samples incorporated with BHTand natural extracts did not show any significant differencein Δ119864 value at the beginning of the storage time However atthe end of storage the lowest and highest changes in Δ119864wereobserved in cinnamon-incorporated and control samplesRedmeat color is an important property of visual appearanceand could influence meat purchasing decisions more thanany other quality parametersThe color of meat products andmeat is influenced by metmyoglobin percentage in muscleInitially the myoglobin was changed into oxymyoglobin(light pink color) which could result in brighter redmeat andthen oxymyoglobin was oxidized into metmyoglobin duringstorage [7]

34 Metmyoglobin Content Assay The amount of metmyo-globin has been positively linked to the extent of proteinoxidation in meat products The heme complex of heme(in) proteins consists of iron in the ferrous state (Fe+2)which turns into the ferric state (Fe+3) via a process calledautoxidation [27] The effects of natural extracts on thechanges of metmyoglobin content are shown in Figure 2Themaximum amount of metmyoglobin (7426) was measuredin antioxidant-free samples The presence of antioxidantsresulted in a significant decrease (1625ndash1847) in the

amounts of metmyoglobin developed during storage whichwas attributed to the strong antioxidant activity An etal [19] evaluated the percent metmyoglobin of the porkjerky samples incorporated with different kimchi powderconcentrations It has been reported that the metmyoglobincontents () of the samples prepared with various kimchipowder levels (ranged from 81 to 83) were significantly(119875 lt 005) lower than that of control sample (85) [19]There was no significant difference between the amounts ofmetmyoglobin under the influence of natural extracts or BHTindicating that these natural extracts can be utilized as asubstitute for BHT to prevent discoloration

The myoglobin reactions with peroxides result in theformation of lipid oxidation promoting compounds [28]The lowest amount of metmyoglobin was measured in thesamples formulated with cinnamon extract indicating thatit was more effective than the other antioxidants (eithernatural or synthetic) in preventing metmyoglobin formationA reverse relationship between the metmyoglobin level and119886lowast value was observed in this study A decrease in 119886lowast valuescorresponding to the decreased redness of lamb meat as aresult of myoglobin oxidation (metmyoglobin formation) hasbeen reported previously [29 30]

Metmyoglobin content increased during storage Thelowest increasing rate was observed in the samples incor-porated with rosemary extract The highest amount of met-myoglobin was observed in the control sample at the endof storage Changes in the metmyoglobin content of controlsample became significant after 15 days

6 Journal of Food Quality

Table 2 Thiobarbituric acid reactive substances (TBARS) values (mg malonaldehyde per kg) of beef burger during frozen storage at minus18∘CSample Storage period (days)

0 15 30 45 60Control 012 plusmn 001lowast 015 plusmn 002 020 plusmn 002 023 plusmn 001 041 plusmn 004BHT 010 plusmn 001 013 plusmn 001 015 plusmn 002 018 plusmn 001 023 plusmn 002Cinnamon extract 011 plusmn 001 013 plusmn 001 016 plusmn 001 017 plusmn 002 024 plusmn 002Rosemary extract 011 plusmn 001 013 plusmn 002 017 plusmn 002 019 plusmn 002 022 plusmn 002Shirazi thyme extract 012 plusmn 001 014 plusmn 002 017 plusmn 002 018 plusmn 001 026 plusmn 002lowastData represent averages of three independent repeats plusmn standard errors

35 Oxidative Stability Initiation is the step in which afatty acid radical is produced Two notable initiators inoxidative stability are OH∙ and HOO∙ which combines witha hydrogen atom to make water and a fatty acid radical Thefatty acid radical is not a very stable molecule so it reactsreadily with molecular oxygen thereby creating a peroxyl-fatty acid radical This radical is also an unstable species thatreacts with another free fatty acid producing a different fattyacid radical and a lipid peroxide or a cyclic peroxide if ithad reacted with itself This cycle continues as the new fattyacid radical reacts in the same wayThe radical reaction stopswhen two radicals react and produce a nonradical speciesThe lipid oxidation leads to produce of some componentscausing off-flavors and reduced nutritional quality such asmalondialdehyde and 4-hydroxynonenal

Thiobarbituric acid test can be used to determine thesecondary products of lipid oxidation in different foods suchas meat and its products [31] Thiobarbituric acid reactivesubstances (TBARS) values of different formulations (as afunction of storage time) are shown in Table 2 Exceptfor control sample the variations in TBARS values of theother formulations revealed a similar pattern Due to theabsence of antioxidant in formulation the observed changesin TBARS values of control were significantly (119875 lt 005)higher than others (8636 higher than rosemary) Natu-ral extracts were as effective as BHT for preventing lipidoxidation in beef burgers This observation indicated thatnatural herbal extracts are suitable replacers for syntheticantioxidant It has been reported that rosemary oleoresin(7704) and a mixture of BHT and BHA (7869) wasequally efficient in inhibiting the lipid oxidation of breakfastsausage containing 25 turkey meat [32] These findings arealso in good agreement with those of Mielnik et al [33] whoreported lower TBARS values after cooking of mechanicallydeboned turkey meat already stored in dark cold and treatedwith rosemary (8834) and grape seed extracts (8383)Sanchez-Escalante et al [34] reported that incorporatingrosemary essential oil into beef patties led to a significant(119875 lt 005) decrease (6400) in TBARS values during coldstorage The essential oil of rosemary was also effective inpreventing (7243) the rancidity of heat-treated turkeymeatproducts [35] It has also been reported that rosemary extractaddition into deboned poultry meat can protect (9820) theproduct from cooking-induced oxidation [36]

Regardless of sample type examined TBARS valuesincreased significantly during the frozen storage and reached

43

45

47

49

51

53

55

57

59

Tota

l aer

obic

bac

teria

l cou

nt (l

og cf

ug)

15 30 45 600Storage period (Days)

52

53

54

55

56

57

58

59

6

61

pH

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

Figure 3 Total aerobic bacterial count (log cfug) (solid symbols)and pH value (open symbols) of different beef burger formulationsas a function of storage time

to a maximum amount of 041mg malonaldehyde per kg inantioxidant-free (control) sample after 60 days At TBARSvalues of 20 off-flavors are definitely detectable and themeatis considered to be unacceptable [37]

36 Changes in pH Values Changes in pH values of beefburgers during frozen storage are shown in Figure 3 Allformulations revealed relatively similar pH values just afterproduction ranging from 588 to 593 coinciding with theISIRI 2008 Mohamed and Mansour [38] similarly reportedthat no significant differences (119875 gt 005) were observed in thepH values of beef patties after incorporating natural herbalextracts

A downward pattern of different rates was observed in thepH values of all formulations during frozen storage As nomicrobial growth was expected during storage the decreasein the pH values could be attributed to the microbial growthduring thawing (by consuming sugar and producing organicacids) Control sample had the lowest pH (551) at the end ofstorage Emiroglu et al [39] reported that the pH values of

Journal of Food Quality 7

all fresh ground beef patty samples treated with thyme andoregano generally decreased after sixth day of storage (119875 gt005)

Also the result showed that to decrease pH amount oflipid oxidation and metmyoglobin significantly increasedLapidot et al (2005) evaluated lipid peroxidation of grilledred turkey muscle (Donor Kabab) as affected by pH In thisstudy they show indeed that lipid peroxidation and myo-globin of a real fast food (turkey Doner Kebab shawarma) issignificantly more rapidly oxidized at pH 30 than at pH 50

37 Microbial Growth As shown in Figure 3 total aerobicbacterial counts of antioxidants-incorporated formulationswere not significantly (119875 lt 005) different The highestamount of total count was observed in control sample(Figure 3) Shirazi thyme-incorporated beef burgers had thelowest microbial count which could be attributed to thehigh antimicrobial properties resulting from thymol and car-vacrol The antibacterial mechanism of thymol and carvacrolis the disruption of the cytoplasmic membrane which raisesits permeability and depolarizes its potential Total countof frozen raw beef burger should be lower than 6 log cfug[40] Except for the control sample the microbial counts ofbeef burgers were lower than the maximum allowed countA relatively good correlation was observed between the pHvalues and total aerobic counts For example control samplehad the lowest pH and the highestmicrobial count Rosemaryextract (1000 ppm) inhibitory effect on the microbial growthof surface-applied beef steaks has been reported by Djenaneet al [41] However Sanchez-Escalante et al [34] reportedthat rosemary did not affect the microbial counts of beefpatties during storage (3 logCFUg)

An increase in the microbial counts was observed duringstorage but not beyond the standard range As a rule ofthumb in good manufacturing and hygienic practices duringpreparation of beef burger and its related products rapidand proper storage is important for decreasing the microbialgrowth and enhancing the shelf life

Vieira et al [42] studied the effect of frozen storage condi-tions (temperature and length of storage) on microbiologicaland sensory quality of rustic crossbred beef at different statesof ageing The result showed that psychrotrophic bacteriaincreased (138 logCFUg) significantly during 90-day storage38 Sensory Properties Color flavor and texture are themostimportant sensory attributes which influence the acceptabil-ity of meat products by consumers [43] Sensory evaluationresults of cooked beef burgers are shown in Figure 4 Gener-ally incorporating Shirazi thyme cinnamon and rosemaryextracts into beef burger formulations had no significantinfluence on the sensory properties Although samples for-mulated with Shirazi thyme and cinnamon extracts with6944 and 7167 acceptability obtained the highest tastescores by panelists (119875 lt 005) The antioxidant prop-erties of natural extracts were the main reason for theincreased sensory scores of natural extract-incorporatedformulations through preventing the formation of oxidation-mediated off-flavors and off-odors (short-chain aldehydes

4

45

5

55

6

65

7Appearance

Taste

OdorTexture

Overall

ControlBHTRosemary extract

Shirazi thyme extractCinnamon extract

Figure 4 Sensory evaluation of different beef burger formulationsa 9-point descriptive scale (1 = extremely poor and 9 = highlyacceptable) was used during evaluation

and ketones) during storage Moreover the presence ofpleasant volatile constituents in natural extracts (particu-larly in cinnamon and Shirazi thyme) led to an increasedsensory score in comparison to the BHT-incorporatedformulation

A significant increase in the flavor scores of beef pattiesincorporated with antioxidant mechanically deboned poul-try meat during frozen storage was similarly reported byMohamed and Mansour [38]

4 Conclusion

This work aimed to study the possible replacement ofsynthetic antioxidant BHT with natural extracts (includingShirazi thyme cinnamon and rosemary extracts) in beefburger formulation Different samples were prepared thendifferent characteristics such as protein and lipid oxidationand physicochemical microbial and sensory properties wereevaluated during frozen storage Herbal extracts could inhibitthe lipid oxidation in formulated burgers Moreover it wasdemonstrated that natural herbal extracts were generallybetter than BHT in preventing the lipid and protein oxi-dations as well as improving the sensory attributes of beefburgersTherefore it can be concluded that natural extracts ofShirazi thyme (0022mgmL) cinnamon (0373mgmL) androsemary (0062mgmL) can be used as natural substitutesfor BHT (0107mgmL)This substitutionmay have potentialimplication for developing green-labeled meat product Infuture studies it would be informative to study the effect ofmixed extracts and their possible synergistic or antagonisticeffects in extending the shelf life of meat products

8 Journal of Food Quality

Additional Points

Practical Applications Beef burger containing natural antiox-idant is one of themost important functional food for humanconsumption attributable to its nutritional properties andhealth effects However the nutraceutical properties of thisfood have improved due to alternative BHT with extractsThe present investigation demonstrated the effects of addingvarious natural antioxidants to the beef burger so as tomonitor the changes that occur to the physicochemicalantimicrobial and sensorial properties of the beef burger

Conflicts of Interest

The authors declare that they have no conflicts of interest

Acknowledgments

This research project was financially supported by ScientificAffairs Shiraz University and Department of Food Scienceand Technology Shiraz University Shiraz Iran

References

[1] D Ladikos and V Lougovois ldquoLipid oxidation in muscle foodsa reviewrdquo Food Chemistry vol 35 no 4 pp 295ndash314 1990

[2] C JMussinan andM JMorello ldquoFlavor analysis developmentsin isolation and characterizationrdquo American Chemical Societypp 343ndash358 1998

[3] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWTmdashFoodScience and Technology vol 68 pp 385ndash390 2016

[4] G Comi E Tirloni D Andyanto M Manzano and LIacumin ldquoUse of bio-protective cultures to improve the shelf-life and the sensorial characteristics of commercial hamburg-ersrdquo LWTmdashFood Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[5] F Shahidi ldquoAntioxidants in food and food antioxidantsrdquoFoodNahrung vol 44 pp 158ndash163 2000

[6] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[7] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[8] H H Hashemi Gahruie M H Eskandari G Mesbahi andM A Hanifpour ldquoScientific and technical aspects of yogurtfortification a reviewrdquo Food Science and Human Wellness vol4 no 1 pp 1ndash8 2015

[9] K Yamazaki S Kawamorita H Ohmiya and M SawamuraldquoDirected ortho borylation of phenol derivatives catalyzed by asilica-supported iridium complexrdquo Organic Letters vol 12 no18 pp 3978ndash3981 2010

[10] A Roberts and L A Haighton ldquoA hard look at FDArsquos review ofGRAS noticesrdquo Regulatory Toxicology and Pharmacology vol79 pp S124-S128 2016

[11] H H Hashemi Gahruie E Ziaee M H Eskandari andS M Hosseini ldquoCharacterization of basil seed gum-basededible films incorporated with Zataria multiflora essential oilnanoemulsionrdquo Carbohydrate Polymers vol 166 pp 93ndash1032017

[12] S K Devatkal K Narsaiah and A Borah ldquoAnti-oxidant effectof extracts of kinnow rind pomegranate rind and seed powdersin cooked goatmeat pattiesrdquoMeat Science vol 85 no 1 pp 155ndash159 2010

[13] M Estevez R Ramırez S Ventanas and R Cava ldquoSage androsemary essential oils versus BHT for the inhibition of lipidoxidative reactions in liver paterdquo LWTmdashFood Science andTechnology vol 40 no 1 pp 58ndash65 2007

[14] E Abdollahzadeh M Rezaei and H Hosseini ldquoAntibacterialactivity of plant essential oils and extracts the role of thymeessential oil nisin and their combination to control listeriamonocytogenes inoculated in minced fish meatrdquo Food Controlvol 35 no 1 pp 177ndash183 2014

[15] A Alaklabi I A Arif A Ahamed R Surendra Kumar andA Idhayadhulla ldquoEvaluation of antioxidant and anticanceractivities of chemical constituents of the saururus chinensis rootextractsrdquo Saudi Journal of Biological Sciences 2017

[16] M Cam Y Hısıl and G Durmaz ldquoClassification of eightpomegranate juices based on antioxidant capacity measured byfourmethodsrdquo FoodChemistry vol 112 no 3 pp 721ndash726 2009

[17] AOAC Association of Official Agricultural Chemists ldquoOfficialmethods of analysis of AOAC Internationalrdquo in AgricultureChemicals Contaminants Drugs vol 1 AOAC InternationalArlington VA USA 16th edition 1995

[18] K L Yam and S E Papadakis ldquoA simple digital imagingmethodfor measuring and analyzing color of food surfacesrdquo Journal ofFood Engineering vol 61 no 1 pp 137ndash142 2004

[19] K-I An J-H Choi Y-S Choi et al ldquoEffects of kimchi powderon quality characteristics of semi-dried pork jerkyrdquo KoreanJournal for Food Science of Animal Resources vol 30 no 2 pp198ndash205 2010

[20] B Kodal Coskun E Calikoglu Z Karagoz Emiroglu and KCandogan ldquoAntioxidant active packaging with soy edible filmsand oregano or thyme essential oils for oxidative stability ofground beef pattiesrdquo Journal of Food Quality vol 37 no 3 pp203ndash212 2014

[21] B Shan Y Z Cai M Sun and H Corke ldquoAntioxidant capacityof 26 spice extracts and characterization of their phenolicconstituentsrdquo Journal of Agricultural and Food Chemistry vol53 no 20 pp 7749ndash7759 2005

[22] A-M Roussel I Hininger R Benaraba T N Ziegenfuss andR A Anderson ldquoAntioxidant effects of a cinnamon extract inpeople with impaired fasting glucose that are overweight orobeserdquo Journal of the American College of Nutrition vol 28 no1 pp 16ndash21 2009

[23] S Moreno T Scheyer C S Romano and A A VojnovldquoAntioxidant and antimicrobial activities of rosemary extractslinked to their polyphenol compositionrdquo Free Radical Researchvol 40 no 2 pp 223ndash231 2006

[24] F Sharififar M H Moshafi S H Mansouri M Khodashenasand M Khoshnoodi ldquoIn vitro evaluation of antibacterial andantioxidant activities of the essential oil and methanol extractof endemic Zataria multiflora Boissrdquo Food Control vol 18 no7 pp 800ndash805 2007

[25] R Carpenter M N OrsquoGrady Y C OrsquoCallaghan N M OrsquoBrienand J P Kerry ldquoEvaluation of the antioxidant potential of grape

Journal of Food Quality 9

seed and bearberry extracts in raw and cooked porkrdquo MeatScience vol 76 no 4 pp 604ndash610 2007

[26] M T Nunez de Gonzalez B S Hafley R M Boleman R KMiller K S Rhee and J T Keeton ldquoAntioxidant propertiesof plum concentrates and powder in precooked roast beef toreduce lipid oxidationrdquo Meat Science vol 80 no 4 pp 997ndash1004 2008

[27] M P Richards and M A Dettmann ldquoComparative analysisof different hemoglobins autoxidation reaction with peroxideand lipid oxidationrdquo Journal of Agricultural and FoodChemistryvol 51 no 13 pp 3886ndash3891 2003

[28] J Everse and N Hsia ldquoThe toxicities of native and modifiedhemoglobinsrdquo Free Radical Biology and Medicine vol 22 no6 pp 1075ndash1099 1997

[29] C Kennedy D J Buckley and J P Kerry ldquoInfluence of differentgas compositions on the short-term storage stability of mother-packaged retail-ready lamb packsrdquo Meat Science vol 69 no 1pp 27ndash33 2005

[30] J P Kerry M G OrsquoSullivan D J Buckley P B Lynch andP A Morrissey ldquoThe effects of dietary 120572-tocopheryl acetatesupplementation and modified atmosphere packaging (MAP)on the quality of lamb pattiesrdquo Meat Science vol 56 no 1 pp61ndash66 2000

[31] J Fernandez J A Perez-Alvarez and J A Fernandez-LopezldquoThiobarbituric acid test for monitoring lipid oxidation inmeatrdquo Food Chemistry vol 59 no 3 pp 345ndash353 1997

[32] S Barbut D B Josephson and A J Maurer ldquoAntioxidantproperties of rosemary oleoresin in Turkey sausagerdquo Journal ofFood Science vol 50 no 5 pp 1356ndash1359 1985

[33] M B Mielnik K Aaby and G Skrede ldquoCommercial antioxi-dants control lipid oxidation in mechanically deboned turkeymeatrdquoMeat Science vol 65 no 3 pp 1147ndash1155 2003

[34] A Sanchez-Escalante D Djenane G Torrescano J A Beltranand P Roncales ldquoThe effects of ascorbic acid taurine carnosineand rosemary powder on colour and lipid stability of beef pattiespackaged in modified atmosphererdquoMeat Science vol 58 no 4pp 421ndash429 2001

[35] M B Mielnik S Sem B Egelandsdal and G Skrede ldquoBy-products from herbs essential oil production as ingredient inmarinade for Turkey thighsrdquo LWTmdashFood Science and Technol-ogy vol 41 no 1 pp 93ndash100 2008

[36] J H Macneil P S Dimick and M G Mast ldquoUse of chemicalcompounds and a rosemary spice extract in quality mainte-nance of deboned poultry meatrdquo Journal of Food Science vol38 no 6 pp 1080-1081 1973

[37] E TEC ldquoMeat technology update 1-6 2009rdquo[38] H M H Mohamed and H A Mansour ldquoIncorporating

essential oils of marjoram and rosemary in the formulation ofbeef patties manufactured with mechanically deboned poultrymeat to improve the lipid stability and sensory attributesrdquoLWTmdashFood Science and Technology vol 45 no 1 pp 79ndash872012

[39] Z K Emiroglu G P Yemis B K Coskun and K CandoganldquoAntimicrobial activity of soy edible films incorporated withthyme and oregano essential oils on fresh ground beef pattiesrdquoMeat Science vol 86 no 2 pp 283ndash288 2010

[40] ISIR Raw frozen hamburgermdashSpecifications vol 2304 Instituteof standards and industrial research of Iran Karaj Iran 3rdedition 2008

[41] DDjenane A Sanchez-Escalante J A Beltran andP RoncalesldquoAbility of 120572-tocopherol taurine and rosemary in combination

with vitamin C to increase the oxidative stability of beef steakspackaged in modified atmosphererdquo Food Chemistry vol 76 no4 pp 407ndash415 2002

[42] C Vieira M T Diaz B Martınez and M D Garcıa-CachanldquoEffect of frozen storage conditions (temperature and lengthof storage) on microbiological and sensory quality of rusticcrossbred beef at different states of ageingrdquo Meat Science vol83 no 3 pp 398ndash404 2009

[43] J Aliakbarlu and S Khalili Sadaghiani ldquoEffect of avishaneshirazi (zataria multiflora) and clove (syzygium aromaticum)essential oils on microbiological chemical and sensory proper-ties of ground sheep meat during refrigerated storagerdquo Journalof Food Quality vol 38 no 4 pp 240ndash247 2015

Research ArticleOptimization of Ultrasound Extraction of Cactus Pear(Opuntia ficus indica) Seed Oil Based on AntioxidantActivity and Evaluation of Its Antimicrobial Activity

Mariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-CansinoErnesto Alaniacutes-Garciacutea Luis Delgado-Olivares Joseacute Alberto Ariza-OrtegaEsther Ramiacuterez-Moreno and Joseacute de Jesuacutes Manriacutequez-Torres

Centro de Investigacion Interdisciplinario Area Academica de Nutricion Instituto de Ciencias de la Salud Universidad Autonoma delEstado de Hidalgo Circuito Actopan-Tilcuautla SN Ex Hacienda La Concepcion 42160 San Agustın Tlaxiaca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 20 February 2017 Accepted 9 April 2017 Published 27 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Marıa de los Angeles Ortega-Ortega et alThis is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The purpose of the present study was to determine the optimal ultrasound conditions (amplitude level and time) for the extractionof cactus pear seed oil with the highest antioxidant activity using a closed system Seed oil was analyzed for yield antioxidant activityby ABTS and DPPH and antimicrobial activity Conventional extraction methods were assessed for comparison Amplitude levelsignificantly affected antioxidant activity in linear terms (p lt 00001 DPPH and p lt 0001 ABTS resp) so at lower amplitudes thehigher antioxidant activity was achieved The optimum ultrasound extraction conditions were of 78 amplitude for 10min andyielded antioxidant activity values of 6625mg AAE100 g and 289120583mol TE100 g for ABTS and DPPH respectively Comparedwith conventional extraction methods ultrasound exhibited lower oil yield and antioxidant activity but had the potential toachieve comparable results if multiple ultrasound extractions are performed in the time needed by conventional methods Seed oilsshowed similar antimicrobial activity despite the extraction method and were more effective against Escherichia coli The resultsdemonstrated that ultrasound can be an alternative extraction method of seed oils from fruits such as cactus pear

1 Introduction

Cactus pear fruit (Opuntia ficus indica) is common in aridand semiarid regions around the world [1] This fruit that ismainly consumed fresh in Mexico [2] is composed by pulppeel and seeds [3] According to several studies cactus pearfruit has bioactive compounds [4 5] with high antioxidantand antimicrobial activity [6 7] Some of these compoundsare found in the seeds [8] which comprise 3 to 15 of thecactus pear pulp [9] and are usually considered waste afterpulp processing [7] Seeds also have a high content of oil(988 gkg) [10] characterized by high levels of linoleic andoleic acids [7] and other components as phenols [11] all whichmay contribute to humanhealth [12] Currently seed oils havebeen used as natural agents for food preservation [13] andmany have exhibited antimicrobial and antioxidant activity

some of these oils are from pumpkin [14] apple [15] blackcumin [16] and basil [17] among other seeds Cactus pearseeds fromOpuntia dillenii also have a high antioxidant activ-ity derived from bioactive compounds such as polyphenolsand polyunsaturated fatty acids [18] Some polyunsaturatedfatty acids have also been identified in seeds from Opuntiaficus indica [19 20] implying that these seeds may also havehigh antioxidant activity

Seed oil is usually extracted by means of conventionalmethods such as Soxhlet and maceration using heat agita-tion or long extraction times [21] Microwave supercriticalfluids and ultrasonic assisted extraction are unconventionalmethods that exert a physical effect on the sample [22]Ultrasound has been used to extract antioxidants frommanyfood materials including seeds Ultrasound and ultrasound-assisted extractions use sound waves to produce cavitation

HindawiJournal of Food QualityVolume 2017 Article ID 9315360 9 pageshttpsdoiorg10115520179315360

2 Journal of Food Quality

microbubbles that collapse violently in the sample and facili-tate the release and extraction of several compounds [23ndash25]Some researchers had evaluated ultrasound-assisted extrac-tion in an open system using a sonicator probe directly onthe liquid sample to obtain seed oil fromflaxseed [26] Koreanpine [27] and pomegranate [28] The purpose of the presentstudy was to optimize the extraction conditions of cactuspear seed oil using ultrasound in a closed system based onantioxidant activity and using response surfacemethodologyYield extraction and antioxidant and antimicrobial activitywere compared with conventional methods

2 Materials and Methods

21 Sample Green cactus pear (Opuntia ficus indica) Reynavariety was provided by the Mexican Association CoMeN-Tuna (Consejo Mexicano del Nopal y la Tuna AC ofActopanHidalgoMexico) in spring of 2012Thegreen cactuspear seeds were obtained after several washes with water thatremoved the pulp and residues The seeds were leaved todry at ambient temperature until they reached a moisture of643 After the seeds were crushed using an industrial mill(Cyclotec 1093 Tecator Hoganas AB Sweden) the powderwas passed through a mesh sieve to obtain a particle size ofapproximate 05mm and then stored in sealed plastic bags atroom temperature and dark conditions

22 Ultrasound Extraction Ultrasound (VCX-1500 Sonic ampMaterials Inc Newtown CTUSA) at 1500Wwith a constantfrequency of 20 kHz and a probe of 25mm was used forthe extraction of green cactus pear seeds oil Extractionfrom milled and sieved seeds (20 g) was carried out at anamplitude and time ranges of 80 to 90 and 5 to 15minrespectively and a fixed outlet temperature of 25∘C A sampleof 400mL was introduced in a jacketed vessel with waterat 4∘C circulating through the secondary layer [29] Afterextraction the aqueous and solid phases were separatedby filtration using a vacuum pump (DOA-P704-AA GASTManufacturing Inc BentonHarbor MI USA) Both phasesaqueous and solid (this last was dried) (Weston 74-1001-wWeston Products LLC Strongsville OH USA) were mixedwith hexane for 30min and then separated from the solventby filtration The aqueous phase was centrifuged (Allegra25R Beckman Couler CA USA) at 10000 rpm for 30minat 4∘C and was stored in plastic containers and kept frozenuntil analysis The solid phase was stored in hermeticallysealed bags in the dark The solvent obtained from the twophaseswas evaporated (BUCHILabortechnikAG Flawil SGSwitzerland) at 40∘C to obtain the oil

23 Soxhlet Extraction Soxhlet extraction was performedaccording to the AOAC [30] Milled and sieved seeds (5 g)hexane (120mL) and a universal fat extraction system (BuchiLabortechnik AG Flawil SG Switzerland) were used

24 Maceration Extraction Milled and sieved seeds (10 g)were introduced in a previously defatted cotton bag andthen immersed in 200mL of hexane in a closed glass at atemperature of asymp25∘C After the sample was stored in a dark

place for 24 hrs the oil was obtained after solvent evaporationusing a rotary evaporator (BUCHI Labortechnik AG FlawilSG Switzerland) at 40∘C

25 Yield Oil yield was determined according to Chouguiet al [31] using the following equation

Oil () = (1198721 minus11987201198722 ) times 100 (1)

where1198720 is the weight of the empty Eppendorf tube (g)1198721is the weight of the Eppendorf tube after evaporation (g) and1198722 is the weight of the milled seeds (g)

The oil was stored in 2mL amber Eppendorf tubes atminus32∘C until analysis

26 Determination of Antioxidant Activity

261 ABTS Assay Antiradical capacity by ABTS was mea-sured according to Kuskoski et al [32] The radical cation221015840azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) diam-monium salt (ABTS∙+) was produced by reacting 7mMABTSstock solution with 245mM potassium persulfate in thedark at room temperature for 16 hrs before being used TheABTS∙+ solution was diluted with deionized water to anabsorbance of 070 plusmn 010 at 754 nm An aliquot of 20120583L ofsample was added to 980120583L of the diluted ABTS∙+ solutionand absorbance readings were taken after 7min incubationat room temperature The absorbance of the mixture wasmeasured at 754 nm in themicroplate reader (PowerWaveXSUV-Biotek software KC Junior VT USA) and antioxidantcapacity was expressed as mg ascorbic acid equivalent per100 g of oil (mg AAE100 g)

262 DPPH Assay Antiradical activity was measured using11-diphenyl-2-picrylhydrazyl (DPPH∙) radical as describedby Morales and Jimenez-Perez [33] A methanol-acetatesolution (74mg100mL) of the stable DPPH∙ radical wasprepared A sample aliquot of 100120583Lwas placed into vials and500 120583L of DPPH∙ solution was added before the mixture wasleft to sit at room temperature for 1 hr Finally absorbancewasmeasured at 520 nm in the microplate reader (Power WaveXS UV-Biotek software KC JuniorWinooski VT USA) andantioxidant activity was expressed as 120583mol of Trolox equiva-lents per 100 g of oil (120583mol TE100 g)

27 Experimental Design

271 Optimization The optimization of the ultrasoundextraction conditions was performed using the responsesurface methodology (RSM) with a central composite rotat-able design for two independent extraction variables at fivelevelsThe independent extraction variables (amplitude level80ndash90 time 5ndash15min) were determined based on prelimi-nary experiments where higher antioxidant activity by ABTSand DPPH was observed Design consisted in thirteen com-binations with five central points replicates (Table 1) Exper-imental data were subjected to multiple nonlinear regression

Journal of Food Quality 3

Table 1 Experimental design matrix

Numbera Pattern Amplitude level () Time (min)119883119894 119883119895

(1) 00 85 10(2) +minus 90 5(3) ++ 90 15(4) 00 85 10(5) A0 92 10(6) minusminus 80 5(7) 00 85 10(8) a0 78 10(9) 0A 85 17(10) minus+ 80 15(11) 00 85 10(12) 00 85 10(13) 0a 85 3aNonrandomized

analysis (JMP 702 SAS Institute Inc Cary NC USA) fittedto a second-order polynomial model

119884 = 1205730 +2

sum119894=1

120573119894119883119894 +2

sum119894=1

1205731198941198941198832119894 +sum119894

sum119895=119894+1

120573119894119895119883119894119883119895 (2)

where 119884 is the predicted response 1205730 is the constant coeffi-cient120573119894 is the lineal coefficient120573119894119894 is the quadratic coefficientand120573119894119895 is the interaction coefficients In thismodel119883119894 and119883119895are the independent extraction variables amplitude level ()and time (min) respectively

The adequacy of themathematicalmodel was determinedusing the coefficient 1198772The significance of the model regres-sion coefficients was evaluated using an analysis of varianceThree-dimensional curves from the response surface plotswere obtained to interpret the effects of the interactionbetween independent variables on the response variablesContour plots were generated to represent the extrapolationand interpret the optimization of the extraction variablesusing the Sigma Plot 123 graphing software (SYTAT softwareInc Richmond CA USA)

272 Treatment Comparison Comparison between extrac-tion methods (ultrasound-optimized Soxhlet and macera-tion) was carried out by a one-way analysis of variance(ANOVA) All determinations were performed in triplicateand significant differences between means were determinedby Duncan test (p le 005) using the SPSS program (150 SPSSInc Chicago IL USA)

28 Scanning Electron Microscopy Scanning electron micro-scopy (SEM) was used to examine the morphological alter-ations caused to the cactus pear seeds before and after theultrasound extraction Samples deposited on the siliconwaferwere coated with a thin layer of gold (Denton VacuumDesk V Moorestown NJ USA) applying 20 millitorr and

20mA during 4min Samples were observed in a scanningelectronic microcopy (JEOL JSM-6300 Peabody MA USA)at 1000 and 500 amplifications and micrographs were takento establish the structural comparison between both samples

29 Antimicrobial Activity The green cactus pear seed oilwas tested against one Gram-positive bacteria Staphylococ-cus aureus (ATCC 1654) and two Gram-negative bacteriaEscherichia coli (ATCC 25922) and Pseudomonas aeruginosa(ATCC 27853) All microorganisms were obtained from theMexicanMicrobial Culture Collection of CINVESTAV of theNational Polytechnic Institute (Mexico) For each microor-ganism bacterial suspensions were made in a soybean-casein digest medium to a concentration of approximately108 CFUmL

To evaluate the antimicrobial activity and the mini-mum inhibitory concentration (MIC) the disk diffusionmethod was used Each bacterial suspension (100 120583L fromthe 108 CFUmL) was spread on prepared agar plates (sterileStandardMethodsAgar for bacteria) Filter sterile paper discs(6mm in diameter) were impregnated with 6667 50 3333and 1667 120583L of the undiluted oil and were placed on theinoculated plates The negative control was hexane whileampicillin (10 120583g) and streptomycin (10 120583g) were used aspositive controls The plates where incubated at 37∘C (ArsaAR-130 Felisa Jalisco Mexico) for 24 hrs The diameters ofthe inhibition zones were measured in millimeters and theresults of MIC were expressed as 120583g120583L

3 Results and Discussion

31 Extraction Yield Table 2 shows the oil yields achievedby the ultrasound treatments The extraction yield variedfrom 375 to 6 and the maximum yield was obtained at thehighest amplitude level of 92 Oil yield strongly dependedon amplitude level probably because at high amplitudes thecavitation effect increases [21] and induces physical changeson the structure of the seed such as disruption of the cell wallsreduction of the particle size and increase of exposure areaThese conditions may facilitate the penetration of the solventand thus the extraction of oil [26 28 34] The maximumyield was achieved after 10min of treatment and longertimes (15min) at high amplitudes (90) did not increase oilextraction (Table 2) Albeit time is an important variable afteryield reaches a peak a longer treatment does not maximizeextraction the same was described by Zhang et al [27] forKorean pine seed who demonstrated that oil yield increasedwith time but when it reached amaximum yield equilibratedand then decreased gradually This may be attributed to aninitial complete fracture of the cell walls during the firstminutes of the cavitation effect [26 28 34]

32 Antioxidant Activity of Green Cactus Pear Seed OilExtracted by Ultrasound Due to the complexity of theoxidation processes it is advisable to performmore than onemethod to obtain the antioxidant profile of a sample [35]In order to determine the antioxidant activity of the green

4 Journal of Food Quality

Table 2 Extraction yield and antioxidant activity of green cactus pear seed oil extracted by ultrasound under different conditions

Extraction conditions Antioxidant activity

Amplitude level () Time (min) Oil yield () ABTS DPPHmg AAE100 g 120583mol TE100 g

85 10 575 plusmn 003 6615 plusmn 407 24610 plusmn 09290 5 415 plusmn 001 5598 plusmn 313 14176 plusmn 39090 15 485 plusmn 002 5993 plusmn 445 16702 plusmn 11485 10 525 plusmn 001 6812 plusmn 659 23601 plusmn 32292 10 600 plusmn 006 5584 plusmn 236 10163 plusmn 46880 5 525 plusmn 001 6607 plusmn 217 26707 plusmn 73785 10 375 plusmn 000 6837 plusmn 392 24505 plusmn 23778 10 540 plusmn 010 6599 plusmn 501 28926 plusmn 02685 17 560 plusmn 006 6578 plusmn 037 26009 plusmn 13380 15 540 plusmn 000 6691 plusmn 320 28496 plusmn 09385 10 575 plusmn 000 6773 plusmn 040 27755 plusmn 17185 10 530 plusmn 010 6744 plusmn 389 24508 plusmn 29285 3 550 plusmn 010 6763 plusmn 000 25005 plusmn 199plusmn standard deviation

Table 3 Antioxidant activity regression coefficients of the ultra-sound extraction conditions

Coefficient ABTS DPPH1205730 67562964a 24996199a

120573119894 minus3927762b minus6357459a120573119895 02724311 71702572120573119894119895 077572 18421052120573119894119894 minus3719624b minus2977102b120573119895119895 minus0826106 004258041198772adj 093 096120573119894 amplitude level 120573119895 time significance levels a119901 lt 00001 b119901 lt 0001

cactus pear seed oil two parameters were evaluated antiox-idant and scavenging capacity by ABTS and DPPH respec-tively The results and experimental design are described inTable 2 Antioxidant activity ranged from 5584 to 6837mgAAE100 g for ABTS and 10163 to 28926120583mol TE100 g forDPPH A 1198772 value closest to one or at least of 080 indicates agood fit of themodel [36]The1198772 values for ABTS andDPPHwere 093 and 096 respectively (Table 3) indicating thatthe averages obtained adjusted to the mathematical responsesurface model

33 Effect of Ultrasound Extraction Conditions on the Antiox-idant Activity of Cactus Pear Seed Oil In this study asecond-order polynomial model for predicting the antiox-idant activity of green cactus pear seed oil was obtainedby multiple linear regression analysis of the experimentaldata Table 3 shows the regression coefficients and significantprobabilities of the linear quadratic and interaction effects ofthe ultrasound conditions on the seed oil antioxidant activityBoth ABTS and DPPH values were significantly affected byamplitude level in linear term (120573119894) at 119901 lt 00001 DPPH and119901 lt 0001 ABTS respectively as well as in its quadratic term

(120573119894119894) at 119901 lt 0001 DPPH and ABTS The three-dimensionalsurface plots constructed to observe the effect of ultrasoundprocessing (Figure 1) demonstrated that antioxidant activitywas higher when the applied amplitude decreased

34 Optimization of the Ultrasound Extraction Conditions ofCactus Pear Seed Oil Optimal extraction conditions wereselected from the overlapped contour plots inwhich the effectof amplitude level and time on the antioxidant activity ofgreen cactus pear seed oil was considered

Figure 2 shows the optimal zone where the highestantioxidant activity by ABTS and DPPH was achieved Theconditions corresponded to amplitude of 78 applied for10min In this zone the values for antioxidant activity wereof 6625mg AAE100 g and 289 120583mol TE100 g for ABTS andDPPH respectively

35 Comparison between Methods

Extraction Yield and Antioxidant Activity Figure 3 comparesthe oil yields obtained by the three extraction methodsThe results revealed that the yield obtained using the opti-mized ultrasound extraction was significantly lower than theobtained with the Soxhlet and maceration procedures Thehigher oil yield obtained by Soxhlet could be attributed to theconstant and extended contact (4 to 6 hrs) of the sample withthe solvent at high temperatures in addition to the repeatedwashing cycles [37] The ultrasound yield was closer to thatof maceration method but this last one required longer time(24 hrs) as compared to 10min ultrasound treatment

The results of antioxidant activity by ABTS andDPPH areshown in Figure 4 Both parameters were significantly higherin the oil extracted by Soxhlet (5433 plusmn 084mg AAE100 gand 26660 plusmn 197 120583mol TE100 g resp) compared to theother extraction methods The ultrasound and macerationextractions exhibited similar antioxidant activity by ABTSwhile DPPH was significantly higher for the ultrasound seed

Journal of Food Quality 5

45

50

55

60

65

70

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(mg

AA

E100

g)A

ntio

xida

nt ac

tivity

(a)

50

100

150

200

250

300

350

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(120583m

ol T

E100

g)A

ntio

xida

nt ac

tivity

(b)

Figure 1 Effect of the ultrasound extraction on the antioxidant activity of green cactus pear seed oil (a) ABTS (b) DPPH

121

109

133145

157

169181

157

169

193

169

181

205

193

205

217

217

205

229

217

229

241

229

241

253

241

253

253

265

265

265

265

277

277

277

265

289

DPPH

5650

5650

557555005425

572558005875

5950

6025

6100

6175

6250

5950

6025

63256400

6175

6250

6250

6325

6475

6325

64006475

6400

6550

6475

6550

6550

6625

6625

6625

6700

6700

6700

6775

6775

6775

6700

6700

6625

6550

6475

6625

ABTS

Optimun condition

4

6

8

10

12

14

16

Tim

e (m

in)

80 82 84 86 88 90 9278Amplitude level ()

Figure 2 Optimal ultrasound extraction conditions of green cactuspear seed oil based on the highest antioxidant activity

oil Albeit the oil extracted by the Soxhlet method presentedhigher yield and antioxidant activity the ultrasound-assistedextraction may be enhanced if multiple extractions arecarried out in a time comparable to the required by theSoxhlet procedure (4ndash6 hrs)

36 Antimicrobial Activity Escherichia coli and Staphylo-coccus aureus are distributed in nature (water soil andvegetation) and are also part of the human intestinal

c

a

b

Ultrasound Soxhlet Maceration0

1

2

3

4

5

6

7

8Yi

eld

()

Figure 3 Cactus pear seed oil yield achieved by different extractionmethods abcDifferent letters mean significant differences betweenmethods (p lt 005)

b a b

b

a

c

Ultrasound Soxhlet Maceration0

255075

100125150175200225250275300

DPPH (120583mol TE100 g)ABTS (mg AAE100 g)

Figure 4 Antioxidant activity by ABTS and DPPH of cactus pearseed oil extracted by different methods abcDifferent letters meansignificant differences between methods (p lt 005)

6 Journal of Food Quality

Table 4 Antimicrobial activity of cactus pear seed oil extracted by different methods

Diameter of inhibition zone (mm)Oillowast (+) control (minus) control

Staphylococcus aureus (Gram-positive)Ultrasound 917 plusmn 029a 1889 plusmn 154 NDSoxhlet 950 plusmn 087a 1878 plusmn 164 NDMaceration 978 plusmn 069a 1811 plusmn 117 NDEscherichia coli (Gram-negative)Ultrasound 778 plusmn 019a 1556 plusmn 212 NDSoxhlet 756 plusmn 019a 1533 plusmn 265 NDMaceration 756 plusmn 038a 1400 plusmn 233 NDPseudomonas aeruginosa (Gram-negative)Ultrasound ND 1256 plusmn 038 NDSoxhlet ND 1222 plusmn 038 NDMaceration ND 1278 plusmn 038 NDlowastSeed oil 6667120583L (+) control ampicillin (disc 10 120583g Staphylococcus aureus and Escherichia coli) and streptomycin (disc 10 120583g Pseudomonas aeruginosa) (minus)control hexane ND not detected plusmn standard deviation a Same superscripts indicates that there is no significant difference (p gt 005)

microbiota [38] Pseudomonas aeruginosa besides beingpresent in the intestinalmicrobiota [39] is a bacteria found inthe soil fertilizers and water used for food production [40]and thus it can contaminate fresh or processed food whichis an indicator of inadequate sanitation or improper han-dling during food production [41] Table 4 summarizes theantimicrobial activity of green cactus pear seed oil Extractionmethod did not have a significant effect on the antimicrobialactivity against Staphylococcus aureus and Escherichia colibut the effect was lower than the positive controls Theseresults may be explained by the similar seed oil concentrationand combined action of compounds on the structure ofmicrobial cells [42 43] despite the extraction method Seedoil did not exhibit antimicrobial activity against Pseudomonasaeruginosa probably due to the oil chemical composition thetype of microorganism and the own characteristics of thebacteria [42ndash44]The antimicrobial activity of oils is generallymore effective against Gram-positive bacteria in comparisonto Gram-negative bacteria which are more resistant mainlybecause their outer membrane is less permeable [42 4345 46] The results suggest that Pseudomonas aeruginosawas more resistant than Escherichia coli probably due tothe lipopolysaccharides present in the outer membrane thatrestrict the diffusion of compounds making it less permeable[45]The resistance can also be caused by systems of exclusionpumps that eject antimicrobial compounds from the inside ofthe bacteria before they can cause damage [39 44]

37 Effect of Ultrasound on the Physical Structure Scanningelectron micrographs of the green cactus pear seeds powderbefore and after the ultrasound treatment at magnificationsfactors of 1000x and 500x are shown in Figure 5 Beforethe ultrasound treatment and despite the previous millingprocess in the control sample it was possible to identify intactstructures of the seeds cell as well as some starch granules

(Figure 5(a)) After the ultrasound treatment the cell struc-tural damage and the variations in the shape and size of theparticles were observed (Figure 5(b)) For instance starchgranules were not observed because sonication fragmentedthese particles while cavitation phenomenon disrupted thecell structures of the seeds [47 48]

4 Conclusions

This study demonstrated that response surface methodologyand a second-order polynomial model were effective tools todetermine the optimumprocessing conditions of ultrasound-assisted extraction based on the maximum values of antiox-idant activity The results demonstrated that cactus pearseed oil has good antioxidant and antimicrobial propertiesUltrasound-assisted extraction was comparable to macera-tion but a single ultrasound process yielded less oil andlower antioxidant activity than solvent extraction (Soxhlet)Ultrasound can be considered an alternative technology forthe extraction of seed oil but further research is required todetermine the uses of the seed oil and the technology withinthe food industry and the potential of several ultrasoundcycles at the optimized conditions

Conflicts of Interest

The authors declare that there are no conflicts of interest

Acknowledgments

This work was financially supported by Programa Integral deFortalecimiento Institucional (PIFI 2014-2015) The authorsacknowledge Mexican Association CoMeNTuna (HidalgoMexico) for providing the plant materials Marıa de losAngeles Ortega-Ortega participated in this research and she

Journal of Food Quality 7

(i) (ii)

A A

(a)

(i) (ii)

(b)

Figure 5 Scanning electron micrographs of green cactus pear seed powder before (a) and after (b) ultrasound treatment (i) 1000x (ii) 500xA The black circle shows a starch granule

received her Bachelorrsquos degree in nutrition in the Universi-dad Autonoma del Estado de Hidalgo Mexico (Act no 12872016)

References

[1] L Lozano ldquoEcofisiologıa de la tuna (Opuntia ficusmdashindica (L)Mill)rdquo Horticultura Argentina vol 30 no 72 pp 37ndash52 2011

[2] LMedina-Torres J A Gallegos-Infante R F Gonzalez-Laredoand N E Rocha-Guzman ldquoDrying kinetics of nopal (Opuntiaficusmdashindica) using three different methods and their effect ontheir mechanical propertiesrdquo LWTmdashFood Science and Technol-ogy vol 41 no 7 pp 1183ndash1188 2008

[3] J A Reyes-Aguero J R Aguirre-Rivera and H M HernandezldquoSystematic notes and a detailed description of Opuntia ficusindica (L)Mill (Cactaceae)rdquoAgrociencia vol 39 no 4 pp 395ndash408 2005

[4] H I Jun M N Cha E I Yang D G Choi and Y S KimldquoPhysicochemical properties and antioxidant activity of Koreancactus (Opuntia humifusa) cladodesrdquoHorticulture Environmentand Biotechnology vol 54 no 3 pp 288ndash295 2013

[5] A Rabhi H Falleh F Limam R Ksouri C Abdelly and ARaies ldquoUpshot of the ripening time on biological activitiesphenol content and fatty acid composition of Tunisian Opuntiaficus-indica fruitrdquo African Journal of Biotechnology vol 12 no40 pp 5875ndash5885 2013

[6] M Kaur A Kaur and R Sharma ldquoPharmacological actions ofOpuntia ficus indica a reviewrdquo Journal of Applied Pharmaceuti-cal Science vol 2 no 7 pp 15ndash18 2012

[7] M R Bhatt and P S Nagar ldquoEvaluation of physicochemicalproperty and fatty acid composition ofOpuntia elatior seed oilrdquoJournal of the Professional Association for Cactus Developmentvol 15 pp 13ndash19 2013

[8] M Ennouri H Fetoui E Bourret N Zeghal F Guermazi andH Attia ldquoEvaluation of some biological parameters of Opuntiaficus indica 2 Influence of seed supplemented diet on ratsrdquo Bio-resource Technology vol 97 no 16 pp 2136ndash2140 2006

[9] SAGARPA Secretarıa de Agricultura Ganaderıa DesarrolloRural Pesca y Alimentacion Pliegos de condiciones para eluso de la marca oficial Mexico calidad suprema en tuna 2005httpwwwmexicocalidadsupremaorgassetsgaleriaPC 0462005 Tunapdf

[10] M F Ramadan and J-TMorsel ldquoOil cactus pear (Opuntia ficus-indica L)rdquo Food Chemistry vol 82 no 3 pp 339ndash345 2003

[11] K El-Mostafa Y Kharrassi A Badreddine et al ldquoNopal Cactus(Opuntia ficus-indica) as a source of bioactive compounds fornutrition health and diseaserdquo Molecules vol 19 no 9 pp14879ndash14901 2014

[12] Z Ghazi M Ramdai M L Fauconnier B El Mahi and RCheikh ldquoFatty acids sterols and Vitamin E composition of seedoil of Opuntia ficus indica and Opuntia dilenii from MoroccordquoJournal of Materials and Environmental Science vol 4 no 6 pp967ndash972 2013

[13] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extrac of Laururs nobillis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

8 Journal of Food Quality

[14] A Nawirska-Olszanska A Kita A Biesiada A Sokol-Łętowska and A Z Kucharska ldquoCharacteristics of antioxidantactivity and composition of pumpkin seed oils in 12 cultivarsrdquoFood Chemistry vol 139 no 1ndash4 pp 155ndash161 2013

[15] V Cervantes-Cardoza N E Rocha-Guzman J A Gallego-Infante M Rosales-Castro L Medina-Torres and R FGonzalez-Laredo ldquoActividad antioxidante de extractos desemilla de tres variedades de manzana (Malus domestica Borkh-Rosaceae-)rdquo Boletın Latinoamericano y del Caribe de PlantasMedicinales y Aromaticas vol 9 no 6 pp 446ndash456 2010

[16] M K M Nair P Vasudevan and K Venkitanarayanan ldquoAnti-bacterial effect of black seed oil onListeriamonocytogenesrdquoFoodControl vol 16 no 5 pp 395ndash398 2005

[17] A I Hussain F Anwar S T H Sherazi and R PrzybylskildquoChemical composition antioxidant and antimicrobial activi-ties of basil (Ocimum basilicum) essential oils depends on sea-sonal variationsrdquo Food Chemistry vol 108 no 3 pp 986ndash9952008

[18] W Liu Y J Fu Y G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[19] M T Labuschagne and A Hugo ldquoOil content and fatty acidcomposition of cactus pear seed compared with cotton andgrape seedrdquo Journal of Food Biochemistry vol 34 no 1 pp 93ndash100 2010

[20] S Zine S Gharby and M El Hadek ldquoPhysicochemical char-acterization of Opuntia ficus-indica seed oil from MoroccordquoBiosciences Biotechnology Research Asia vol 10 no 1 pp 99ndash105 2013

[21] R Azuola and P Vargas ldquoExtraccion de sustancias asistida porultrasonido (EUA)rdquoTecnologıa enMarcha vol 20 no 4 pp 30ndash40 2007

[22] M Gao and C Z Liu ldquoComparison of techniques for theextraction of flavonoids fromcultured cells of SaussureamedusaMaximrdquo World Journal of Microbiology and Biotechnology vol21 no 8-9 pp 1461ndash1463 2005

[23] B Karki B P Lamsal S Jung et al ldquoEnhancing protein andsugar release from defatted soy flakes using ultrasound tech-nologyrdquo Journal of Food Engineering vol 96 no 2 pp 270ndash2782010

[24] F Adam M Abert-Vian G Peltier and F Chemat ldquolsquoSolvent-freersquo ultrasound-assisted extraction of lipids from freshmicroal-gae cells a green clean and scalable processrdquo BioresourceTechnology vol 114 pp 457ndash465 2012

[25] T Allaf V Tomao K Ruiz and F Chemat ldquoInstant controlledpressure drop technology and ultrasound assisted extraction forsequential extraction of essential oil and antioxidantsrdquo Ultra-sonics Sonochemistry vol 20 no 1 pp 239ndash246 2013

[26] Z S Zhang L J Wang D Li S S Jiao X D Chen and ZH Mao ldquoUltrasound-assisted extraction of oil from flaxseedrdquoSeparation and Purification Technology vol 62 no 1 pp 192ndash198 2008

[27] T Zhang Z Wang and X Chen ldquoUltrasound-associatedextraction of seed oil of Korean pinerdquo Journal of Forest Researchvol 16 no 2 pp 140ndash142 2005

[28] A M Goula ldquoUltrasound-assisted extraction of pomegranateseed oilmdashkinetic modelingrdquo Journal of Food Engineering vol117 no 4 pp 492ndash498 2013

[29] Q Y Zafra-Rojas N S Cruz-Cansino A Quintero-Lira etal ldquoApplication of ultrasound in a closed system optimum

condition for antioxidants extraction of blackberry (Rubusfructicosus) residuesrdquoMolecules vol 21 no 7 p 950 2016

[30] AOAC Official Methods of Analysis AOAC InternationalGaithersburg Md USA 18th edition 2005

[31] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[32] EM Kuskoski A G Asuero AM Troncoso J Mancini-Filhoand R Fett ldquoAplicacion de diversos metodos quımicos paradeterminar actividad antioxidante en pulpa de frutosrdquo Cienciae Tecnologia de Alimentos vol 25 no 4 pp 726ndash732 2005

[33] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[34] Y Tian Z Xu B Zheng and Y Martin Lo ldquoOptimization ofultrasonic-assisted extraction of pomegranate (Punica grana-tum L) seed oilrdquo Ultrasonics Sonochemistry vol 20 no 1 pp202ndash208 2013

[35] M L Agudo ldquoTecnicas para la determinacion de compuestosantioxidantes en alimentosrdquo 2010 httpwwwanpebadajozesautodidactaautodidacta archivosnumero 9 archivosl amedinapdf

[36] S K Ho C P Tan Y Y Thoo F Abas and C W HoldquoUltrasound-assisted extraction of antioxidants inMisai Kucing(Orthosiphon stamineus)rdquo Molecules vol 19 no 8 pp 12640ndash12659 2014

[37] S R Kirk R Sawyer and H Egan ldquoMetodos quımicos gen-eralesrdquo inComposicion y Analisis de Alimentos pp 25ndash29 Com-panıa editorial continental Ciudad de Mexico Mexico 2002

[38] S Vazquez S OrsquoNeill and M Legnani ldquoImportancia de loscoliformes en los alimentosrdquo 2013 httpwwwmontevideogubuysitesdefaultfilesimportancia de los coliformes en losalimentospdf

[39] C A Gomez-Alvarez A L Leal-Castro M J Perez de Gonza-lez and M L Navarrete-Jimenez ldquoMecanismos de resistenciaen Pseudomonas aeruginosa entendiendo a un peligroso ene-migordquo Revista de la Facultad de Medicina de la UniversidadNacional de Colombia vol 53 no 1 pp 27ndash34 2005

[40] S D Kominos C E Copeland B Grosiak and B Postic ldquoIntro-duction of Pseudomonas aeruginosa in to a hospital via vegeta-blesrdquo Applied Microbiology vol 24 no 4 pp 567ndash570 1972

[41] NOM Norma Oficial Mexicana NOM-210-SSA1-2014 Pro-ductos y servicios Metodos de prueba microbiologicosDeterminacion de microorganismos indicadores Determina-cion de microorganismos patogenos 2014 httpdofgobmxnota detallephpcodigo=539868ampfecha=26062015

[42] F Reyes-Jurado E Palou and A Lopez-Malo ldquoMetodos deevaluacion de la actividad antimicrobiana y de determinacionde los componentes quımicas de los aceites esencialesrdquo TemasSelectos de Ingenierıa de Alimentos vol 8 pp 68ndash78 2014

[43] D Zekaria ldquoLos aceites esenciales una alternativa a los antimi-crobianosrdquo 2015 httpwwwwpsa-aecaesaeca imgs docswpsa1182855355apdf

[44] DM Livermore ldquoMultiplemechanisms of antimicrobial resist-ance in Pseudomonas aeruginosa our worst nightmarerdquo Clini-cal Infectious Diseases vol 34 no 5 pp 634ndash640 2002

[45] M Viuda-Martos M A Mohamady J Fernandez-Lopez et alldquoIn vitro antioxidant and antibacterial activities of essentials oilsobtained from Egyptian aromatic plantsrdquo Food Control vol 22no 11 pp 1715ndash1722 2011

Journal of Food Quality 9

[46] X Feas L M Estevinho C Salinero et al ldquoTriacylglyc-eride antioxidant and antimicrobial features of virgin camelliaoleiferaC reticulata andC sasanqua oilsrdquoMolecules vol 18 no4 pp 4573ndash4587 2013

[47] R G Earnshaw ldquoUltrasound a new opportunity for foodpreservationrdquo in Ultrasound in Food Processing M J W PoveyandT JMason Eds pp 183ndash192 Editorial BlackAcademic andProfessional New York NY USA 1998

[48] M Vinatoru ldquoAn overview of the ultrasonically assisted extrac-tion of bioactive principles from herbsrdquo Ultrasonics Sonochem-istry vol 8 no 3 pp 303ndash313 2001

Research ArticleAntioxidant and Antimicrobial Properties of CactusPear (Opuntia) Seed Oils

Esther Ramiacuterez-Moreno1 Raquel Carintildeo-Corteacutes2 Nelly del Socorro Cruz-Cansino1

Luis Delgado-Olivares1 Joseacute Alberto Ariza-Ortega1 Vanessa Yelina Montantildeez-Izquierdo3

Mariacutea Manuela Hernaacutendez-Herrero3 and Tomaacutes Filardo-Kerstupp4

1Academic Area of Nutrition Health Sciences Institute Autonomous University of Hidalgo State 42160 Pachuca HGO Mexico2Academic Area of Medicine Autonomous University of Hidalgo State Eliseo Ramırez Ulloa 400 42090 Pachuca HGO Mexico3Department of Food Hygiene Faculty of Veterinary Autonomous University of Barcelona 08193 Bellaterra Spain4Academic Area of Chemistry Basic Science and Engineering Institute Autonomous University of Hidalgo StateCarretera Pachuca-Tulancingo Km 45 Mineral de la Reforma 42183 Pachuca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 23 January 2017 Accepted 5 April 2017 Published 26 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Esther Ramırez-Moreno et alThis is an open access article distributed under the Creative CommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Seed oils from two Mexican varieties of cactus pear (green Opuntia albicarpa and red Opuntia ficus indica) were extracted withdifferent solvents (hexane ethanol and ethyl acetate) to evaluate their antioxidant activity The seed oil with higher antioxidantactivitywas selected to evaluate antimicrobial activityThe fatty acid profilewas analyzed by gas chromatography-mass spectrometry(GC-MS) Oil from green cactus pear seeds obtained with ethanol and ethyl acetate exhibited higher antioxidant activity (119901 lt 005)of 323 and 316 120583mol TE20mg (p lt 005) respectively compared to red cactus pear seed oil (asymp274 and 247 120583mol TE20mgwith ethyl acetate and ethanol resp) The oil obtained with ethanol and higher antioxidant activity was used to determine theantimicrobial activity Both cactus pear oils produced a microbial inhibition zone in most of the microorganisms evaluatedparticularly Saccharomyces cerevisiae which had similar diameter (38ndash40mm) The oil fatty acids profiles of both varieties weresimilar and exhibited a high content of linoleic acid while two fatty acids (linolenic and behenic) found in red cactus pear were notobserved in the green variety

1 Introduction

A relatively untapped source of lipid and protein rawmaterialis the by-product of fruit-processing plants Millions ofpounds of fruit seeds are discarded yearly causing disposalproblems while proper utilization of these waste productscould lead to an important new source of oil and meal [1]Seeds of fruits collect at least some cytoplasmic lipid bodies asmajor storage reserve for lipid accumulation [2] Fruit seedsoils are of great interest because they are edible oils with highdegree of unsaturation antioxidant radical scavenging prop-erties [3ndash8] and a broad spectrum of antimicrobial activity[9ndash15] Therefore the oil from plants can be potentially usedby the food industry for the manufacturing of ldquonaturalrdquo orldquogreenrdquo safe foods [16] and extend shelf-life [17 18]

The oil from cactus pear seed has been found to havean appreciable amount of oil with high levels of unsaturatedfatty acids [19] with antioxidant [20 21] and antimicrobialactivity [22] as well as cardioprotective antithrombotic anti-inflammatory antiarrhythmic hypolipidemic and antihy-perglycemic effect [23 24] These properties are of interestfor the pharmaceutical and food industry However theconcentration and effectiveness of these oils may vary amongcultivars or varieties crop environmental factors (eg lighttemperature and type of soil nutrients) or methods andsolvents used for their extraction Therefore the purpose ofthis research was to determine the antioxidant and antimi-crobial activity and fatty acid profile of the oil obtained fromtwo Mexican varieties of cactus pear (Opuntia albicarpa andOpuntia ficus indica) seeds extracted with different solvents

HindawiJournal of Food QualityVolume 2017 Article ID 3075907 8 pageshttpsdoiorg10115520173075907

2 Journal of Food Quality

2 Materials and Methods

21 Plant Material Two Mexican varieties of cactus pear(Opuntia albicarpa and Opuntia ficus indica) fruit green (cvReyna) and red (cv Rojo Pelon) respectively were providedby theMexican association CoMeNTuna (ConsejoMexicanodel Nopal y la Tuna AC Actopan Hidalgo Mexico) Fruitsfree of external injuries were selected washed and manuallypeeled Cactus pear seeds were obtained after juice wasextracted stirring the pulpwith an industrial blender (38BL52LBC10 Waring Comercial USA) and passing it through aconventional strainer The seeds retained were washed in thestrainer with water until pulp residues were removed

22 Powder Seed and Oil Extraction Green cactus pear seeds(GCPS) and red cactus pear seeds (RCPS)were sun-dried andthen grounded (Cyclotec 1093 Tecator Sweden) to a 1mmdiameter mesh and stored at minus32∘C until further analysisTheseed oil was extracted as follows 25 g of powdered seeds wasmixed with 500mL of solvents with varying polarities (hex-ane ethanol and ethyl acetate) and the obtained residue wasreextracted until extraction solvents become colourless Allthe extracts were filtered through filtration paper Whatmannumber 1 and the filtered extracts were collected for furtherdrying and removal of the remaining solvent at 50∘C using arotary evaporator (BUCHI R-200 Switzerland) All extractswere placed in plastic bottles and then stored at minus20∘C untilused The oils obtained were used to further analysis

23 Free Radical Scavenging Assay The free radical scaven-ging activity was measured using 11-diphenyl-2-picrylhy-drazyl (DPPH∙) radical as described byMorales and Jimenez-Perez [25] A volume of 500 120583L of ethanolic DPPH∙ solution(74mg100mL) was added to a sample aliquot of 100 120583Lplaced in vialsThemixturewas left to sit at room temperaturefor 1 h and then was vortexed and centrifuged at 3000 rpm for10 minutesThe absorbance of the supernatant was measuredat 520 nm in amicroplate reader (PowerWave XSUV-Bioteksoftware KC Junior USA) and 120583mol of Trolox equivalentsper 20 milligram (120583mol TE20mg) of sample was obtainedOil samples with best antioxidant capacity obtained from thedifferent solvents were used for the antimicrobial analysis

24 Antimicrobial Activity Eight standard freeze-dried cul-tures of bacteria Candida albicans (ATCC 10231) Escherichiacoli O58H21 (ATCC 10536) Escherichia coli O157H7(CCUG 44857) Staphylococcus aureus (ATCC 13565) Liste-ria monocytogenes (CCUG 15526) Pseudomonas aeruginosa(ATCC 15442) Saccharomyces cerevisiae (CECT 1942) andSalmonella Typhi (CCUG 29478) were obtained in ther-mosealed vials from the Spanish Type Culture Collection(Autonomous University of Barcelona Barcelona Spain)Freeze-dried cultures were rehydrated in tryptone soy brothat 37∘C for 18 h and then were used to inoculate tryptone soyagar and malt extract agar plates all microorganisms wereincubated at 37∘CexceptCandida albicans and Saccharomycescerevisiae which were incubated at 25∘C Individual colonies

were maintained on specific agar slants stored at 4∘C andsubcultured every 15 days

Disc Diffusion Assay Antimicrobial activity of oil extractedfromGCPS andRCPSwas carried out using the disc diffusionmethod [26] Petri plates were filled with sim20mL of steriletryptone soy agar for bacteria and malt extract agar for fungiThe test cultures were swabbed on the top of the solidifiedmedia and allowed to dry for 10 minutes Serial dilutions(10ndash50 120583gmL) of the seed oil from a stock solution (1mgmL)were prepared in 20 DMSO and 10 120583L loaded onto thesterile blank discs (BBL Sensi-Disc) of 6 millimetersof diameter On the media surface the loaded disks wereplaced and left for 30 minutes at room temperature toallow compound diffusion The seed oil was serially dilutedin MuellerndashHinton broth medium and duplicate tubes ofeach dilution (10ndash100 120583gmL) were inoculated with 5 times106 cells of the test bacteria strain and culturesThe antibioticagents Sensi-Disc streptomycin ampicillin and sulfamethox-azoletrimethoprim (BBL Sensi-Disc) were used as positivecontrols at the same concentration level After plates wereincubated at 37∘C for 24 h the diameters of the inhibitionzones were recorded in millimeters Three independentrepetitions were performed and tests were made in triplicate

25 GC-MS Analysis The GC-MS analysis was performedwith a GC-MS HP-5890 (Hewlett-Packard Company PaloAlto California USA) equipped with a Flame IonizationDetector (FID) and a ZB-WAX fused silica capillary column(60m times 025mm id times 025mm film thickness) packedwith 5 phenylmethylpolysiloxane (Phenomenex TorranceCA) To obtain the methyl esters the cactus pear seed oilswere saponified and derivatized using KOH 1N (IUPAC1969) Changes in the fatty acids of the oils samples werecompared against a standard mixture of 37 components offatty acids methyl esters (FAMEs) (Food Industry FAMEsMix Restek) comprised by methyl esters with chains C40C60 C80 C100 C110 C120 C130 C140 C141 C150C151 C160 C161 C170 C171 C180 C181n9c C181n9tC182n6c C182n6t C183n6 C183n3 C200 C201n9 C202C203n6 C203n3 C204n6 C205n3 C210 C220 C221n9C222 C226n3 C230 C240 and C241n9 The samplevolume injected was of 2 120583L (split ratio 20 2) at an injectorand detector temperatures of 225 and 225∘C respectively N2was used as carrier gas at a flow rate of 12mLsdotminminus1 Fattyacids were calculated as percentage of total FAMEs

26 Statistical Analysis All values were obtained by triplicateand expressed as means plusmn standard deviations (SD) Datawere analyzed using the SPSS V15 software (SPSS InstituteInc Cary NC) An ANOVA was carried out to determinedifferences between oils extracted as well as its antimicrobialactivity that were significant at the 5 level of probability anda Tukey test was used for comparison of data

3 Results and Discussion

31 Yield Comparison between Extraction Solvents Hexaneethanol and ethyl acetate were used to extract the oil from

Journal of Food Quality 3

1183

669

1013

511

106

381

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

2

4

6

8

10

12

14

Oil

yiel

d (

)

Figure 1 Oil yields () extracted from GCPS and RCPS withhexane ethanol and ethyl acetate

cactus pear seeds The extraction yields are compared inFigure 1 which shows that the higher amount of oil () wasobtained from the green cultivar and that yield depended onthe solvent used Oil extraction with hexane was higher forboth fruit varieties (1183 for GCPS and 689 for RCPS)followed by ethanol which reached the same yield as ethylacetate for GCPS (asymp10) Ethyl acetate was the least effectivesolvent for RCPS The extraction yields were similar to thosereported (asymp7 to 11) for several varieties of Opuntia ficusindica [27ndash29] This extraction yields will vary depending onseveral factors as fruit variety harvest period maturationgeographic region percentage of oil in the seed and chemicalcompounds found in the source and by the extractionmethod[30] Researchers have determined that solvent extractioncombinedwith othermethods could increase oil yield as highpressure or supercritical fluid combined with solvent reacheda yield of 933 from tobacco seeds (Nicotiana tabacum L)while sonication and Soxhlet reached a 775 and 1372respectively [31]

32 Free Radical Scavenging Activity Solvent extraction isusually used for isolation of antioxidants the extractiondepends on the solvent selected based on the different antiox-idant compounds with varying polarity [32 33] DPPH is astable free radical that accepts an electron or hydrogen radicalto become a stable diamagnetic molecule [34 35]The DPPHassay has also been used to predict the oxidative stability ofedible oils [36 37] The antioxidant activity determined byDPPH of the oil extracted from RCPS and GCPS is shownin Figure 2 Oil from the GCPS extracted with ethanol andethyl acetate exhibited the higher antioxidant activity (119901 lt005) of 323 and 316 120583mol TE20mg extract respectivelyfollowed by RCPS oil extracted with ethyl acetate (274120583molTE20mg extract) and ethanol (247 120583mol TE20mg extract)These results demonstrate that the extraction solvent hada significant effect on the free radical scavenging capacityof the oil where the hexane had the lower values In ourstudy the green variety exhibited a higher antioxidant activityregardless of solvent Different results may depend mainly

e

d

a

c

ab

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

50

100

150

200

250

300

350

휇m

ol T

E20

mg

extr

act

Figure 2 Antioxidant activity of GCPS and RCPS oils extractedwith different solvents andashdDifferent letters above bars indicate thatsamples are significantly different (119901 lt 005)

on the content and concentration of bioactive compounds inthe oil but other factors such as solvent polarity solubilityof the extracts in different testing systems stereoselectivityof the radicals [38] and strong synergism between fattyacids [6] may affect antioxidant activities Other studies havealso reported diverse antioxidant activity among oils fromdifferent Opuntia varieties [20 39 40]

33 Antibacterial and Antifungal Activity The most recom-mended way to prevent or inhibit microbial growth in foodsis the use of food preservatives Essential oils are secondarymetabolites of plants that have wide applications in thefood flavoring and preservative industry [41] Six differentbacterium and two fungi species were used to screen theantimicrobial potential of the oils extracted from the twovarieties of cactus pear seeds Oil extracted with ethanolexhibited the highest antioxidant activity and therefore itwas used to evaluate the antibacterial and antifungal activityFigure 3 shows the results from the microbial assay wheremost microorganisms showed an inhibition zone whenexposed to GCPS and RCPS oils except Salmonella Typhiand Escherichia coli O157H7 (image not shown) From thesetwo microorganisms the first showed an inhibition zonein the presence of antibiotic agents streptomycin (S) ampi-cillin (AMP) and sulfamethoxazoletrimethoprim (STX) indiameters of 146 113 and 273mm respectively (Table 1)while Escherichia coli O157H7 was only inhibited by SXT(253mm) which agrees with other reports of multiantibi-otic resistance of E coli O157H7 due to the presence ofthe gene cluster AMR-SSuT [42] and production of beta-lactamase [43] On the other hand Saccharomyces cerevisiaewas highly inhibited (38ndash40mm) by the extracted oils butgrew in presence of the antimicrobial agents (Figure 3)Similar results were observed for Candida albicans althoughinhibition zones were smaller and similar for both oilsThese observations demonstrate that certain compounds inthe cactus pear seed oil have antimicrobial activity Otherresearchers also reported similar observations for cactus

4 Journal of Food Quality

Table 1 Diameters of growth inhibition zones (mm) in the presence of oil extracted from cactus pear seeds and conventional antimicrobialsA

Microbial cultures Extract Antimicrobial agentGCPS RCPS S AMP SXT

Saccharomyces cerevisiae (CECT1942) 383 plusmn 42a 403 plusmn 45a ND ND NDEscherichia coli O58H21 (ATCC 10536) 119 plusmn 07d 114 plusmn 09d 195 plusmn 14b 178 plusmn 15c 299 plusmn 09a

Escherichia coli O157H7 (CCUG 44857) NDB ND ND ND 253 plusmn 10Staphylococcus aureus (ATCC 13565) 121 plusmn 10c 111 plusmn 11c 183 plusmn 09b 281 plusmn 15a 333 plusmn 19a

Listeria monocytogenes (CCUG15526) 133 plusmn 15c 114 plusmn 09d 213 plusmn 12a 173 plusmn 08c 376 plusmn 18a

Pseudomonas aeruginosa (ATCC15442) 164 plusmn 21c 151 plusmn 20c 201 plusmn 15b 241 plusmn 25a 366 plusmn 29a

Salmonella typhi (CCUG29478) ND ND 146 plusmn 04b 113 plusmn 18c 273 plusmn 08a

Candida albicans (ATCC 10231) 111 plusmn 10a 110 plusmn 18a ND ND NDAInhibition zone diameters for oil and reference antibiotics are means plusmn SE of three replicas GCPS green cactus pear seed oil extract RCPS red cactus pearseed oil extract S streptomycin (10120583gdisc) AMP ampicillin (10 120583gdisc) and SXT sulfamethoxazoletrimethoprim (10120583gdisc) BND not detected activityandashdDifferent letters in the same row indicate significant differences

RG

SXT

S

AMP

(a)

RG

SXT

S

AMP

(b)

R G

SXTS

AMP

(c)

RG

SXTS

AMP

(d)

RG

SXT

S

AMP

(e)

R G

SXT

S

AMP

(f)

Figure 3 Antimicrobial activity of oil extracted from green cactus pear (G) oil extracted from red cactus pear seeds (R) streptomycin(S) ampicillin (AMP) and sulfamethoxazoletrimethoprim (SXT) Candida albicans (ATCC 10231) (a) Escherichia coli O58H21 (ATCC10536) (b) Staphylococcus aureus (ATCC 13565) (c) Listeria monocytogenes (CCUG15526) (d) Pseudomonas aeruginosa (ATCC15442) (e)Saccharomyces cerevisiae (CECT1942) (f)

pear fruit cv Opuntia stricta [44] and for other plants asfennel (Foeniculum vulgare L) and chamomile (Matricariachamomilla L) [5] Differences in the levels of antimicrobialactivity may be partially attributed to variable chemicalcomposition of the oils [45] Mnayer et al [46] suggestedthat oil compounds can act on different bacterial structureswhile Gill et al [47] mentioned that whole oils have a greater

antibacterial activity than the major component mixed sothat minor components are critical for the activity and exerta synergistic effect [16 48 49]

In the present study the antimicrobial activity of cactuspear seed oil was more effective against fungi comparedto bacteria cultures These interesting results suggest thatthere is a link between the oil chemical contents and the

Journal of Food Quality 5

Table 2 Percentages of FAMEs in crude cactus pear seed oil extracts

FAMEs Green cactus pear seed oil extract Red cactus pear seed oil extractC140 0078 plusmn 000 0066 plusmn 001C160 12327 plusmn 009 12887 plusmn 002C161 0429 plusmn 002 0570 plusmn 001C162 0073 plusmn 000 0540 plusmn 000C170 0060 plusmn 001 0075 plusmn 000C180 3436 plusmn 001 3389 plusmn 007C181 16215 plusmn 003 17061 plusmn 001C182 67448 plusmn 008 65407 plusmn 001C183 Ni 0372 plusmn 001C220 Ni 0160 plusmn 001Means of 3 replicates plusmn SE Ni not identified

140

160

181

182

18017

016

116

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(a)14

0 161

162

170

180

181

182

183

220

160

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(b)

Figure 4 Chromatograms of FAMEs of cactus pear seed oil extract (a) Green cactus pear seed oil extract (b) red cactus pear seed oil extractIn both oils extracts were identified myristic (C140) palmitic (C160) palmitoleic (C161 cis-9) hexadecadienoic (C162 cis-9 12) margaric(C170) stearic (C180) oleic (C181 cis-9) linoleic (C182 cis-9 12) except linolenic (C183 cis-6 9 12) and behenic (C220) fatty acids thatwere identified only in red cactus pear seed

antimicrobial activity The membrane disruption could beone mechanism of action by inactivating microbial adhesionenzymes and proteins transport [15 46] RCPS and GCPSextracts inhibited most of the evaluated bacterial and fungispecies (Table 1) however antimicrobial activity was notdetected for Salmonella Typhi which is a gram-negative bac-terium In general gram-negative bacteria have an effectiveoutermembrane that restricts the penetration of amphipathiccompounds and has a mechanism to extrude toxins across[50]Thismay explain the apparent antimicrobial ineffective-ness of the oils against the permeability barrier in addition tothe presence of multidrug resistance encoding plasmids [51]

34 Fatty Acid Profile FAMEs chromatograms and percent-ages are shown in Figure 4 and Table 2 Cactus pear seed oilscontained saturated and unsaturated fatty acids the linoleicfatty acid being the predominant (674 and 654 in GCPSand RCPS oils resp) Minimal amounts of myristic (C140)palmitoleic (C161) hexadecadienoic (C162) and margaric(C170) fatty acids in both oils were also identified The fattyacids profiles of the two cactus pear varieties were similarhowever theGCPS had a slightly higher content of the linoleicacid (C182)while the fatty acids linolenic (C183) and behenic(C220) were in minimal amounts only in the RCPS

Different studies have established that factors as cultivartype temperature and harvest time have a strong influence inparameter as pH Brix vitamin C sugars and fat content [5253] Oumato et al [52] found differences in linoleic fatty acid(C182) content among cactus pear cultivars In other studythe oleic acid (C181) content was significantly influenced bythe cultivar and location interaction [53] providing uniquecharacteristics to the oil

In comparison with other plants oils the linoleic acid(C182) content of the cactus pear fruit was similar to thelevels reported for sunflower oil (62) [54] and higher thanwheat germ oil (5505) [55] and soybean oil (5270)[56] The contents of other FAMEs in cactus pear varietiessuch as palmitic (C160) oleic (C181) and stearic (C180)were similar to those reported for Castilla blackberry (Rubusglaucus Benth) with 1124 passion fruit (Passiflora edulis)with 1547 [57] and grape (Vitis vinifera) with 35 [58]

Other researchers have reported similar fatty acidsprofile to our findings for different plant materials andhave analyzed the antimicrobial effectiveness against dif-ferent microorganisms For instance fatty acids found inAllium cepa were found to effectively inhibit Staphylococcusaureus Bacillus subtilis Enterococcus faecalis Escherichia coliand Klebsiella pneumoniae [59] Oil extracted from SwieteniaMacrophylla king seed oil inhibited growth of S aureus

6 Journal of Food Quality

S Typhimurium and P aeruginosa [60] These studies de-monstrate that seed oil can inhibit fungi and bacteria buttheir efficacy would depend on their concentration levels andspecific pathogen [15]

4 Conclusions

Oil yield from the green cactus pearwas higher in comparisonto the red cultivar andwas also influenced by the solvent usedHexane exhibited high extraction yield while oils extractedwith ethanol had the better antioxidant activity The resultsdemonstrated that oil extracts from both varieties have anoticeable antimicrobial activity against gram-positive andgram-negative bacteria comparable to antimicrobial com-pounds such as ampicillin streptomycin and sulfamethoxa-zoletrimethoprimThis research provides further incentivesto develop additives for the food cosmetic and pharmaceu-tical sectors seeking natural compounds with antimicrobialactivity Further studies are needed to determine the specificcomponent responsible for the antimicrobial activity in cac-tus pear seeds oil and determine the optimum levels of oilextract and the antimicrobial effectiveness in the foodmatrix

Additional Points

Practical Application Our results suggest that the oilsextracted from cactus pear seeds have the potential to be usedas a natural antioxidant and antimicrobial agents by the foodcosmetic and pharmaceutical sectors

Conflicts of Interest

The authors have declared that no conflicts of interest exist

Acknowledgments

This study was possible thanks to the financial supportfrom the Programa Integral de Fortalecimiento Institucional(PIFI 2013ndash2015) Mexico This research project was partiallysupported by the Food Hygiene Department Faculty ofVeterinary from the Autonomous University of BarcelonaSpain The authors acknowledge the Mexican associationCoMeNTuna (Consejo Mexicano del Nopal y la TunaHidalgo Mexico) for providing the plant materials

References

[1] B S Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Acids in Foods and Their Health Implications pp 263ndash301 CRC Press 3rd edition 2007

[2] D J Murphy I Hernandez-Pinzon and K Patel ldquoRole oflipid bodies and lipid-body proteins in seeds and other tissuesrdquoJournal of Plant Physiology vol 158 no 4 pp 471ndash478 2001

[3] A Kedia B Prakash P KMishra andN K Dubey ldquoAntifungaland antiaflatoxigenic properties of Cuminum cyminum (L)seed essential oil and its efficacy as a preservative in storedcommoditiesrdquo International Journal of Food Microbiology vol168-169 pp 1ndash7 2014

[4] S Singh S S Das G Singh C SchuffM P de Lampasona andC A Catalan ldquoComposition in vitro antioxidant and antimi-crobial activities of essential oil and oleoresins obtained fromblack cumin seeds (Nigella sativa L)rdquo BioMed Research Inter-national vol 2014 Article ID 918209 10 pages 2014

[5] M H H Roby M A Sarhan K A-H Selim and K I KhalelldquoAntioxidant and antimicrobial activities of essential oil andextracts of fennel (Foeniculum vulgare L) and chamomile(Matricaria chamomilla L)rdquo Industrial Crops and Products vol44 pp 437ndash445 2013

[6] G Kavoosi A Tafsiry A A Ebdam and V Rowshan ldquoEvalua-tion of antioxidant and antimicrobial activities of essential oilsfrom carum copticum seed and ferula assafoetida latexrdquo Journalof Food Science vol 78 no 2 pp T356ndashT361 2013

[7] S Lalas O Gortzi V Athanasiadis J Tsaknis and I ChinouldquoDetermination of antimicrobial activity and resistance tooxidation of Moringa peregrina seed oilrdquoMolecules vol 17 no3 pp 2330ndash2334 2012

[8] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extract of Laurus nobilis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

[9] R S Bhat and S Al-daihan ldquoAntimicrobial activity of Litchichinensis and Nephelium lappaceum aqueous seed extractsagainst some pathogenic bacterial strainsrdquo Journal of King SaudUniversitymdashScience vol 26 no 1 pp 79ndash82 2014

[10] J M Silvan E Mingo M Hidalgo S de Pascual-Teresa A VCarrascosa and A J Martinez-Rodriguez ldquoAntibacterial activ-ity of a grape seed extract and its fractions against Campylobac-ter spprdquo Food Control vol 29 no 1 pp 25ndash31 2013

[11] K Rakholiya M Kaneria D Desai and S Chanda ldquoAntimi-crobial activity of decoction extracts of residual parts (seedand peels) ofMangifera indica L var Kesar against pathogenicand food spoilage microorganismrdquo in Microbial pathogens andstrategies for combating them science technology and educationA Mendez-Vilas Ed vol 2 pp 850ndash856 2013

[12] N A Hasan M Z Nawahwi and H Ab Malek ldquoAntimicrobialactivity ofNigella sativa seed extractrdquo Sains Malaysiana vol 42no 2 pp 143ndash147 2013

[13] Z I Sajid F Anwar G Shabir G Rasul KM Alkharfy and A-H Gilani ldquoAntioxidant antimicrobial properties and phenolicsof different solvent extracts from bark leaves and seeds ofPongamia pinnata (L) pierrerdquoMolecules vol 17 no 4 pp 3917ndash3932 2012

[14] M Khoobchandani B K Ojeswi N Ganesh et al ldquoAntimicro-bial properties and analytical profile of traditional Eruca sativaseed oil comparisonwith various aerial and root plant extractsrdquoFood Chemistry vol 120 no 1 pp 217ndash224 2010

[15] V Kesari A Das and L Rangan ldquoPhysico-chemical charac-terization and antimicrobial activity from seed oil of Pongamiapinnata a potential biofuel croprdquo Biomass and Bioenergy vol34 no 1 pp 108ndash115 2010

[16] K Carovic-Stanko S Orlic O Politeo et al ldquoComposition andantibacterial activities of essential oils of seven Ocimum taxardquoFood Chemistry vol 119 no 1 pp 196ndash201 2010

[17] MM Tajkarimi S A Ibrahim andDO Cliver ldquoAntimicrobialherb and spice compounds in foodrdquo Food Control vol 21 no 9pp 1199ndash1218 2010

[18] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

Journal of Food Quality 7

[19] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[20] W Liu Y-J Fu Y-G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[21] B Matthaus and M M Ozcan ldquoHabitat effects on yield fattyacid composition and tocopherol contents of prickly pear(Opuntia ficus-indica L) seed oilsrdquo Scientia Horticulturae vol131 pp 95ndash98 2011

[22] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research vol 27 no 14 pp 1305ndash1314 2013

[23] KMobraten TMHaug C R Kleiveland and T Lea ldquoOmega-3 and omega-6 PUFAs induce the same GPR120-mediatedsignalling events but with different kinetics and intensity inCaco-2 cellsrdquo Lipids in Health and Disease vol 12 no 1 ArticleID 101 2013

[24] A BerraaouanA ZiyyatHMekhfi et al ldquoEvaluation of antidi-abetic properties of cactus pear seed oil in ratsrdquo PharmaceuticalBiology vol 52 no 10 pp 1286ndash1290 2014

[25] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[26] P R Murray E J Baron M A Pfaller F C Tenover and R HYolkeManual of Clinical Microbiology 1995 Washington DCUSA

[27] M Ennouri H Fetoui E Bourret N Zeghal and H AttialdquoEvaluation of some biological parameters of Opuntia ficusindica 1 Influence of a seed oil supplemented diet on ratsrdquoBioresource Technology vol 97 no 12 pp 1382ndash1386 2006

[28] Y Habibi L Heux M Mahrouz and M R Vignon ldquoMorpho-logical and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruitsrdquo Carbohydrate Polymers vol 72 no 1pp 102ndash112 2008

[29] MMoudenM Boujnah S Salmaoui S Zantar and A DouiraldquoEffect of two extraction methods and harvest period andperformance there statement of fatty oils of figs pear seedrdquoInternational Journal of Pure amp Applied Bioscience vol 4 no1 pp 1ndash8 2016

[30] A El Finti M Belayadi R El Boullani F Msanda and A ElMousadik ldquoAssessment of some agro-technological parametersof cactus pear fruit (Opuntia ficus-indica Mill) in Moroccocultivarsrdquo Journal of Medicinal Plants Research no 7 pp 2574ndash2583 2013

[31] S Majdi M Barzegar A Jabbari and M Agha AlikhanildquoSupercritical fluid extraction of tobacco seed oil and itscomparison with solvent extraction methodsrdquo Journal of Agri-cultural Science and Technology vol 14 no 5 pp 1043ndash10512012

[32] E M Marinova and N V Yanishlieva ldquoAntioxidative activity ofextracts from selected species of the family Lamiaceae insunflower oilrdquo Food Chemistry vol 58 no 3 pp 245ndash248 1997

[33] Y-Y Soong and P J Barlow ldquoAntioxidant activity and phenoliccontent of selected fruit seedsrdquo Food Chemistry vol 88 no 3pp 411ndash417 2004

[34] J R Soares T C P Dinis A P Cunha and L M AlmeidaldquoAntioxidant activities of some extracts of Thymus zygisrdquo FreeRadical Research vol 26 no 5 pp 469ndash478 1997

[35] I GulcinMOktay E Kirecci and O I Kufrevioglu ldquoScreeningof antioxidant and antimicrobial activities of anise (Pimpinellaanisum L) seed extractsrdquo Food Chemistry vol 83 pp 371ndash3822003

[36] J Lee H Chung P-S Chang and J Lee ldquoDevelopment of amethod predicting the oxidative stability of edible oils using 22-diphenyl-1-picrylhydrazyl (DPPH)rdquo Food Chemistry vol 103no 2 pp 662ndash669 2007

[37] A Fazio P Plastina J Meijerink R F Witkamp and BGabriele ldquoComparative analyses of seeds of wild fruits ofRubus and Sambucus species from Southern Italy fatty acidcomposition of the oil total phenolic content antioxidant andanti-inflammatory properties of the methanolic extractsrdquo FoodChemistry vol 140 no 4 pp 817ndash824 2013

[38] R L Prior X Wu and K Schaich ldquoStandardized methods forthe determination of antioxidant capacity and phenolics infoods and dietary supplementsrdquo Journal of Agricultural andFood Chemistry vol 53 no 10 pp 4290ndash4302 2005

[39] A Cardador-Martınez C Jimenez-Martınez and G SandovalldquoRevalorization of cactus pear (Opuntia spp) wastes as a sourceof antioxidantsrdquo Ciencia e Tecnologia de Alimentos vol 31 no3 pp 782ndash788 2011

[40] Z Ghazi M Ramdani M Tahri et al ldquoChemical compositionand antioxidant activity of seeds oils and fruit juicerdquo Journalof Materials and Environmental Science vol 6 no 8 pp 2338ndash2345 2015

[41] V K Bajpai K-H Baek and S C Kang ldquoControl of Salmonellain foods by using essential oils a reviewrdquo Food ResearchInternational vol 45 no 2 pp 722ndash734 2012

[42] K Ziebell R P Johnson A M Kropinski et al ldquoGenecluster conferring streptomycin sulfonamide and tetracyclineresistance in Escherichia coli O157H7 phage types 23 45 and67rdquo Applied and Environmental Microbiology vol 77 no 5 pp1900ndash1903 2011

[43] O Chandra K J Putra and I Wayan ldquoAntibiotic resistanceprofiles of Escherichia coli O157H7 in cattle at Suth-KutaBadung Regency Bali Indonesiardquo Global Veterinaria vol 15no 5 pp 480ndash484 2015

[44] E Moosazadeh M R Akhgar and A Kariminik ldquoChemicalcomposition and antimicrobial activity of Opuntia stricta Fessential oilrdquo Journal of Biodiversity and Environmental Sciencesvol 4 pp 94ndash101 2014

[45] S Burt ldquoEssential oils their antibacterial properties and poten-tial applications in foods - a reviewrdquo International Journal ofFood Microbiology vol 94 no 3 pp 223ndash253 2004

[46] D Mnayer A-S Fabiano-Tixier E Petitcolas et al ldquoChemicalcomposition antibacterial and antioxidant activities of sixessentials oils from the Alliaceae familyrdquo Molecules vol 19 no12 pp 20034ndash20053 2014

[47] A O Gill P Delaquis P Russo and R A Holley ldquoEvaluationof antilisterial action of cilantro oil on vacuum packed hamrdquoInternational Journal of FoodMicrobiology vol 73 no 1 pp 83ndash92 2002

[48] M Turgis K D Vu C Dupont and M Lacroix ldquoCombinedantimicrobial effect of essential oils and bacteriocins againstfoodborne pathogens and food spoilage bacteriardquoFoodResearchInternational vol 48 no 2 pp 696ndash702 2012

[49] H Zengin and A H Baysal ldquoAntibacterial and antioxi-dant activity of essential oil terpenes against pathogenic andspoilage-forming bacteria and cell structure-activity relation-ships evaluated by SEM microscopyrdquo Molecules vol 19 no 11pp 17773ndash17798 2014

8 Journal of Food Quality

[50] G Tegos F R Stermitz O Lomovskaya and K Lewis ldquoMul-tidrug pump inhibitors uncover remarkable activity of plantantimicrobialsrdquo Antimicrobial Agents and Chemotherapy vol46 no 10 pp 3133ndash3141 2002

[51] M Baltazar A Ngandjio K E Holt et al ldquoMultidrug-resistantSalmonella enterica serotype typhi Gulf of Guinea RegionAfricardquo Emerging Infectious Diseases vol 21 no 4 pp 655ndash6592015

[52] J Oumato S ZriraM Boujnah andB Saidi ldquoEffect ofmaturitystage onmorphological and chemical characteristics ofOpuntiaficus indica from Moroccordquo International Journal of Innovationand Applied Studies vol 20 no 1 pp 400ndash410 2017

[53] M deWit A Hugo N Shongwe and R van derMerwe ldquoEffectof cultivar season and locality on lipid content and fatty acidcomposition of cactus pear seed oilrdquo South African Journal ofPlant and Soil no 33 pp 279ndash288 2016

[54] Australian Oilseeds Federation Incorporated 2015 Section 1ldquoQuality standards technical information amp typical analysisrdquono 14 pp 31ndash40 2016 (Accessed 1 November 2015)

[55] A Awad A Adel A A M Nady and AAE ldquoWheat germ anoverview on nutritional value antioxidant potential andantibacterial characteristicsrdquo Food and Nutrition Sciences vol6 no 2 pp 265ndash277 2015

[56] P Pumrojana S Terapuntuwat and P Pakdee ldquoInfluence offatty acid composition of soybean oil vs beef tallow on egg yolkfatty acid profiles of laying hensrdquo Pakistan Journal of Nutritionvol 14 no 7 pp 383ndash387 2015

[57] A F Ceron M O Osorio and B A Hurtado ldquoIdentificacionde acidos grasos contenidos en los aceites extraıdos a partir desemillas de tres diferentes especies de frutasrdquo Acta Agronomicavol 61 no 2 pp 126ndash132 2012

[58] J Orsavova L Misurcova J Vavra Ambrozova R Vicha andJ Mlcek ldquoFatty acids composition of vegetable oils and itscontribution to dietary energy intake and dependence of car-diovascular mortality on dietary intake of fatty acidsrdquo Interna-tional Journal of Molecular Sciences vol 16 no 6 pp 12871ndash12890 2015

[59] M Derbali A Elaissi I Cheraief and M Aouni ldquoFatty acidcomposition and antimicrobial activity against sensitive andmulti-drug resistant bacteria of Tunisian Allium cepa seedextractrdquo Research amp Reviews Journal of Hospital and ClinicalPharmacy vol 2 no 2 pp 30ndash34 2016

[60] M B Suliman A H Nour M M Yusoff P Kuppusamy A RYuvaraj and S A Mazza ldquoFatty acid composition and antibac-terial activity of Swietenia macrophylla king seed oilrdquo AfricanJournal of Plant Science vol 7 no 7 pp 300ndash303 2013

Page 2: Natural Preservatives to Improve Food Quality and Safety

Natural Preservatives to ImproveFood Quality and Safety

Journal of Food Quality

Natural Preservatives to ImproveFood Quality and Safety

Lead Guest Editor Moreno BondiGuest Editors Simona de NiederhausernChrissanthy Papadopoulou Andrea Laukova and Patrizia Messi

Copyright copy 2017 Hindawi All rights reserved

This is a special issue published in ldquoJournal of Food Qualityrdquo All articles are open access articles distributed under the Creative Com-mons Attribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Editorial Board

Encarna Aguayo SpainRiccarda Antiochia ItalyJorge Barros-Velaacutezquez SpainJoseacute A Beltraacuten SpainAacute A Carbonell-Barrachina SpainMarina Carcea ItalyMaria Rosaria Corbo ItalyEgidio De Benedetto ItalyAlessandra Del Caro ItalyAntimo Di Maro Italy

Rossella Di Monaco ItalyHuumlseyin Erten TurkeySusana Fiszman SpainAndrea Galimberti ItalyEfstathios Giaouris GreeceVicente M Goacutemez-Loacutepez SpainElena Gonzaacutelez-Fandos SpainAlejandro Hernaacutendez SpainJesuacutes Lozano SpainSara Panseri Italy

Mariacutea B Peacuterez-Gago SpainWitoon Prinyawiwatkul USAEduardo Pueacutertolas SpainJuan E Rivera MexicoFlora V Romeo ItalyJordi Rovira SpainAmy Simonne USAGiuseppe Zeppa Italy

Contents

Natural Preservatives to Improve Food Quality and SafetyMoreno Bondi Andrea Laukovaacute Simona de Niederhausern Patrizia Messi and Chrissanthy PapadopoulouVolume 2017 Article ID 1090932 3 pages

Natural Food Additives and Preservatives for Fish-Paste Products A Review of the Past Present andFuture States of ResearchKhawaja Muhammad Imran Bashir Jin-Soo Kim Jeong Hyeon An Jae Hak Sohn and Jae-Suk ChoiVolume 2017 Article ID 9675469 31 pages

Development of a Chemically Defined Medium for Better Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31Wenli Liu Lanwei Zhang and Huaxi YiVolume 2017 Article ID 9017452 8 pages

Lipid Oxidation Color Changes and Microbiological Quality of Frozen Beef Burgers Incorporatedwith ShiraziThyme Cinnamon and Rosemary ExtractsHadi Hashemi Gahruie Seyed Mohammad Hashem HosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan ShadVolume 2017 Article ID 6350156 9 pages

Optimization of Ultrasound Extraction of Cactus Pear (Opuntia ficus indica) Seed Oil Based onAntioxidant Activity and Evaluation of Its Antimicrobial ActivityMariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-Cansino Ernesto Alaniacutes-GarciacuteaLuis Delgado-Olivares Joseacute Alberto Ariza-Ortega Esther Ramiacuterez-Morenoand Joseacute de Jesuacutes Manriacutequez-TorresVolume 2017 Article ID 9315360 9 pages

Antioxidant and Antimicrobial Properties of Cactus Pear (Opuntia) Seed OilsEsther Ramiacuterez-Moreno Raquel Carintildeo-Corteacutes Nelly del Socorro Cruz-Cansino Luis Delgado-OlivaresJoseacute Alberto Ariza-Ortega Vanessa Yelina Montantildeez-Izquierdo Mariacutea Manuela Hernaacutendez-Herreroand Tomaacutes Filardo-KerstuppVolume 2017 Article ID 3075907 8 pages

EditorialNatural Preservatives to Improve Food Quality and Safety

Moreno Bondi1 Andrea Laukovaacute2 Simona de Niederhausern1

Patrizia Messi1 and Chrissanthy Papadopoulou3

1Department of Life Sciences University of Modena and Reggio Emilia Via G Campi 287 Modena Italy2Institute of Animal Physiology Slovak Academy of Sciences Soltesovej 4-6 040 01 Kosice Slovakia3Microbiology Department Faculty of Medicine School of Health Sciences University of Ioannina Ioannina Greece

Correspondence should be addressed to Moreno Bondi morenobondiunimoreit

Received 12 October 2017 Accepted 12 October 2017 Published 12 December 2017

Copyright copy 2017 Moreno Bondi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Food products can be contaminated by a variety of path-ogenic and spoilage microbiota the former causing food-borne diseases and the latter causing significant economiclosses for the food industry due to undesirable effects onthe food properties According to the Centers for DiseaseControl and Prevention (CDC) each year in the UnitedStates 48 million people get sick 128000 are hospitalizedand 3000 die because of foodborne infections Howeveralthough foodborne outbreaks are well recorded sporadiccases are not because not all patients visit the doctor orenter the hospital and the causative agent is not alwaysidentified A considerable number of foodborne pathogens ofgreat public health importance (eg VTEC E coli serotypesCampylobacter jejuni Listeria monocytogenes and Yersiniaenterocolitica) have emerged during the recent two decadescausing severe illness and foodborne outbreaks worldwide

Microbial food spoilage is also an area of immenseconcern for the food industry It is estimated that as much as25 of all food produced is lost after harvest due to microbialactivity While the growth of spoilage microbiota in foodsis not harmful for the human health it has negative impacton the shelf-life textural characteristics and overall qualityof the finished products affects the consumer choices andresults in significant commercial losses Thus prevention orinhibition of microbial growth in foods is of outmost impor-tance for the current globalized food production Hencethere is still the need for new processing methods to be usedeither alone or in combination with the already existing onesable to reduce or eliminate foodborne pathogens and spoilagebacteria

Chemical additives have been extensively used to preventthe survival and proliferation of microorganisms but their

safety and impact on human health are under discussionSince the reduction or elimination of pathogens and spoilagemicroorganisms in food is the foremost priority the currenttrends in food processing are focusing on the use of naturalcompounds which are considered as safe alternatives andsatisfy the consumer preferences for more ldquogreen foodsrdquoHence the increased awareness on the safety of food additivesand preservatives and the consumerrsquos trend to avoid foodscontaining chemicals which in the long-term may haveadverse impact on their health have generated a significantnumber of studies and publications on the potential useof various natural substances recognized as GRAS (Gener-ally Recognized as Safe) to be used as food preservativesChemical compounds added to foods as antioxidant agentsare also of concern particularly when important proteinsources (eg burgers steaks) are involved in the daily diet ofwesternized consumer living in the developed countries [1 2]Synthetic antioxidants such as BHT TBHQ and BHA havedemonstrated various adverse effects on the human healthincluding allergy headache asthma and dermatitis Recentstudies on the utilization of natural antioxidants (eg herbalessential oils and extracts) indicate their capacity and safety[3 4] Also the antimicrobial properties of natural substancessuch as plant essential oils and extracts have been extensivelystudied with promising results [5] The proper recycling anduse of fruit-processing plants by-products like fruit seedsor skins discarded and piling up in huge amounts everyyear are of great interest for the food industry particularlytheir potential to be a useful source of oil and meal [6]Additionally the oil from plant seeds can be used by thefood industry for manufacturing more ldquonaturalrdquo or ldquogreenrdquofoods and also can sufficiently extend the shelf-life of the

HindawiJournal of Food QualityVolume 2017 Article ID 1090932 3 pageshttpsdoiorg10115520171090932

2 Journal of Food Quality

food product [7] The oils derived from fruit seeds oils mayalso have some more useful properties beyond being justldquoediblerdquoThe oil derived from the seed extract of twoMexicanvarieties of cactus pear (Opuntia albicarpa and Opuntia ficusindica) has been found to have sufficient antioxidant andantimicrobial properties [8] Furthermore some biologicalactive compounds produced by microorganisms are widelyused in the food industry as well A good alternative toconventional chemically synthesized food preservatives is theuse of natural antimicrobials such as bacteriocins producedby lactic acid bacteria (LAB) with Nisin being officiallyemployed by the food industry and thus the most widelyused Bacteriocins are peptides actually microbial toxinsproduced from various microorganisms and so far someof them (eg enterocins produced mostly by enterococci)have shown remarkable antimicrobial potential and theirapplication as a natural barrier against pathogens and foodspoilage has been proven to be very efficient when used inthe form of purified or semipurified extracts or as protectivecultures [9 10] Therefore as the developments in foodpreservation are focusing on the implementation of naturalantimicrobials and antioxidants this special issue exploresthe potential of alternatives to currently used preserva-tives through the publication of five high-quality articleswhich aim to address recent advancements in the field ofnatural food preservatives and antioxidants The prospectto replace synthetic preservatives with natural substanceshas been demonstrated by comparing the effects of Shirazithyme cinnamon and rosemary extracts (denoted as naturalantioxidants) with those of the synthetic antioxidant BHT onprotein and lipid oxidations physicochemical microbial andsensory characteristics of frozen beef burgers during storageSpecifically the oxidative stability of the beef burgers contain-ing Shirazi thyme cinnamon and rosemary extracts was welldemonstrated and the antibacterial activitywas documentedas the total microbial counts of the tested burgers were wellbelow the maximum allowed limit Besides the evaluationof the antimicrobial and antioxidant properties of naturalsubstances it is important to optimize their recovery Withregard to bacteriocins to enhance Enterocin Y31 productionand simplify the steps of separation and purification a propersimplified and defined medium (SDM) has been developedfor the Enterococcus faecium Y31 growth and enhancementof the Enterocin Y31 production The bacterial growth didnot result in Enterocin Y31 production in MRS medium andtherefore both the growth rate and the EnterocinY31 produc-tion were set as the goal for the investigation Single omissionexperiments revealed that 5 gL NaCl five vitamins twonucleic acid bases MgSO4sdot7H2O MnSO4sdot4H2O KH2PO4K2HPO4 CH3COONa fourteen amino acids and glucosewere essential for the adequate strain growth and EnterocinY31 production As a result a novel simplified and definedmedium (SDM) was formulated containing 30 ingredientsin which the Enterocin Y31 production yield was higherwhen compared to either MRS or CDM The developmentof the SDM improved the Enterocin Y31 production andsimplified the steps of purification (only two steps) whichis very promising and increases its potential applicationsReferring to seedsrsquo oils the optimization of the extraction

conditions of cactus pear seed oil has been obtained usingultrasound in a closed system based on the antioxidantactivity and using response surface methodology The yieldextraction and antioxidant and antimicrobial activity werecompared with those obtained using both conventional andunconventional methods such as Soxhlet and macerationusing heat agitation or long extraction times microwavesupercritical fluids and ultrasound-assisted extraction inan open and in a closed system The results have shownthat ultrasound exhibited lower oil yield and antioxidantactivity but had the potential to achieve comparable resultsif multiple ultrasound extractions are performed in the timeneeded by conventional methods Seed oils showed similarantimicrobial activity despite the extraction method and canbe an alternative extraction method of seed oils from fruitssuch as cactus pear Lastly the replacement of chemicaladditives with natural compounds has been addressed for fishfoods as well Fish-paste products also known as fish cakes orsurimi-based products are worldwide favorites Surimi a wetprotein concentrate of fish muscle is used as an intermediateraw material to produce surimi seafood The flavor texturetaste shelf-life and market value of surimi-based productsdepend on several factors including the additives used toprepare the surimi While preparing surimi with chemicaladditives several problems have been observed such as alack of unique characteristics inferior acceptability and poorfunctionality In this context a systematic review of fish-paste products prepared using natural food additives (eganimal seafood and plant source additives herbs and orientalmedicines grains and roots and functional food materials)has been performed which summarizes the existing relevantknowledge in the production of new value-added foodstuffsof interest for the surimi industry

In conclusion this special issue offers to the readers thechance to be informed on the recent advancements relatedto the antimicrobial and antioxidant properties of naturalsubstances that are of interest for the contemporary foodindustry Their prospective use in the food production hasthe potential to lead towards the production of safer andhealthier foods not excluding their contribution to a moreefficient preservation of the environment when chemicalswill be replaced with natural substances

Moreno BondiAndrea Laukova

Simona de NiederhausernPatrizia Messi

Chrissanthy Papadopoulou

References

[1] G Comi E Tirloni D AndyantoMManzano and L IacuminldquoUse of bio-protective cultures to improve the shelf-life andthe sensorial characteristics of commercial hamburgersrdquo LWT -Food Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[2] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWT - FoodScience and Technology vol 68 pp 385ndash390 2016

Journal of Food Quality 3

[3] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[4] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[5] H Sakkas P Gousia V Economou V Sakkas S Petsios and CPapadopoulou ldquoIn vitro antimicrobial activity of five essentialoils on multidrug resistant Gram-negative clinical isolatesrdquoJournal of Intercultural Ethnopharmacology vol 5 no 3 pp212ndash218 2016

[6] B Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Fatty Acids in Foods and their Health ImplicationsThirdEdition vol 20073230 of Food Science and Technology pp 263ndash301 CRC Press 3rd Edition edition 2007

[7] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

[8] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research (Formerly Natural Product Letters)vol 27 no 14 pp 1305ndash1314 2013

[9] R Iseppi F Pilati M Marini et al ldquoAnti-listerial activity of apolymeric film coated with hybrid coatings doped with Ente-rocin 416K1 for use as bioactive food packagingrdquo InternationalJournal of Food Microbiology vol 123 no 3 pp 281ndash287 2008

[10] A Laukova and P Turek ldquoEffect of enterocin 4231 in Slovak fer-mented salami puchov after its experimental inoculation withListeria Innocua Lirdquo ACTA Scientiarum Polonorum TechnologiaAlimentaria vol 10 no 4 pp 423ndash431 2011

Review ArticleNatural Food Additives and Preservatives forFish-Paste Products A Review of the Past Present andFuture States of Research

Khawaja Muhammad Imran Bashir1 Jin-Soo Kim2 Jeong Hyeon An1

Jae Hak Sohn13 and Jae-Suk Choi13

1Seafood Research Center IACF Silla University 606 Advanced Seafood Processing Complex Wonyang-roAmnam-dong Seo-gu Busan 49277 Republic of Korea2Department of Seafood and Aquaculture Science Gyeongsang National University 38 Cheondaegukchi-gilTongyeong-si Gyeongsangnam-do 53064 Republic of Korea3Food Biotechnology Division of Bioindustry College of Medical and Life Sciences Silla University 140 Baegyang-daero700 beon-gil Sasang-gu Busan 46958 Republic of Korea

Correspondence should be addressed to Jae-Suk Choi jsc1008sillaackr

Received 9 June 2017 Revised 15 August 2017 Accepted 17 September 2017 Published 27 November 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Khawaja Muhammad Imran Bashir et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Fish-paste products also known as fish cakes or surimi-based products are worldwide favorites Surimi a wet protein concentrateof fish muscle is used as an intermediate raw material to produce surimi seafood The flavor texture taste shelf-life and marketvalue of surimi-based products depend on the source of the fish meat type of applied heat treatment and additives used toprepare the surimi While preparing surimi with chemical additives several problems have been observed such as a lack of uniquecharacteristics inferior acceptability and poor functionality Various types of fish-paste products have been developed by usingdifferent ingredients (eg vegetables seafood herbs and oriental medicines grains and roots including carrots and functionalfood materials) However a systematic review of fish-paste products prepared using natural food additives has not yet beenperformedTherefore the quality characteristics of fish-paste products and their functionalities were elucidated in this study Withthe increasing demand for surimi seafood products the functional properties physiochemical properties and shelf-life of surimi-based products need to be improved This review will aid the preparation of new value-added products in the surimi industry

1 Introduction

Fish-paste products popularly known as fish cakes areproduced from frozen surimi (ie they are a kind of surimi-based product) and are popular in Korea and Japan [1] Inthe Korean Food Standards Codex fish cakes are known asa processed marine product comprising salt-soluble proteinsisolated from fish meat [2] Fish muscle is mechanicallydeboned washed with water and blended with cryoprotec-tants to prepare a wet concentrate of proteins called surimiSurimi is a Japanese term that is also known as washed fishmince It is a refined fish myofibrillar protein manufacturedthrough numerous step-by-step processes including headinggutting filleting deboning (mincing) washing dewatering

refining mixing with cryoprotectants freezing and metaldetection for HACCP [3] The myofibrillar proteins make itan excellent ingredient for developing food products It hasexcellent gelling properties and forms strong and elastic gelsupon heating [4]

The setting and deformation are important to preparesurimi and surimi-based products Setting also known asldquosuwarirdquo in Japanese is a very important process which hasa significant influence on the physiological and rheologicalproperties of surimi-based products Setting is a vital processin the quality estimation of surimi because it helps to improvethe water-holding capacity as well as the gel texture of surimi-based productsWhen fishmince paste (sol) is heated at a lowtemperature (up to 50∘C) a loose network (suwari) is formed

HindawiJournal of Food QualityVolume 2017 Article ID 9675469 31 pageshttpsdoiorg10115520179675469

2 Journal of Food Quality

from myosin and actomyosin molecules this process isreferred to as setting Setting is species dependent and occursover a range of temperatures (up to 50∘C) and to a varyingextent As the temperature is increased to around 70∘Csuwari is partially disrupted to form a broken net structure(modori) a phenomenon attributed to the dissociation ofmyosin from actin and the possible fragmentation of the actinfilament [5ndash7]

Most of the surimi-based products are different types offish-paste products while less than 10 include fish burgersfish ham and fish sausages [3] Surimi-based products areprepared by mixing the raw or frozen surimi with saltsand other ingredients molded and heated to form the finalproduct in the specified shape and texture and pasteurizedbefore packaging The kind of heat treatment depends on theflavor texture and appearance of the desired final productand may include broiling steaming deep-fat frying andboiling [8] while fish-paste products in South Korea aremostly prepared by frying [9] Textural characteristics suchas gel strength are the major determinant of surimi priceand quality [10] Several studies have attempted to enhancethe textural quality of surimi or surimi-based products usingvarious protein additives [11ndash14]

Surimi quality and gelling property are mainly affectedby both intrinsic factors (effect of fish species seasonalitysexual maturity and freshness or rigor) and extrinsic fac-tors (harvesting handling water characteristics processingtime and temperature solubilization of myofibrillar proteinsduring processing the activity of the endogenous or addedprotein oxidants and proteolytic enzymes washing cyclessalinity and pH) [3 134] Surimi forms thermoirreversiblegels upon heating which do not deform with further changein the temperature This phenomenon of surimi and surimi-based products is similar to that observed in other proteinssuch as egg white milk-lactoglobulin and wheat glutenAdditionally surimi produces gels of very high deformabilityand strength This heat-induced gelation property of surimimakes it a very valuable food ingredient [134]

The gel-forming ability and capacity of surimi areadversely affected by the proteolytic degradation of myofib-rillar proteinsThe presence of indigenous proteinases causedgel softening in surimi made from fish species for examplethreadfin bream [135] arrow tooth flounder [136] Pacificwhiting [137] and lizard fish and bigeye snapper [20 59]Various active proteinases in fish muscle are responsible forsoftening of the surimi gels Nakamura and Ogawa and Anet al testified that cathepsins L and B were the most activecysteine proteinases in Pacific whiting surimi and fish filletsrespectively [7 138] The myofibril-associated proteinasesobserved in lizardfish surimi were serine proteinases andcysteine while a serine proteinase was reported in the bigeyesnapper surimi [20 59]

Seasonal analysis of the compositional properties ofAlaska pollock and Pacific whiting showed higher proteincontents in winter while the moisture contents were higherin summer [139 140] Surimi prepared from cold-water fishspecies with low thermostability of myofibrillar proteinsmakes setting easier Normally a myofibrillar protein withlow thermostability is optimum to do setting because its

reactivity is increased due to the loose internal structure bysodium chloride addition and heat denaturation In contrastthe myofibrillar protein of tropical fish species with high heatstability is difficult to denature and form the myofibrillarprotein network structure in surimi [3]

Several research groups have studied ways to enhance thequality of surimi-based products by investigating the changesin microbial content enzyme activity nutrient content andacceptability characteristics the use of raw materials thestandardization of the manufacturing process storage andmarketing Natural and chemical food-grade additives suchas konjac flour proteinase inhibitors egg white and hydro-colloids have been used to enhance the gelling properties ofsurimi [12 17 20 23 34 141ndash143] The trypsin inhibitor inegg white plays a major role in improving the gel strengthof surimi The addition of egg white inhibits the proteolyticactivity of the modori-inducing enzyme in fish meat andsuppresses the decrease of elasticity in surimi Serum pro-teins have strong inhibiting abilities against the action ofvarious proteases with different active centers such as SHgroups and serine groups In addition they also containtransglutaminases that accelerate the setting Egg white andserum proteins also play an important role in inhibiting theenzymatic activity of the parasites Apart from the use ofadditives gel strengthening can be achieved by treating thegels at low temperatures (0ndash40∘C) before cooking [144 145]Furthermore the gel quality of surimi and surimi-basedproducts can also be enhanced by using alternate fish speciesor by acid and alkali washing to increase the myofibrillarprotein concentrations [7 146 147]

Surimi production worldwide reached around800000MT by 2011-2012 [3] while South Korea alonecontributed approx 156000MT in 2013 Over the yearsthe size of the market for Korean fish-paste products hasgradually increased reaching sim350 million US dollars in2013 (based on the amount produced) [148] Howevermanufacturers have had several problems in producingsurimi-based products such as a lack of unique character-istics and inferior acceptability and functionality Thereforethere have been several attempts to develop new fish-pasteproducts with excellent acceptability and functionalityTo this end numerous types of fish-paste products havebeen developed using various natural ingredients such asvegetables seafood animals plants herbs and orientalmedicines seaweed and functional food materials It is ofworldwide interest to use these natural food preservativesinstead of chemical or synthetic ones However to date nosystematic review of fish-paste products supplemented withvarious food raw materials has been performed Thereforethe quality characteristics of fish-paste products and theirfunctionalities were elucidated in this study

2 Improvement of the Gel Properties ofFish-Paste Products

Various food additives derived from animals (eg beefswine and chicken) seafood (eg fish invertebrates) plants(eg legumes cereals) sugars polyols and functional mate-rials used in fish-paste products to improve their gelling

Journal of Food Quality 3

capabilities and strength are listed in Table 1 and describedbelow

21 Animal Source Additives Various food-grade proteaseinhibitors from animal sources are used to enhance thephysical properties of surimi-based products as well to pre-vent the protein degradation The ability of beef plasma andother food-grade additives in surimi and fishmince preparedfrom Pacific whiting (Merluccius productus) was studied byMorrissey et al [12] The strongest proteolytic inhibitionwas observed with beef plasma protein at a concentrationas low as 1 Reppond and Babbitt reported the increase ingel strength of gels prepared by arrow tooth flounder at aconcentration of 2 with a yellow hue color [16] Weeras-inghe et al characterized the inhibitory activity of these food-grade inhibitors and reported that the inhibitory activity wasmainly because of specific serine proteinase inhibitors [17]The addition of 2 dried bovine plasma to steamed fish-pasteslightly increased the chewiness and hardness but it showeda negative effect on the gel strength [18] Duangmal andTaluengphol reported that the higher levels of beef plasmaprotein unfavorably affected gel characteristics of red tilapiasurimi gels [19]

The effect of porcine plasmaprotein on the bigeye snapper(Priacanthus tayenus) surimi gel characteristics was investi-gated by Benjakul et al [14]The gels supplemented with 05porcine plasma protein had the highest level of deformationand breaking force Benjakul and colleagues later reportedthe effect of porcine plasma protein on the gel characteristicsof surimi from bigeye croaker (Pennahia macrophthalmus)bigeye snapper (P tayenus) barracuda (Sphyraena jello)and threadfin bream (Nemipterus bleekeri) [20] The porcineplasma protein was effective in increasing the deformationand breaking force of kamaboko gels Higher breaking forcesand levels of deformation occurred when chicken plasmaprotein was supplemented to sardine kamaboko gels at levelsup to 2 [21] The inhibitory activities of cysteine proteinaseinhibitor fraction from chicken plasma on Pacific whitingand arrow tooth flounder mince were reported by Rawdkuenet al [22] Furthermore similar results were observed intheir extended study onPacificwhiting surimi where chickenplasma at a level of 2 inhibited the degradation of myosinheavy chain proteins [23]

Ovomucoid is a mucoprotein obtained from egg whitethat has been tested for its potential as a gel-degradationinhibitor [24 25] The addition of 2 ovomucoid couldincrease the breaking strength and gel deformation [28]The autolytic activities of lizardfish (Saurida tumbil) surimiand mince under the application of protease inhibitors wereinvestigated by Yongsawatdigul and Piyadhammaviboon[26] At all preincubation conditions egg white enhancedthe gel-forming capability of S tumbil surimi to a greaterextent than did whey protein concentrateThe addition of 1egg white and preincubation at 25∘C increased the breakingforce by twofold Campo-Deano and Tovar [27] reportedthat the addition of egg albumen at 15 and 2 for Alaskapollock and Pacific whiting surimi respectively enhancedthe gel strength of crab sticks According to Hunt et al theincorporation of 2-3 special dried egg white improved

the gel textural characteristics of Alaska pollock and Pacificwhiting surimi [28]

Whey is the complete set of proteins isolated fromthe watery portion of milk Whey protein is comprisedof 20 milk protein and 80 casein [149] Whey proteinconcentrates have generally been used as an emulsifierfiller water binder protein supplement foam stabilizer andthickener as well as gelling agent [150] Rawdkuen andBenjakul investigated the effect of whey protein concentrateon the gelling characteristics of surimi prepared fromgoatfish(Mulloidichthys vanicolensis) bigeye snapper (P tayenus)lizardfish (S tumbil) and threadfin bream (N bleekeri) [29]All the tested surimi supplemented with 3 whey proteinconcentrate displayed inhibitory activity against autolysis andsignificantly reduced gel whiteness However better water-holding capacity was obtained by increasing concentrationsof whey protein concentrate

Plasma proteins produced from pig cow and chickenbyproducts are relatively affordable and easily collectiblesources [143 151 152] However outbreaks of foot-and-mouthdisease avian influenza andmad cow disease as well as a banonproteins frompig bone and skin in some states for religiouscauses have made it essential to search alternative sources[153 154] Various fish plasma proteins have been testedincluding those from rainbow trout and salmon [31 35 36]

22 Seafood Additives The effects of shrimp head proteinhydrolysate fromdifferent shrimp namely black tiger shrimp(Penaeus monodon) northern pink shrimp (Pandalus eous)and endeavour shrimp (Metapenaeus endeavouri) on thegelling properties of lizardfish (Saurida spp) surimi wereinvestigated by Ruttanapornvareesakul et al [30] It wasreported that the freeze-induced denaturation of lizardfishmuscle protein could be reduced by the supplementation ofshrimp head protein hydrolysate at a concentration of 5resulting in higher Ca-ATPase activity and gel strength Theeffects of rainbow trout plasma proteins on the gelling prop-erties of surimi prepared by Alaska pollock were investigatedby Li et al [31] Gel degradation deformation the breakingforce water-holding capacity and whiteness enhanced withincreasing amounts of rainbow trout plasma protein anddecreased at higher concentrationsThe rainbow trout plasmaprotein at a concentration of 075mgg could be used asa potential protease inhibitor to inhibit gel weakening inAlaska pollock surimi Li et al reported the higher inhibitoryactivities of the recombinant chum salmon cystatin againstautolysis of Alaska pollock surimi [155]

Fish gelatin is extracted from the collagen of fish skinand it is used as a food additive Hernandez-Briones et alstudied the functional and mechanical properties of Alaskapollock surimi gels while using fish gelatin as an additive[32] The increasing concentration of gelatin affected thewhiteness but the sensory panelists were unable to detect itThese results showed that fish gelatin was not effective as afunctional additive in Alaska pollock surimi Nevertheless itcould be added at up to 10 gkg without negatively affectingthe mechanical properties of surimi Yin et al reported asignificant improvement in the endogenous transglutaminaseactivity of Alaska pollock surimi prepared with nanoscaled

4 Journal of Food Quality

Table1Naturalfood

additiv

esused

toim

provethe

gelpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Animalsource

additiv

es

Beefplasma

hydrolysate

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Atlanticmenhaden

(Brevoortia

tyrann

us)

Alaskap

ollock

(Theragra

chalcogram

ma)

Moistu

recontentproteincontent

cook

inglossw

ater-holding

capacitytexturetorsio

ntest

05

ndash15

[15]

Bovine

plasma

Bostaurus

Heatedin

awater

bath

Powder

Arrow

toothflo

under

(Atheresthessto

mias)

Walleye

pollo

ck

Moistu

recontentpu

nchtorsion

colortest

2[16]

Beefplasma

protein

Bostaurus

mdashPo

wder

Pacific

whitin

g(M

erlucciusp

rodu

ctus)

Proteincontentinhibitory

assay

4[17]

Drie

dbo

vine

plasma

Bostaurus

Steaming

Powder

Alaskap

ollock

(Tchalco

gram

ma)

Nutrie

ntcontentpH

water-holding

capacitytexture

and

sensoryevaluatio

n2

[18]

Beefplasma

protein

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Redtilapia

(Oniloticus

xO

placidus)

Colortextureexpressiblewater

protein

totalsulfhydrylcon

tent

2gkg

[19]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Bigeye

snapper

(Pria

canthu

stayenus)

Expressib

ledrip

amou

ntcolor

texturesetting

cond

ition

s05

[14]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Threadfin

bream

(Nem

ipterus

bleekeri)Bigeyes

napp

er(Ptayenus)

Baracuda

(Sphyraena

jello)and

Bigeye

croaker

(Penna

hiamacrophthalmus)

Trichloroacetic

acid-solub

lepeptidescolortextureprotein

content

05

[20]

Chickenplasma

protein

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Sardine

(Sardinella

gibbosa)

Colortextureexpressiblemoistu

re

proteincontentautolysis

activ

ity2

[21]

Cyste

inep

roteinase

inhibitorfrom

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Arrow

toothflo

under

(Astomias)Pacific

whitin

g(M

produ

ctus)

Autolysis

andinhibitory

activ

ity

pHprotein

content

3[22]

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Pacific

whitin

g(M

produ

ctus)

Torsionandfracture

test

dynamic

rheologicalattribute

2[23]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[24]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[25]

Eggwhite(EW)

Gallusgallusd

omesticus

Heatedin

awater

bath

Powder

Lizardfish(Saurid

atumbil)

mince

andsurim

iAu

tolytic

activ

itytexturalattributes

EW1

[26]

Eggalbu

min

Gallusgallusd

omesticus

Heatedin

thec

ooking

roller

Eggwhite

itself

Surim

i-based

crab

sticksfrom

Alaskap

ollock

(AP)

Pacific

whitin

g(PW)

(Mprodu

ctus)

Transie

nttest

streng

thtest

texture

dynamicrheologicaland

physical

attributes

AP

15

PW2

[27]

Journal of Food Quality 5

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Regu

lard

riedegg

white(REW

)speciald

riedegg

white(SEW

)liq

uideggwhite

(LEW

)

Gallusgallusd

omesticus

Heatedin

awater

bath

Spray-dried

powder

Pacific

whitin

g(M

produ

ctus)

Totalsulfhydrylgroup

sfracture

test

dynamicrheologicalattribute

SEW2-3

[28]

Wheyprotein

concentrate

Bostaurus

Heatedin

awater

bath

Wheyprotein

concentrate

Bigeye

snapper(Ptayenu

s)Goatfish

(Mulloidich

thys

vanicolen

sis)

Threadfin

bream

(Nblee

keri)

and

Lizardfish(Stum

bil)

Water-holding

capacitycolor

autolytic

activ

ity3

[29]

Seafoo

dadditiv

esSh

rimphead

proteinhydrolysate

from

northern

pink

shrim

pendeavou

rshrim

pand

blacktig

ershrim

p

Pand

alus

eous

Metapenaeus

endeavouri

Pena

eusm

onodon

Heatedin

awater

bath

Drie

dmatter

Lizardfish

(Saurid

aspp)

Gelstr

engthcolorgel-forming

abilityC

a-AT

Pase

activ

ity5

[30]

Rainbo

wtro

utplasmap

rotein

Oncorhynchu

smykiss

Heatedin

awater

bath

Freeze-drie

dplasma

Alaskap

ollock

Proxim

atea

nalysisw

ater-holding

capacitycolortextureprotein

content

075

mgg

[31]

Fish

gelatin

Com

mercialfishgelatin

(Gelatin

Rousselot)

Heatedin

awater

bath

Powder

Alaskap

ollock

Colorm

echanicalfunctio

nal

sensoryattributes

10gkg

[32]

Nanoscaled

fish-bo

neof

Pacific

whitin

gMprodu

ctus

Heatedin

awater

bath

Powder

Alaskap

ollock

Texturescanning

electron

microscop

y1g10

0g[33]

Nanoscaled

fish-bo

ne(N

FB)+

driedeggwhite

(DEW

)

Mprodu

ctusGallus

gallu

sdom

esticus

Heatedin

awater

bath

Powder

Pacific

whitin

g(M

produ

ctus)

Rheologicaland

texturalattributes

DEW

1+

10mgNFB

Cag

surim

ipaste

[34]

Salm

onbloo

dplasma

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)

Scanning

electronmicroscop

yproteincontentdynamic

rheologicalattributes

1g10

0g[35]

6 Journal of Food QualityTa

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Freeze-drie

dchinoo

ksalm

onplasma(

FSP)

and

concentrate

salm

onplasma

(CSP

)

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)surim

iand

Salm

onmince

Proteolytic

inhibitio

nautolysis

proteincontent

Salm

onminceC

SPgt

FSP

Pacific

whitin

gsurim

iFSP

[36]

Partially

purifi

edtrypsin

inhibitor

from

ther

oeof

yello

wfin

tuna

fish

Thun

nusa

lbacares

Heatedin

awater

bath

Freeze-drie

dBigeye

snapper

(Pria

canthu

smacracanthu

s)Proteolysis

colorw

ater-holding

capacitygellin

gprop

ertie

s3g

100g

[37]

Squidink

tyrosin

ase(SIT)

+tann

icacid

(TA)

Todarodesp

acificus

Heatedin

awater

bath

Mixture

Sardine

(Sardinella

albella)

Tyrosin

asea

ctivityinvitro

oxidationassaycolortexturaland

sensoryattributes

SIT

500U

gprotein+

TA1

[38]

Plantsou

rcea

dditives

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soybean

protein

Wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[39]

Soyprotein

eggwhite(EW)

wheyprotein

concentrate

(WPC

)La

ctalbumin

(LA)

milk

proteiniso

late

(MPI)

Glycinem

ax

Gallusgallusd

omesticus

Bostaurus

Coo

kedin

aste

amcooker

Powder

AlaskaP

ollock

(Tchalco

gram

ma)

Textureexpressib

lemoistu

recontentwater

retentionprop

ertie

sEW

andMPI

[4041]

Legu

mes

eed

extractfrom

blackcowpea

whitecowpea

soybeanseeds

Mun

gbean

peanut

Vignaun

guicu

lata

Glycinem

axVignaradiata

Arachish

ypogaea

mdash

Freeze-drie

dproteinase

inhibitor

extracts

Threadfin

bream

(Nem

ipterid

ae)

ThermalstabilitypHprotein

contentproteinase

inhibitory

assay

Blackcowpea

soybeanseeds

30mgg

[42]

Legu

mes

eed

extractfrom

Cow

pea

pigeon

pea

bambara

grou

ndnu

ts

Vignaun

guicu

lata

Cajanu

scajan

Vo

andzeia

subterranea

mdashPartially

purifi

edTrypsin

Threadfin

bream

(Nem

ipterid

ae)

Sarcop

lasm

icmod

ori-ind

ucing

proteinase

activ

itycolor

30ku

nits

g[43]

bambara

grou

ndnu

tprotein

isolate

Vignasubterranea

Heatedin

awater

bath

Powder

Threadfin

bream

(Nblee

keri)

Colorautolysis

025

g100g

[44]

Soyproteiniso

late

Glycinem

axHeatedin

awater

bath

Com

mercial

soyprotein

isolate

(JinQ

ui1200)

Alaskap

ollock

(Tchalco

gram

ma)

Com

mon

carp

(Cyprin

uscarpio)

Totaln

itrogen

andmoistu

recontentgelstre

ngthcolor

10

[45]

Journal of Food Quality 7Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soyprotein

wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[46]

Dietary

fiber

(DF)

from

peaa

ndchicory+

microbial

transglutaminase

(MTG

ase)

Cichorium

intybu

sPisum

sativ

umHeatedin

awater

bath

Powder

Hake(Mcapensis)

Gilthead

seabream

(Sparusa

urata)

Seab

ass(Dice

ntrarchu

slabrax)

Meagre(Argyrosomus

regius)

Dyn

amicrheologicalattributes

MTG

ase100U

g[47]

Proteiniso

lates

from

Mun

gbean

(MBP

I)black

bean

(BBP

I)bam

bara

grou

ndnu

t(BG

PI)

Phaseolusa

ureus

Phaseolusv

ulgarisV

igna

subterranea

mdashFreeze-drie

dpo

wder

mdash

Scanning

electronmicroscop

yproteolytic

autolyticandtrypsin

inhibitory

activ

ityassaycolor

texturetrichloroacetic

acid-solub

lepeptidec

ontent

1g10

0g[48]

Partially

purifi

edtrypsin

inhibitor

from

adzukibean

Vignaangularis

Heatedin

awater

bath

Freeze-drie

dpo

wder

Threadfin

bream

(Nblee

keri)

Proteincontenttexturecolor

trypsin

inhibitory

activ

ityautolytic

activ

ityassay

3g10

0g[49]

Amylose(A)a

ndam

ylop

ectin

(AP)

mdashHeatedin

awater

bath

Powder

Walleye

pollo

ck(T

chalcogram

ma)

Gelationandbreaking

strength

Amylose70+

Amylop

ectin

4

[50]

Wheatsta

rch

Triticum

aestivum

Heatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Com

pressio

ntest

dynamic

viscoelasticityscann

ingele

ctron

microscop

y

Starch10g

+Surim

i10g

[51]

Natives

weetp

otato

starch(N

SPS)

and

Mod

ified

sweet

potato

starch

(MSP

S)

Ipom

oeabatatas

Heatedon

acontrolled

stress

rheometer

Powder

Alaskap

ollock

(T

chalcogram

ma)

Dyn

amicrheologicalattributes

5[52]

Potato

starch

Solanu

mtuberosum

Heatedin

the

Krehalon

ecasin

gfilm

Powder

Pacific

sand

lance(Am

modytes

personatus

Gira

rd)

Proxim

atea

nalysis

protein

compo

sition

colorfoldingtext

texturalandsensoryattributes

8[53]

Rice

flour

Oryza

sativa

Fried

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorrheologicaland

sensoryattributes

10ndash15

[54]

Rice

flour

Oryza

sativa

Fried

Powder

Threadfin

bream

(Nem

ipterid

ae)

Moistu

recontentpH

color

texturalandsensoryattributes

50

[55]

Rice

flour

Oryza

sativa

Fried

Powder

Goldenthreadfin

bream

(Nem

ipterusv

irgatus)

Gelstr

engthsensoryattributes

14

[56]

Cryoprotectantsa

ndhu

mectants

Xanthan(X)

locustbean

(LB)

gumsa

loneX

LB

ratio

Ceratoniasiliqua

Heatedin

awater

bath

Powder

Silver

carp

(Hypophthalm

ichthys

molitrix)

Torsiontest

gel-formingability

mechanicalattributes

XLB

025075

[57]

Pectin

gum

(HM

LM)+

CaCl2

mdashHeatedin

awater

bath

Gum

and

powder

Silver

carp

(Hm

olitrix)

Water-holding

capacitym

echanical

andtexturalattributes

Pectin

gum1+

CaCl202

[58]

8 Journal of Food Quality

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Chito

san7B

from

praw

nshell

Not

mentio

ned

Heatedin

awater

bath

Not

mentio

ned

Barred

garfish

(Hem

iramphus

far)

ProteincontentSE

Mtextural

attributes

1[59]

Konjac

glucom

annan

aqueou

sdisp

ersio

nAm

orphophallu

skonjac

Heatedin

awater

bath

Aqueou

sdispersio

n

Giant

squid(D

osidicu

sgigas)

Alaskap

ollock

(T

chalcogram

ma)

ProteinsolubilitypH

texturaland

viscoelasticrheologicalattributes

1[60]

Carrageenan+

NaC

lorK

Clmdash

Heatedin

awater

bath

Hydrocollo

idAlaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorcompressio

ntest

Carrageenan1+

KCl15

[61]

Amorphophallu

skonjac

flour

(AKF

)Am

orphophallu

skonjac

Heatedin

awater

bath

Flou

rGiant

squid(D

gigas)

Water

retentionabilitycolor

texturalandsensoryattributes

10

[62]

NaC

l+high

hydrostatic

pressure

(HHP)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Proxim

atea

nalysis

FTIR

SEM

colormechanicalrheologicaland

sensoryattributes

HHP

300MPa

+NaC

l03

[63]

Sodium

chlorid

esugarspolyols

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Larim

ichthys

polya

ctis)

Water

activ

ityV

BNcolor

moistu

recontent

Sodium

chlorid

e4

Glucose10

Glycerin

10

[64]

Starchglycine

sodium

lactate

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Lpolya

ctis)

Water

activ

ityV

BNcolorm

oistu

recontent

Sodium

lactate75

[65]

Glycerol

mdashSteamed

Liqu

idMackerel(Scom

berjaponicu

s)andBrazilian

sand

perch

(Pseud

opercis

semifa

sciata)

Water

activ

itytexturaland

sensory

attributes

20

[66]

Naa

ndCa

salts

ofpo

lyuron

ides

and

carboxym

ethyl

cellu

lose

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gel-

streng

theningeffects

2ndash6

[67]

L-ascorbicacid

(AsA

)and

dehydro-L-

ascorbicacid

(DAs

A)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthanalysis

DAsA

10120583

gg

[68]

Sodium

-L-

ascorbate

(SA)

mdash

Steamed

inNojax

cellu

lose

casin

g

Powder

Alaskap

ollock

(T

chalcogram

ma)

pHtexturaland

sensoryattributes

02

[69]

120596-3

fatty

acids

from

algae

Not

mentio

ned

Heatedin

awater

bath

Oil

Cod

(Gadus

morhu

a)TB

ARS

fattyacid

contentcolor

500m

g85

g[70]

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)

Microscop

icob

servation

viscosity

gel-formingability

10

[71]

Journal of Food Quality 9Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)Th

readfin

bream

(Nem

ipterid

ae)White

croaker(Ge

nyonem

uslin

eatus)

andJapanese

jack

mackerel(Trachu

rus

japonicus)

Proxim

atea

nalysis

color

water-holding

capacityphysic

alattributes

5ndash30

[72]

120596-3

PUFA

s-ric

hoils

Flaxseedalgae

menhaden

krillblend

(flaxseed

algae

krill

811)

Heatedin

awater

bath

Oil

Alaskap

ollock

(T

chalcogram

ma)

Torsiontest

andrheological

attributes

9g10

0g[73]

Ethano

licKiam

woo

dextract

(EKW

E)+

commercialtann

in(C

T)

Hopea

sp

Heatedin

awater

bath

Overdrie

dpo

wder

Strip

edcatfish

(Pangasiu

shypophthalmus)

pHV

BNT

BARS

color

TCA-

solublep

eptid

emoistu

re

proteincontents

texturalattributes

EKWE

008

CT002

ndash004

[74]

Cocon

uthu

skextractw

ithethano

l60(C

HE-E6

0)

80(C

HE-E8

0)

Cocosn

ucifera

Heatedin

awater

bath

Freeze-drie

dpo

wder

Sardine

(Salbella)

Totalpheno

licexpressible

moistu

reT

CA-solub

lepeptideand

proteincontents

colortextual

rheologicalandsensoryattributes

CHE-E6

00125

[75]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Solutio

nMackerel

(Rastre

lligerk

anagurta)

SEMexpressiblemoistu

reprotein

contentcolortexturalandsensory

attributes

OFA

040

OTA

050

OCF

050

OCT

010

[76]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Bigeye

snapper

(Ptayenus)

SEMexpressiblemoistu

reprotein

andfre

eaminoacid

contentcolor

texturalandsensoryattributes

OFA

020

OTA

005

OCF

015

OCT

005

[77]

Eggwhitepo

wder

(EW)whey

protein

concentrate(WPC

)

Gallusgallusd

omesticus

Triticum

aestivum

Heatedin

awater

bath

Powdera

ndconcentrate

Lizardfish

(Stum

bil)mince

andsurim

i

Autolytic

activ

ityT

CA-solub

leoligop

eptid

esprotein

content

texturalattributes

EW4

WPC

4

[26]

Zinc

sulfate

(ZnS

O4)sodium

tripolypho

sphate

(STP

P)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Yello

wstr

ipetrevally

(Sela

roideslep

tolep

is)

Expressib

lemoistu

relipid

phosph

olipidand

proteincontent

Ca-ATP

asea

ctivitycolortextural

attributes

ZnSO460120583

molkg+

STPP

05

[78]

SEMscann

ingelectro

nmicroscop

yFT

IRFou

rier-transfo

rminfrared

spectro

scop

yVBN

volatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stancesT

CAtric

hloroacetic

acid

10 Journal of Food Quality

fish bones [33] Furthermore a study on the rheologicaland textural attributes of Pacific whiting surimi showedthat slow heating and the addition of nanoscaled fish bonessignificantly enhanced gel strength [34]

Fowler and Park reported an enhanced gelling strengthand effectively inhibited proteinase activity in Pacific whitingsurimi gels heated ohmically [35] Fowler and Park laterstudied the effects of salmon plasma from Chinook salmonon proteolytic inhibition of surimi [36] Salmon plasmaeffectively inhibited both serine and cysteine proteases as wellas proteases isolated from Pacific whiting Salmon plasmaconcentrated by ultrafiltration performed slightly better thanfreeze-dried salmon plasma at inhibiting autolysis in salmonmince

Klomklao et al reported inhibitory activity of a par-tially purified trypsin inhibitor (TIYTR) from yellowfintuna (Thunnus albacores) on the gelling characteristics ofbigeye snapper (Priacanthus macracanthus) surimi [37] Theincorporation of TIYTR with a level of 30 g100 g resultedin the enhanced deformation and breaking force of surimigels suggesting that the TIYTR could be employed as anaffordable and alternative proteinase inhibitor to enhance thegel strength of surimi prepared by bigeye snapper

Vate and Benjakul investigated the effects of squid inktyrosinase mixtures of tannic acid and protein on the gellingcharacteristics of sardine surimi [38] The highest deforma-tion and breaking force were obtained when surimi gels wereallowed to react for 90min while being supplemented with1 tannic acid and 500Ug squid ink tyrosinase proteinHowever gels with an added squid ink tyrosinasetannicacid mixture were whiter than the control The surimi gelssupplemented with squid ink tyrosinasetannic acid mixtureshowed the maximum overall acceptance scores suggestingthat it could be used as an additive to increase the surimi gelproperties

23 Plant Source Additives The chicken plasma proteinegg white and beef plasma protein are considered as themost effective protease inhibitors for surimi [17 22 23156] However the use of chicken plasma and beef plasmaprotein has been forbidden because of the occurrence of avianinfluenza and mad cow disease respectively In additionhigher concentrations of beef plasma proteins have also beenassociated with off-flavors while egg white is expensive andhas an unwanted egg-like odor [29 156] Additionally veg-etarians would not want to consume surimi-based productsprepared with additives from animal or even seafood sourcesTherefore alternate food-grade additives are still desired toenhance the gel strength of surimi without affecting thecustomer demandVarious natural additives derived from theplant sources have been briefly described below

231 Legumes Theeffects of vegetable protein contentmois-ture heating and setting conditions on the physical attributesof kamaboko were examined by Yamashita [39] A firm gelwas obtained at 60∘C for kamaboko with soybean proteinand at 80∘C with wheat gluten When the kamaboko gelswere supplemented with 5 vegetable protein the changes injelly strength softness and expressiblewater of the kamaboko

with wheat gluten were somewhat greater than those of thekamaboko with soybean protein According to the results ofChung and Lee the addition of plant proteins including soyprotein isolate lactoalbumin and wheat gluten remarkablylessened the strength of non-animal protein-incorporatedsurimi gels [40] The textural and sensory attributes offiberized surimi gel products were categorized as an increasein overall textural desirability and an increase in gel strengthIn another study egg white and milk protein isolate showedhigher water retention ability than whey protein concentratesoy protein isolate and lactoalbumin [41]

Protein isolates from legume seeds can be used as alter-nate protein additives for the quality improvement of surimigels Legume seed isolates comprise trypsin inhibitors andhave been used as the protease inhibitor in the prepara-tion of surimi and surimi-based products [42 43] Ben-jakul et al reported higher protease inhibitory activities ofinhibitor extracts from soybean and black cowpea seeds[42] A reduced gel-degradation activity (modori) and ahigh thermal stability were reported In another study theyreported inhibitory effects of proteinase inhibitor extractsfrom Bambara groundnuts (Voandzeia subterranea) pigeonpea (Cajanus cajan) and cowpea (Vigna unguiculata) onautolysis and gel-degradation activity (modori) of threadfinbream surimi [43] The whiteness of surimi gels reducedslightly with the addition of proteinase inhibitor Similarresults were obtained by Oujifard and colleagues [44] TheBambara groundnut protein extracts at a level of 025 g100 gshowed improved autolytic inhibition deformation andbreaking force in surimi prepared by threadfin bream (Nbleekeri) [44] However a slight reduction in whiteness wasobserved at increasing levels of Bambara groundnut proteinisolates These studies show that the addition of Bambaragroundnut protein extracts at a suitable level could serve asan alternative food inhibitor to enhance the gelling propertiesof surimi

Plant protein isolates mainly soy protein isolates havebeen used in the surimi industry because of their safety andrational price [45] Luo et al indicated the legumin andvicilin two main legume seed storage proteins as bindersand cogelling agents in surimi gels [45] Protease inhibitorsisolated from legume seeds not only can help to reduce thegel-degradation process in surimi but can also improve thesurimi gel properties by acting as filler or binder Luo etal reported higher breaking force and quality characteristicsof silver carp surimi when supplemented at a ratio of 10soy protein isolate [46] Cardoso et al studied the effects ofdietary fiber and microbial transglutaminase from chicoryand pea on the rheological properties of protein paste fromgilthead sea bream hake meagre and seabass [47] It wasfound that a high degree of protein denaturation boosted gelhardness while a low degree of protein denaturation createdgels with high deformability It shows that the addition ofmicrobial transglutaminase could serve as a possible additivefor gels of those species having lesser protein unfoldingability

Kudre et al studied the effects of black bean (Phaseolusvulgaris) and mung bean (Phaseolus aureus) protein isolateson gelling properties and proteolysis of sardines (Sardinella

Journal of Food Quality 11

albella) surimi [48] An increase in deformation breakingforce and water-holding capacity as well as a lower levelof degradation was observed while the whiteness of kam-aboko gels reduced slightly Therefore mung bean or blackbean protein isolates could be effectively used to retardthe proteolysis in sardine surimi leading to improved gelstrength Klomklao and Benjakul studied the effects of thepartially purified trypsin inhibitor from adzuki bean on thegelling properties and proteolysis of threadfin bream (Nbleekeri) surimi [49] An increase in autolysis and inhibitoryactivity against sarcoplasmic proteinases aswell as an increasein deformation and breaking force of kamaboko gel wasobserved at increasing levels of trypsin inhibitor while gelwhiteness decreased slightly

232 Starch Starch is widely used to make fish-paste prod-ucts as it enhances elasticity and increases the weight ofthe products In attempts to control thermal stability stick-iness andor wetness under different serving and storageconditions the functional characteristics of surimi seafoodproducts have been widely studied using modified starchesStarch is the second most abundantly used ingredient in themanufacturing of fish-paste products because of its higherwater-holding ability and capacity to replace fish proteinspartially while preserving the desired gel features at a reducedcost [69 157ndash161]

Kim et al reported a positive correlation between theamount of added starch and the quality of the food products[162] Konoo et al studied the effects of adding starch andamylose to amylopectin contents of starch on the gela-tion properties of frozen walleye pollack surimi [50] Thebreaking strength of gel was not affected by the changein amylose amylopectin ratio However it increased as thecontent of amylose increased in pregelatinized starch [51]A lower packing effect was observed at 90∘C which hypoth-esized that the gelatinization of starch in fish meat can beprevented at this temperature A strong correlation betweenthe amylose to amylopectin contents and the textural andrheological properties of starch-containing surimi gels wasalso reported by Lanier et al [134]

The addition of normal and modified potato or sweetpotato starch resulted in reductions in the characteristicstorage modulus of surimi sols during heating [52] Surimigels supplemented with potato starch showed the highestfirmness and cohesiveness Yoo reported the best texturalproperties of the sand lance (Ammodytes personatus) fish-paste products at a level of 8 potato starch [53] Thesestudies show that potato or sweet potato starch can also beused as a potent food additive for the production of surimi

233 RiceRice Flour Fish meat and wheat flour are themajor ingredients used for the production of surimi-basedproducts Rice flour however can be an important ingredientto enhance the rheological properties of surimi-based prod-ucts Several attempts have been made to evaluate the poten-tial of rice flour as an alternate of wheat flour in the prepara-tion of surimi products [41] The effect of rice flour additionmethods and milling types on the sensory and rheologicalattributes of surimi products were studied by Cho et al [54]

Roll-mil rice at a concentration of 10ndash15 displayed highergel strength and sensory properties which show that roll-millrice had strong potential for replacing wheat flourThe surimiproducts containing rice flour showed similar rheological andsensory characteristics to those of a finest commercial surimiproduct Hence rice flour might be an effective alternative towheat flour for high-quality surimi products

To replace wheat flour Kwon and Lee examined thequality characteristics of fried fish cakes containing rice flour[55] The total content of corn starch and rice flour was2883 of the total content of fish cake doughThere were nonoteworthy differences in the pHmoisture level appearancecolor flavor taste and overall acceptance as compared tothe control group The addition of 50 rice flour to surimi-based products could be an effective way to increase thecontent of rice flour without decreasing texture acceptabilityYoon et al optimized the content of water and rice flourin surimi-based products [56] The surimi-based productsmanufactured under optimal environment were comparablein gel strength to the commercial products However highersensory evaluation scores were observed compared to thoseof the commercial products These studies advocate that therice flour not only can be employed as an alternative to wheatflour but can also be used to enhance the quality of surimiand surimi-based products

234 Potato Powder The food additives extracted frompotato and potato protease inhibitors used in the preparationof fish-paste products are discussed in Sections 21 232 and244

24 Cryoprotectants and Humectants To inhibit denatura-tion and to lessen the damage of gel quality during coldstorage cryoprotectants are usually added to surimi productsPolyunsaturated fatty acids protein additives polyols sugarsamino acids salts and plant extracts are frequently usedas cryoprotectants and humectants to avoid fluctuationsin myofibrillar proteins promoted by freezing storage orthawing [163] Mechanical properties of surimi gels can beimproved by the addition of numerous hydrocolloids such askonjac carrageenan locust bean xanthan gum and differentmicrobial transglutaminases during the preparation of surimiproducts [57 164ndash166] In contrast the addition of alginateshas been reported to weaken surimi gels [69]

241 Saccharides Xanthan is a nongelling polysaccharideproduced by the aerobic fermentation of Xanthomonascampestris [167] The property of xanthan to form highlyviscous and stable solution at low levels makes it acceptablein the food industry [168] Xanthan displays quite remarkablesynergistic interactions with other nongelling polysaccha-rides of the galactomannan family leading to increases in gelformation and viscosity [168 169] The three commerciallyavailable galactomannans are tara gum locust bean gum andguar gum

The impact of low methoxyl pectin on the mechanicalproperties of silver carp surimi gels was studied by Barreraet al [58] An increase in hardness shear stress and water-holding capacity of the surimi gel was observed while no

12 Journal of Food Quality

significant improvement in the mechanical properties wasobserved as compared to the control Benjakul et al reportedthe effects of prawn-shell chitosan on surimi prepared bybarred garfish (Hemiramphus far) [59] Prawn-shell chitosanat a level of 1 of the surimi gel showed an increase in gel-enhancing effect on the heat-induced gelation of myofib-rillar proteins The addition of microbial transglutaminasegenerally increases the deformation and breaking force ofsurimi gel However this effect was significantly retardedin the presence of prawn-shell chitosan resulting in lowermagnitudes of deformation and breaking force

The viscoelastic properties and the thermal stability oflow-grade squid (Dosidicus gigas) surimi were investigated byIglesias-Otero et al [60] The konjac glucomannan aqueousdispersion at a level of 1 expressed the best rheologicalproperties suggesting that the konjac glucomannan aqueousdispersion may be used to enhance the quality characteristicsof low-grade squid surimi gel Ramırez et al evaluated theeffect of protein-hydrochlorides on the gel-forming ability ofmyofibrillar proteins [142] The xanthanlocust bean gum ata ratio of 025075 showed a positive improvement in themechanical attributes of surimi gels Eom et al investigatedthe impact of carrageenan on the gelation property of salt-based Alaska pollock surimi [61] The addition of 15KCl rather than 2 NaCl significantly enhanced the gellingproperty of 120581-carrageenan-induced surimi gel and showedincreased gel strength breaking force and whiteness values

242 Salts Salts help in protein-protein interaction and theaddition of salt is critical during the processing of fish-pasteproducts However the high levels of sodium in foods andconsequently human consumption of sodium have becomea global issue The prime harmful effects of excess sodiumintake are hypertension and increased blood pressure Sub-sequently these conditions lead to cardiovascular diseasesincluding instances of stroke heart attack and relateddiseases as well as gastric cancer and osteoporosis [170ndash172] Therefore to reduce sodium intake levels in fish-pasteproducts Hwang et al prepared the sodium-reduced friedfish cakes containing potassium as a substitute for sodium [1]The quality characteristics of 30 sodium-reduced fried fishcakes were not notably different from those of full-sodiumfried fish cakes however the addition of potassium changedthe color and reduced consumer acceptance To increase theconsumer preference for sodium-reduced fried fish cakes theuse of different food additives might be advantageous

The weak gel-forming ability and the strong fishy smellof the giant squid (D gigas) make it undesirable for themanufacturing of surimi-based products To overcome theseproblems Choi and Kim used Amorphophallus konjac flourto enhance the quality characteristics of giant-squid surimiproducts [62]The increasing levels ofA konjac flour showedincreases in gel texture and water retention ability while areduction in color and taste was observed as compared tothe commercial surimi products The incorporation of theseasoning ingredients such as sweeteners might be helpfulin removing the fishy smell of D gigas ultimately improvingthe gel properties of giant-squid surimi Cando et al reportedthat the sensory and mechanical properties of surimi gels

with reduced-NaCl contents can be improved by the appli-cation of 300Mpa high hydrostatic pressures [63] The gelsmade with lower-NaCl contents revealed stronger and stablenetworks as showed by the ones with higher-NaCl contents

243 Water Activity It has been reported that humectantshad the greatest effect on lowering water activity (119886

119908) with

the efficiency of the reduction in 119886119908value decreasing in the

order of NaCl sodium lactate glycerin propylene glycoland sorbitol when each of them was combined with otherhumectants [173] Kim and Park reported the impact ofhumectants such as sodium chloride sugars and polyols tolower the water activity (119886

119908) of various model kamaboko gels

[64]The effect of sodium chloride on lowering water activity(119886119908) was the highest among all of the examined treatments

while glucose caused browning reaction on the surface ofkamaboko In another study they examined the effect ofstarch glycine and sodium lactate in lowering the wateractivity (119886

119908) of model kamaboko gels [65] Sanchez Pascua et

al reported that glycerol (15ndash50) was effective in reducingthe water activity (119886

119908) in Brazilian sand perch (Pseudopercis

semifasciata) and mackerel (Scomber japonicus marplatensis)[66] Among the tested humectants the efficiency of thereduction in water activity (119886

119908) was observed decreasing in

the order of sodium lactate glycine and starch

244 Polyuronides The effect of sodium and calcium salts ofcarboxymethyl and polyuronides cellulose on the strength-ening of kamaboko gels was investigated by Niwa et al [67]It was reported that the calcium salts of pectinic acid pecticacid alginic acid and carboxymethyl cellulose enhancedthe breaking force of Alaska pollock surimi whereas theirsodium salts except Na-pectinate failed to increase the break-ing force The increase in the breaking force induced by cal-cium carboxymethyl cellulose vanished upon increasing thedegree of substitution of hydroxyl groups to carboxymethylgroups Furthermore fine cellulose particles enhanced thebreaking strain and breaking force and reduced the amount ofexpressible water but were unsuccessful in the case of coarserparticlesThe addition of potato starch can increase the effec-tiveness even in the presence of coarse particles of cellulose

245 Ascorbic Acid The addition of dehydro-L-ascorbicacid and L-ascorbic acid to Alaska pollock surimi increasedthe gel strength [68] It was suggested that the positiveeffect of L-ascorbic acid on gel formation might be due tothe oxidation of sulfhydryl groups in fish proteins Lee etal studied the effects of sodium-L-ascorbate on the gel-forming abilities of surimi prepared by Alaska pollock [69]Sodium-L-ascorbate remarkably enhanced the gel firmnesscohesiveness strength and sensory properties of the fiber-ized products at a level of 02 It directly influenced thesurimi quality regardless of vacuum treatment indicatingthat airborne oxygen was not important Freeze-syneresisstimulated by ascorbate during frozen storage was lessenedby the application of hydroxypropylated-modified starch

246 Unsaturated Fatty Acids The addition of nutritionallybeneficial 120596-3 fatty acids during surimi preparation could

Journal of Food Quality 13

enhance the gel strength and stability [70] For the effectiveuse of highly unsaturated fatty acids such as docosahexaenoicacid (DHA) and eicosapentaenoic acid (EPA) in surimi-basedproducts Okazaki et al studied the gel-forming properties offrozen walleye pollock surimi containing DHA and EPA [71]They reported that to achieve a good quality product thevigorous agitation of surimi with fish oil is essential to allowthe heat-induced gelation of its emulsified product throughthe formation of fine oil droplets

Fukushima et al investigated changes in the physi-cal properties of heat-treated surimi gels prepared fromthreadfin breamwalleye pollock Japanese jackmackerel andwhite croaker [72] The breaking strain breaking strengthand water-holding capacity of the heat-treated gels becamegreater as the amount of fish oil increased Furthermoresurimi seafood was nutritionally enhanced with 120596-3 polyun-saturated fatty acid- (PUFA-) rich oils isolated from natu-ral sources such as algae flaxseed menhaden blend andkrill [73] The Alaska pollock surimi supplemented with120596-3 PUFA-rich oils showed improved protein fundamentaltextural properties heat-induced gelation and endothermaltransitions These studies show that the interaction of unsat-urated fatty acids and surimi proteins could contribute to theimprovement in gel properties without altering the texturalattributes

247 Plant Ethanol Extracts The effect of commercial tan-nin and ethanolic Kiam wood extract on the gelling char-acteristics of ice stored mackerel (Rastrelliger kanagurta)surimi was investigated by Balange et al [74] During12 d of iced storage pH TBARS TCA-soluble peptide andtrimethylamine (TMA) contents as well as total volatilebase (TVB) of mackerel mince increased while gel-formingability myosin heavy chain band intensity and whitenessdecreased consistently Deterioration lipid oxidation andprotein degradation proceeded as storage time increasedAn increase in deformation and breaking force of surimigel was observed with the addition of 030 commercialtannin or 015 ethanolic Kiam wood extract during the first6 d of storage Therefore commercial tannin and ethanolicKiam wood extract had not shown a gel-enhancing effecton mackerel surimi Furthermore Buamard and Benjakulinvestigated the effects of coconut husk ethanolic isolateson the gel-forming ability of sardine (S albella) surimi [75]Breaking force increasedwith the increasing levels of coconuthusk ethanolic isolates while a decrease in whiteness and nodetrimental effect on the sensory attributes of surimi gel wasobserved It was concluded that the addition of coconut huskextracts at a suitable concentration could enhance the gelstrength of sardine surimi with increased acceptability

25 Compound Additives The effect of different oxidizedphenolic compounds such as tannic acid OTA ferulic acidOFA caffeic acid OCF and catechin OCT on the gellingattributes of mackerel (R kanagurta) surimi was studied byBalange and Benjakul [76] Gels supplemented with 050OTA 040 OFA 010 OCT or 050 OCF showedincreases in deformation and breaking forces while a decreasein the expressible moisture content and myosin heavy chain

band intensity was observed In another study they inves-tigated the effects of oxidized phenolic compounds on thegel-forming abilities of bigeye snapper (P tayenus) surimi[77] An increase in breaking force and deformation witha decrease in expressible moisture contents was observedGels supplemented with the oxidized phenolic compoundshad a finer matrix with smaller strandsThe physicochemicalcharacteristics of natural actomyosin advocate that oxidizedphenolics could trigger the induction of disulfide bondformation or the conformational changes and cross-linkingthrough amino groups Therefore the addition of oxidizedphenolic compounds at an optimum concentration couldenhance the strength of surimi gel

Yongsawatdigul and Piyadhammaviboon reported aninhibition in autolysis of surimi and mince preparedby lizardfish (S tumbil) caused by p-tosyl-L-phenylalanylchloromethyl ketone and phenylmethanesulfonyl fluorideindicating the involvement of myofibrillar-associated serineproteinase Tropomyosin and myosin heavy chain proteinswere mainly hydrolyzed resulting in poor textural prop-erties [26] Arfat and Benjakul investigated the effect ofzinc chloride (ZnCl

2) and zinc sulfate (ZnSO

4) on the gel-

forming abilities of surimi produced by yellow stripe trevally(Selaroides leptolepis) [78] The kamaboko gels with ZnSO

4

added up to levels of 60120583molkg showed increased deforma-tion whiteness and breaking force as well as highly denserand interconnected gels Therefore ZnSO

4at a suitable

concentration could enhance gel strength and whiteness ofdark-fleshed fish surimi

3 Improvement in Quality andFunctionality of Fish-Paste Products

Various food additives from seafood (eg fish invertebratesand seaweed) plants (eg vegetables fruits and herbalmedicines) mushrooms animal sources and functionalmaterials used to improve the quality and functionality offish-paste products are listed in (Table 2) and describedbelow

31 Seafood Additives It has been reported that various typesof seafood namely fish including dried anchovy (Engraulisjaponicus) powder [79 80] pufferfish (Lagocephalus lunaris)powder [88] and skate (Raja kenojei) powder [81 82] andinvertebrates including warty sea squirt (Styela clava) groundflesh [83] its freeze-dried tunic powder [84] omandungi(Styela plicata) ground flesh [85] shrimp (Acetes japonicus)powder [86] and seaweed such as green laver (Ulva spp) [87]have been used to enhance the quality and functionality offish-paste

The boiled and dried Japanese anchovy (E japonicus)is a popular fisheries product in Korea and Japan As theflesh can be eaten together with bone boiled and driedanchovy products are regarded as good sources of calcium[174] Bae and Lee evaluated the properties of fried fish-paste with added anchovy (E japonicus) powder containinga high amount of calcium [79]The fish-paste containing 10anchovy powder displayed the highest values of adhesivenesshardness and strength In the overall acceptance of sensory

14 Journal of Food QualityTa

ble2Naturalfood

additiv

esused

toim

provethe

functio

nalpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Seafoo

dadditiv

es

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

1-2

[79]

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

5[80]

Skate

Rajakenojei

Fried

Hot

wind-dried

skin

and

cartilage

(64)p

owder

Seab

ream

Moistu

recontentcolortextural

andsensoryattributes

3[81]

Skate

Rajakenojei

Steamed

Ferm

ented

flesh

Nemipterusv

irgatus

Aminoacidand

moistu

recontentcolortexturaland

sensoryattributes

20

[82]

Wartyseas

quirt

Styelacla

vaFried

Groun

dflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

5[83]

Wartyseas

quirt

Styelacla

vaFried

Freeze-drie

dtunicp

owder

Frozen

Itoyori

Colortexturaland

sensory

attributes

1[84]

Pleatedseas

quirt

Styelaplica

taFried

Grin

dedflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

15

[85]

Shrim

pAc

etesjaponicus

Fried

Powder

Frozen

seab

ream

surim

iMoistu

recontentcolortextural

andsensoryattributes

5[86]

Green

laver

Ulva

spp

Fried

Powder

Frozen

seab

ream

surim

iColorsensory

attributes

5[87]

Pufferfish

Lagocephalus

luna

risFried

Powder

Nemipterusspp

Moistu

recrude

protein

lipid

colortexturalandsensory

attributes

5[88]

Maesaengi

Capsosiphon

fulve

scens

Fried

Freeze-drie

dpo

wder

Frozen

seab

ream

surim

iColortexturaland

sensory

attributes

5[89]

Redsnow

crab

Chionoecetes

japonicus

Fried

Leg-meat

powder

Frozen

Alaskap

ollock

(Tchalco

gram

ma)

Physiochem

icalandsensory

attributes

6[90]

Plantsou

rcea

dditives

Mulberryleaf

Morus

alba

Fried

Powder

Seab

ream

Colortexturesensory

attributes

05

[91]

Onion

Alliu

mcepa

Fried

Ethano

lextract

Cutla

ssfishpaste

Moistu

recontentTB

CVBN

colorsensoryattributes

3[70]

Lotusleaf

Nelumbo

nucifera

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

05

[92]

Beetroot

andSpinach

Beta

vulga

risand

Spinaciaoleracea

Microwave

inkamaboko

shape

mold

Freshbeet

rootspinach

dish

Not

mentio

ned

Moistu

retexture

analysis

Beetroot10

Spinach15

[93]

Citrus

fruits

Citru

slim

onC

junosC

unshiu

Fortun

ellajaponica

varmargarita

Steamed

Groun

dflesh

pulpwith

out

seeds

Min

Daegu

flesh

Colortexturaland

sensory

attributes

Cumqu

at[94]

Journal of Food Quality 15

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Oatbran

+SiO2

Avenasativa

Boiled

Powder

Frozen

Alaskap

ollock

surim

iColortexturaland

physiochem

icalattributes

6gOatbran10

0gSiO2

[95]

Yam

Dioscorea

japonica

Fried

Powder

Pollo

cksqu

idshrim

pFo

ldingtest

colortexturaland

sensoryattributes

2[96]

WolfberryC

hinese

Goji

Fructuslycii

Fried

Powder

Seab

ream

Texturalandsensoryattributes

3[97]

Redginseng

Pana

xginsengCA

Meyer

Fried

Powder

Not

describ

edColorlipid

oxidation

sensory

attributes

1[98]

Korean

angelicar

oot

Angelicae

gigantis

Radix

Fried

Powder

Seab

ream

Texturalandsensoryattributes

05

[99]

Turm

eric

Curcum

alongaL

Fried

Powder

Pollo

cksqu

idshrim

pColorrheologicalandsensory

attributes

3[100]

Wasabi

Wasabiajaponica

Fried

Freeze-drie

dpo

wder

Silver

pomfre

t(Pam

pusa

rgenteus)

ColorT

BCviablec

ellcou

nt

texturalandsensoryattributes

18

[101]

Wolfip

oriaextensa

Poria

cocos

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

3[102]

Mushroo

madditiv

es

Butto

nmushroo

mAg

aricu

sbisp

orus

Fried

Chop

ped

fresh

Argyrosomus

argentatus

Texturalandsensoryattributes

10

[103]

Enok

imushroo

mFlam

mulina

velutip

esFried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

5[104]

Shiitakem

ushroo

mLentinus

edodes

Fried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

10

[105]

King

oyste

rmushroo

mPleurotuseryngii

Fried

Paste

Silver

whitecroaker(Penn

ahiaargentata)

Texturalandsensoryattributes

10

[106]

King

oyste

rmushroo

mPleurotuseryngii

Steamed

Paste

Cuttlefish

(Sepiaesculen

ta)

Texturalphysio

chem

ical

sensoryattributes

40

[107]

Animalsource

additiv

es

Poultrychicken

Gallusgallus

domesticus

Fried

Breastmeat

batte

r

Itoyori

Japanese

threadfin

bream(Ne

mipterus

japonicus)

Chem

icalcompo

sition

color

fatty

acid

compo

sition

TBARS

sensoryattributes

746

or1493

[108]

Functio

nalfoo

dadditiv

es

Long

-chain

cellu

lose

mdashBo

iled

Powdered

cellu

lose

Alaskap

ollock

surim

iTexturalandrheological

attributes

6[109]

Dietary

fiber

from

ascidian

tunic

Halocynthiaroretzi

Boiled

Refin

eddietaryfib

erAlaskap

ollock

surim

iColortexturalph

ysiological

andsensoryattributes

5[110]

16 Journal of Food Quality

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Fibera

nd120596-3

oil

mdashHeatedin

awater

bath

Powdered

fiber120596

-3oil

Alaskap

ollock

surim

iTexturalandrheological

attributes

Fiber6ndash

10g

and120596-3100

g[111]

Flaxseed

orsalm

onoil

Not

describ

edCoo

kedin

awater

bath

Oil

Frozen

Alaskap

ollock

surim

i(Tchalco

gram

ma)

TBARS

colortexturaland

sensoryattributes

2g10

0gfranks

[112]

Soybeanoil

Glycinem

axHeatedin

awater

bath

Oil

Frozen

silverc

arpsurim

iColortexturalattributes

Soybeanoilgt3

[113]

Calcium

powdero

fcuttlefish

bone

treated

with

aceticacid

Sepiaesculen

taHeatin

gin

awater

bath

Calcium

powder

Alaskap

ollock

surim

iMoistu

recontentcolortextural

andsensoryattributes

009

[114]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Alaskap

ollock

meatp

aste

Colortexturaland

sensory

attributes

017

[115]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Sand

lance

(Hypoptychus

dybowskii)

Acid

andperoxide

valueVBN

sensoryattributes

02

[116]

Cheong

gukjang

Ferm

entedGlycine

max

byBa

cillussp

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

2[117]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 17

evaluation small and large size fish-paste with 1 and 2respectively of added anchovy powder was preferred Thesimilar increasing trend of calcium intensity was observedby Bae et al [80] However the fried fish-paste productscontaining 20 anchovy powder displayed the highest valuesof adhesiveness hardness and strength Regarding overallacceptance in the sensory evaluation the fried fish-pastecontaining 5 anchovy was preferred The optimal amountsof added anchovy in the results from Bae and Lee and Bae etal were different which might have been due to the differentdrying methods and sizes of the anchovies used in each study[79 80] Despite the differences in the two studies the resultssuggest that anchovy powder could be applied to fried fish-paste products to achieve high calcium contents

Skate contains many essential fatty acids includinglinolenic acid linoleic acid arachidonic acid DHA andEPA [175] Skate skin contains high percentages of collagenprotein and calcium [176] while its cartilage is rich inchondroitin sulfate [177] To improve quality and nutrientlevels Cho and Kim prepared fried fish-paste with skate (Rkenojei) powder (hot wind-dried skin and cartilage powder[6 4]) [81] According to Park et al preference testingusing steamed fish-paste product with different levels ofadded 14-day-fermented flesh of skate showed significantincreases in brownness smoothness and skate flavor scores[82] The amino acid contents of fish cake samples with20 skate added had the highest overall preference scoresConsequently the addition of 20 skate powder was optimalfor the steamed fish cake to improve its quality characteristicswith higher protein contents

Warty sea squirt (S clava) aquaculture in the Masanarea of Korearsquos south coast contains abundant unsaturatedfatty acids and essential amino acids in its flesh [178] andglycosaminoglycan in its tunic [179] Warty sea squirt has aunique taste and distinct antioxidant and anticancer activities[180] Fried fish-paste supplemented with 20 warty seasquirt (Korean name miduduk) displayed improved qualityand functionality [83] Choi et al reported a fried fish-paste containing freeze-dried byproduct of warty sea squirt(S clava tunic) [84] The hardness and strength of fish-paste increased with increasing amounts of tunic powderFor overall acceptance in sensory evaluation a fish-pastesupplemented with 1 S clava tunic obtained a relativelyhigher score The results suggested that S clava flesh andtunic could be used for fish-paste products to improve theirquality and functionality Park et al reported improvementin the functional properties of fish-paste by adding S plicata(Korean name omandungi) [85] Fried fish-paste containing20 S plicata indicated the highest values of adhesivenesshardness and strength For overall acceptance in sensoryevaluation a fish-paste containing 15 S plicata obtained thehighest score

Seo and Cho reported the preparation of fish-paste withadded shrimp (A japonicus) powder [86] The hardnessspringiness and cohesiveness increased with the increasingconcentration of shrimp powder However the brittlenessand gumminess reduced In the sensory evaluation the fish-paste prepared with 5 shrimp powder was most preferredCho and Kim reported the preparation of fish-paste with

added green laver (Ulva spp) powder [87] The hardnessspringiness and cohesiveness increased with the increasingconcentration of green laver powder However the brittlenessand gumminess decreased upon the addition of green laverpowder In the sensory evaluation a fish-paste prepared with5 green laver powder was preferred over other fish-pastesThese results suggest that green laver powder could be appliedto fish-paste to improve its quality and functionality

Pufferfish containing taurine hydroxyproline lysine andglycine impart a characteristic taste to food [181] To improvethe taste of fish-paste products Park prepared a fish-pasteby adding green rough-backed pufferfish (L lunaris) pow-der [88] The hardness strength gumminess springinessand chewiness of the fish-paste increased depending onpufferfish powder contentThe preparation of fish-paste withadded Capsosiphon fulvescens powder was reported by Park[89] The hardness springiness strength and cohesivenessincreased with the increasing concentrations of C fulvescenspowder However the brittleness and gumminess reducedwith the addition of C fulvescens powder In the sensoryevaluation overall the fish-pastes prepared with 5 Cfulvescens powderwere preferred over other fish-pastesThusthe results show that C fulvescens powder could be used tocreate fish-paste products with high quality and functionality

Kim et al reported the changes in the sensory and physic-ochemical properties of a fish-paste containing red snow crab(Chionoecetes japonicus) leg-meat powder [90] Hardnessgumminess springiness and cohesiveness increased withincreasing levels of red snow crab leg-meat powder Based onthe sensory evaluation it was concluded that the addition ofred snow crab leg-meat powder at a level of 6 could improvethe quality characteristics of fish-paste products

32 Plant Source Additives It has been reported that variousplant sources namely vegetables (eg mulberry beetrootand spinach) fruits (eg citrus) and herbal medicines (egChinese matrimony vine Korean Angelica root) have asignificant effect in improving the quality and functionalityof fish-paste products

Mulberry (Morus alba) leaf has been used traditionallyto treat a disease symptomized by thirst and stroke [182]Ever since mulberry leaf was included as a food material inthe Food Codex in 1988 by the Ministry of Food and DrugSafety (MFDS Osong Chungju South Korea) Mulberry leafpowder has been used in various processed food productsand health functional foods Shin and Park reported theuse of mulberry leaf powder in the preparation of fish-pasteproducts [91] In a texture meter test the hardness increasedbut the cohesiveness springiness gumminess and brittlenessdecreased with increasing levels of mulberry leaf powder Insensory evaluation the fish-paste with 05 mulberry leafpowder revealed the highest acceptance scores in terms offlavor texture and overall quality

Garden onion (bulb onion Allium cepa) is a perennialplant belonging to Liliaceae and is widely used as a spice andseasoning vegetable in both the East and the West Park etal investigated the quality characteristics of fried fish-pastesupplemented with flavonol-rich ethanol extract of onion[183] In the sensory evaluation as the amount of ethanol

18 Journal of Food Quality

extract of onion increased so did the favorability in termsof flavor and taste Notably 3 ethanol extract of onion hadthe best score in overall acceptance The results indicate thatethanol extract of onion can be used to prepare fried fish-paste products with high quality and functionality

Shin reported the production of fish-paste with addedlotus (Nelumbo nucifera) leaf powder [92] The flavor adhe-siveness and hardness increased with the increasing levels oflotus leaf powder The fish-paste with 05 lotus leaf powderdisplayed the highest acceptance scores in terms of springi-ness pleasant taste appearance texture flavor and overallquality Thorat et al prepared kamaboko containing greenchili coriander ginger garlic spice mixture and groundbeetroot or a spinach dish and then subjected the preparationto microwave cooking [93] Kamaboko prepared with 10beetroot and a 15 spinach dish was found to be superior tothe others

Yang and Cho developed a steamed fish cake with added5 ground citrus fruits with skin [94] The addition of citrusfruits did not disturb the flexibility of surimi The pH ofsurimi samples increased in the following order lemon (Cit-rus limon) citron (Citrus junos) tangerine (Citrus unshiu)kumquat (Fortunella japonica var margarita) and controlThe hardness of surimi was highest for lemon followed bycitron tangerine kumquat and control surimi In the sensoryevaluation surimi containing kumquat demonstrated higherscores in terms of color taste and textural properties Theseresults suggest that surimi could be prepared by adding citrusfruits to improve the quality and functionality

Oat bran is a gluten-free dietary fiber that may decreasethe risk of diabetes and heart diseases The physicochemicalproperties of surimi gels supplemented with oat bran werestudied by Alakhrash et al [95] The oat bran and SiO

2

incorporation (6 g100 g) greatly improved water-holdingcapacity and gel texture while a reduction in whiteness wasobserved Kim and Byun conducted tests on the sensoryand physicochemical characteristics of fish-paste with addedyam (Dioscorea japonica) powder [96] The addition of yampowder increased gumminess strength springiness andcohesiveness In the sensory evaluation the addition of 2yam powder had the best scores in terms of taste color andoverall preference

Fructus lycii is a fruit produced by Lycium barbarumL that has been used for nourishment tonicity and nour-ishment of the blood it has antibacterial anticancer andantioxidant properties [182ndash186] Shin et al prepared friedfish-paste containing dried F lycii powder [97] In the texturalanalysis cohesiveness increased while brittleness and gum-miness decreased with increasing levels of F lycii powderThe 3 F lycii powder sample had the highest acceptancescores in terms of appearance texture taste flavor andoverall acceptability

Red ginseng-based fried fish-pastes containing differentsizes and amounts of red ginseng powder were preparedand their biological properties including lipid oxidation toimprove fish-paste quality were investigated [98] The fish-paste products containing red ginseng powder showed asignificant increase in hardness and chewiness Furthermorean inhibitory effect on lipid oxidation and reduced number

of total microbes during storage were observedThese resultssuggest that high-quality fish-pastes could be achieved withthe addition of 1 red ginseng powder which effectivelyimproved both sensory evaluation and physicochemicalproperties

Angelicae Gigantis Radix (the dried root ofAngelica gigasNikai) more popularly known as Korean Angelica is one ofthe widely used herbal medications [187] It has been usedin Korean medicine as an important medication for anemiaand blood circulatory disorders It has also been used formenstrual pains and postmenopausal syndromes Shin et alreported the development of fish-paste with A gigas powder[99] In a texture test hardness chewiness and brittlenessincreasedwith increasing concentrations of AngelicaeGigan-tis powderHowever cohesiveness and springiness decreasedIn the sensory evaluation the fish-paste with 05 AngelicaeGigantis powder showed the highest acceptance scores forappearance flavor taste texture and overall quality

Turmeric (Curcuma longa) has been used in Ayurvedicmedicine from ancient times as a treatment for inflammatoryconditions It has been reportedly used for its various bio-logical activities including antibacterial antiviral antifungalantioxidative and antiatherogenic effects [188] Turmeric hasbeen grown as a special crop in the central and southern areasaround Jindo in South Korea [189] Choi et al investigatedthe sensory and rheological properties of fish-paste preparedwith turmeric powder [84] In terms of textural attributesthe addition of C longa powder decreased springiness andimproved strength In the sensory evaluation the addition of3 C longa powder was associated with the best scores fortaste and overall preference

Wasabi (Wasabia japonica) has various beneficialhealth properties including antioxidative antimicrobialand antimutagenic activities [190 191] Jang et al reporteda high-quality fried fish-paste product made with silverpomfret (Pampus argenteus) which is one of the savorysoft and delicious types of fish prepared by adding wasabipowder [101] Notably hardness gumminess and chewinessincreased significantly with the addition of wasabi powderIn the sensory evaluation 18 wasabi powder showed thebest score in overall acceptability These results show thatwasabi could be used as a food additive or preservative infish-paste products

White Poria cocos wolf is the inner white part of P cocosa parasite found on Pinus densiflora It is used to treat edemachronic gastritis gastric atony nephrosis acute gastroentericcatarrh emesis dizziness and vomiting [192 193] Shin et alprepared a fried fish cake with added white P cocos powderand studied the textural and sensory characteristics [102]In texture tests brittleness was observed to increase whilespringiness decreased with increasing concentrations of Pcocos powder The fish-paste product containing 3 whitePoria cocos powder showed the highest acceptance scores forflavor appearance texture taste and overall quality

Milk-vetch root is one of the most produced herbalmedicines in Korea It is a peeled and dried root of the herba-ceous perennial herb known as Astragalus membranaceuswhich belongs to the Fabaceae family [194] It has been

Journal of Food Quality 19

reported that milk-vetch root exerts diuretic tonic anti-hypertensive hypoglycemic immune-enhancing antitumorand antiviral effects [195] Kim investigated the sensoryand physicochemical properties of fish-paste prepared withmilk-vetch root powder [196] The strength cohesivenessbrittleness and gumminess of the fish-paste increased whileits springiness decreased with an increasing amount of milk-vetch root powder In the sensory evaluation the addition of10 milk-vetch root powder indicated best scores for tastetexture color and overall preference

33 Mushroom Additives Mushroom is a nutritional andfunctional food as well as a vital source of physiologicallybeneficial medicines Mushrooms have been used as tradi-tional medicines in Korea Japan China and other Asiancountries for curing various diseases including lymphaticdisease gastroenteric disorder oral ulcer and various can-cers [197] It has been reported that edible mushrooms inKorea number approximately 350 species [198] Several ediblemushrooms that are highly preferred have been added to fish-paste to enhance their quality and functionality

Ha et al prepared a fried fish-paste product with addedAgaricus bisporus which is a product described as having aracy flavor and taste [103]The elasticity hardness brittlenessand gumminess of fish-paste with the added mushroomincreased however no significant difference in strengthwas observed Regarding overall acceptance in a sensoryevaluation a fish-paste supplemented with 10 A bisporusmushroom showed the highest scores

Enoki mushroom (Flammulina velutipes) is well knownfor its anticarcinogenic and blood pressure-reducing prop-erties To utilize its functional properties enoki mushroomwas added to fried fish cake [104] The sample containing15 mushroom received the highest values for strengthgumminess and brittleness In the sensory evaluation thefish cakes with 5 mushroom obtained favorable scores foroverall acceptance

Shiitake mushroom (Lentinus edodes) is known for itshigh level of 120573-glucans Son et al investigated the effectsof shiitake mushroom on the textural properties of friedfish cake [105] The fish cake containing shiitake mushroomreceived the highest values for strength hardness gummi-ness and brittleness In the sensory evaluation the fish cakeswith 10 shiitake mushroom sample obtained the best scorefor overall acceptance

Kim et al prepared a fried fish cake using cultured kingoyster mushroom (Pleurotus eryngii) and silver white croaker(Pennahia argentata) surimi to enhance its physiologicaleffects [106] In assessing its quality properties fish cake towhich 10 mushroom was added received the highest valuesfor strength hardness gumminess and brittlenessThe effectof king oyster mushroom on the textural and physicochem-ical properties of steamed cuttlefish (Sepia esculenta) fishcake was investigated by Chung et al [107] The fish-pastewith added king oyster mushroom paste revealed significantdecreases in gumminess cohesiveness and hardness whilethe springiness increased with increasing concentrations ofking oystermushroompasteOn the sensory evaluation basisthe cuttlefish-paste supplemented with 30ndash50 king oyster

mushroom showed higher overall acceptability In the studiesby Kim et al and Chung et al the optimal amounts of kingoyster mushroom differed which might have been due tothe different cooking methods and surimi used in each study[106 107]

34 Animal Source Additives Jin et al investigated the effectof chicken meat on the quality characteristics of Itoyori(Japanese threadfin bream Nemipterus japonicus) surimi[108] The physicochemical properties such as fatty acidcomposition shear force and gel characteristics were affectedby substitution with spent laying hen meat batter Howeversensory characteristics were less affected by this substitutionA huge amount of waste in the processing of grass carp isdiscarded To deal with this waste Gao et al studied theprocessing technology used for fish and mushroom pastewith salted fish cubes mushroom soybean and fermentedsoybeans [199]

35 Functional Food Additives Functional food additivesincluding dietary fiber 120596-3-rich oil calcium additives andpropolis have been used in the preparation of fish-pasteproducts to increase their quality and functionality Westernpopulations have an inadequate quantity of health beneficialdietary fiber in their diets Besides fiber most Western pop-ulations also consume an insufficient amount of 120596-3 PUFAswhile their sodiumconsumption greatly surpasses the recom-mended maximum Debusca et al prepared Alaska pollocksurimi fortified with commercial long-chain cellulose as asource of dietary fiber [109] Fiber fortification up to a level of6 improved both texture and color a slight decline in thesevalues was observed at levels of 8 fiber An increase in gelelasticity and thermal gelation of the fish cake was observed

Yook et al prepared a fish-paste by adding dietaryfiber extracted from ascidian (Halocynthia roretzi) tunic toenhance its physiological properties [110] The hardnessgumminess adhesiveness shear force and chewiness of thefish-paste improved with the incorporation of the ascidiandietary fiber The fish-paste with 5 ascidian dietary fiberscored the highest and was generally preferred by sensorypanels Tolasa et al reported that the oxidative stability andthe uniform dispersion of 120596-3 unsaturated fatty acids can beattained in a highly consistent surimi gel system without theuse of antioxidants [200]

Surimi and surimi-based products are famous through-out the world In fact US consumption increased in the1980s while the rate leveled off thereafter The nutrificationof food products with 120596-3 PUFAs increases the health ben-efits of food consequently increasing their market demandPietrowski et al prepared surimi seafood products nutrition-ally enhanced with 120596-3 PUFAs [201] Although the nutrifica-tion of 120596-3 PUFAs indicated an increase in lipid oxidationit was within limits acceptable to consumers The color ofsurimi seafood nutrified with 120596-3 PUFAs generally improvedbut no effect on textural characteristics was observed

Debusca et al reported that the fortification of Alaskapollock surimi with either 120596-3 oil or dietary fiber alone orin combination improved both the textural and rheologicalproperties [111]The120596-3 oil and fiber in combination revealed

20 Journal of Food Quality

greater gelation of surimi and a slight reduction in color prop-erties indicating their interaction with myofibrillar proteinsThus it was suggested that the 120596-3 oils and fiber could beeffectively used as a fortifying agent to prepare high-qualitysurimi products with nutritional benefits Sell et al preparedsurimi franks fortified with salmon oil or flaxseed [112]The textural properties showed differences between franktypes with the flaxseed franks being cohesive less gummysofter and chewy while the sensory evaluation showed nosignificant differences

Chang et al determined the effects of soybean oil andmoisture contents on the physical properties of surimi gels[113] The increasing levels of soybean oil and moisturecontents resulted in an increase in whiteness and reductionin the chewiness hardness and breaking force Setting incombination with soybean oil improved the textural andcolor parameters of surimi gels indicating that soybean oilcould be used to improve the color and textural properties ofsurimi seafood products

Kim et al prepared boiled fish cake using acetic acid-treated cuttlefish bone as a calcium additive agent [114] Theresults of sensory evaluation of texture and whiteness weresimilar to those without this supplementation In the mineralcontent analysis of heat-induced surimi gel calcium contentincreased depending on the increasing concentration ofacetic acid-treated cuttlefish bone powder while phosphoruscontent did not change The optimal concentration of aceticacid-treated cuttlefish bone powder for the preparation ofhigh-quality heat-induced surimi gel was 009

Kim et al prepared Alaska pollock fried fish-pastesupplemented with propolis [115] The addition of propolisenhanced the antispoiling and antioxidative ability as well asgel strength of fried fish-paste In the sensory evaluation theaddition of 017 propolis showed the best score in overallacceptability In another study Kim et al later studied sand-lance (Hypoptychus dybowskii) meat paste prepared withpropolis [116] Similar to the previous report the addition ofpropolis on the fried fish-paste showed higher antioxidativeand antispoiling activities The fried sand-lance meat pasteprepared with 02 added propolis was the most acceptableFurthermore the bitter taste of the sand-lancemeat paste wasreduced by adding 2 sweet amber powder

Cheonggukjang is an ancient Korean food prepared byfermented soybean It contains high levels of dietary fiberoligosaccharides isoflavones saponin lecithin phytic acidand phenolic compounds among others Its many benefi-cial properties have been reported such as thrombolyticanticancer antimicrobial hepatoprotective antioxidant andcholesterol-lowering effects [202] Park et al reported theuse of fish-paste containing cheonggukjang powder [117]Theincreasing concentrations of cheonggukjang resulted in anincreased value of springiness cohesiveness and hardnesshowever a reduction in brittleness and gumminess values offish-paste was observed

4 Shelf-Life Extension of Fish-Paste Products

Fish-paste products may easily spoil due to residualmicrobes that are not removed by sterilization during the

manufacturing process or by contamination in packagingor the distribution process For such reasons even vacuum-packed fried fish-paste products have a shelf-life of fewerthan 10 days during cold storage which is relatively short[121 122] Various efforts have been made to develop long-term storage solutions for fish-paste products via physicaland chemical methods [118ndash122] Although these methodswere found to be very effective for the long-term storageof fish-paste products they require sensitive and complexmanipulation and are costly

The addition of appropriate food additives to fish-pasteproducts as an effective preservation protocol is anotherstrategy Potassium sorbate is a typical synthetic food preser-vative and is commonly used in processed foods includingfish-paste productsThis material is effective in inhibiting thegrowth of variousmicroorganisms as it has a slight sterilizingeffectThe use of this material is permitted to a concentrationof less than 20 gkg in processed fish meat products (FoodCode Ministry of Food and Drug Safety Republic of Korea)According to the results of Walker sorbates and sorbic acidexert a very low level of mammalian toxicity even in chronicstudies as up to 10 of the diet did not show any carcinogenicactivity [203] In addition Thakur and Patel summarizedthe application of sorbates in the shelf-life extension of fishand fish-based products [204] The physical and chemicalmethods along with natural food preservatives for the long-term storage of fish-paste products are listed in Table 3 andbriefly described below

41 Physical and Chemical Methods Various efforts havebeen focused on developing long-term storage solutions forfish-paste products via physical methods including highpressurization [118] microwave pasteurization [93] highhydrostatic pressure treatment [119] and even irradiation[118 121] In addition it has also been reported that treatmentwith chlorine dioxide solution at an appropriate concentra-tion which is harmless to humans could be used to preventspoilage and to extend the shelf-life [122]

High hydrostatic pressure technology has graduallygained popularity in the food industry over the last twodecades [205] In 2013 the worldwide market for highhydrostatic pressure equipment was estimated to be $350million and it is expected to grow Besides high hydrostaticpressure technologies several types of radiation have alsobeen tested including ultraviolet microwaves and gammairradiation treatments Radiation is generally used to controlbiological hazards in the production of fish-paste productsand to prolong the shelf-life of such products [206 207]Gamma radiation exerts potent antimicrobial effects whereasultraviolet rays are effective for the surface but not interiorsterilization of porous dried fish products (eg fish-pasteproducts) However gamma irradiation treatment demandslarge-scale facilities and higher costs [207 208]

Miyao et al reported that growth of the majority of thepathogenic microorganisms present in surimi was inhibitedat a high pressure of between 300 and 400Mpa [118] Severalpressure-resistant strains were isolated from surimi and wereidentified as Moraxella sp Acinetobacter sp Streptococcusfaecalis and Corynebacterium sp It was suggested that

Journal of Food Quality 21

Table3Naturalfood

additiv

esandph

ysicochemicalmetho

dsused

toim

provethe

shelf-life

offish-paste

prod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Physicalandchem

icalmetho

ds

Highhydrostatic

pressure

mdash

High-pressure

treatmento

rheattre

atment

insampletub

ewith

vacuum

packaging

mdashFrozen

Alaskap

ollock

Microbialactiv

ity40

0MPa

[118]

Highhydrostatic

pressure

mdashNot

cooked

mdash

Tuna

fishpaste

Mackerelp

astewith

paprika

mackerelp

astewith

garlic

mackerelp

astealon

eand

salm

onpaste

Microbialactiv

ity200M

Pa[119]

Co-60

Gam

mar

ays

mdashGrilled

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

texturalsensorym

icrobial

physiochem

icalattributes

75kG

y[120]

Co-60

Gam

mar

ays

mdashFried

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

pHtexturalmicrobial

physiochem

icalattributes

3kGy

[121]

Chlorin

edioxide

(ClO2)

mdashSteamed

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

VBN

TBA

RSpHm

icrobial

physicochemicalsensory

attributes

50pp

m[122]

Naturalfood

additiv

esRe

dpepp

erethano

lextract(RP

EE)

andchop

pedfre

shredpepp

er(C

FRP)

Capsicu

mannu

umFried

Ethano

lextract

andchop

ped

fresh

one

Frozen

Alaskap

ollock

TBC

sensoryattributes

RPEE

10

CF

RP5

[123]

Ethano

lextract(EE)

andwater

extract

(WE)

Phellodendron

amurense

Eugenia

caryophyllu

sPinu

srigida

Bletillastr

iata

andPa

eonia

albiflora

mdashmdash

mdashAntim

icrobialattributes

onpu

trefactiveisolatesfrom

fish

meatp

asteprod

ucts

EE2000

ppm

[124]

Eggwhitelysozyme

(EWL)

andor

sodium

hexametapho

sphate

(SHMP)sod

ium

pyroph

osph

ate(SP

P)

Gallusgallus

domesticus

Fried

Powder

Frozen

Alaskap

ollock

Viablecellcoun

tpH

VBN

biochemicalattributes

EWL5

+SP

P05

+SH

MP

01

[125]

Grapefruitseed

extract

Citru

sparadisi

mdashSolutio

nCom

merciallyavailablefi

shmeat

paste

prod

ucts

Proxim

atec

ompo

sition

textural

biochemicalrheologicalsensory

attributes

1000

ppm

[126]

22 Journal of Food Quality

Table3Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Cinn

amon

bark

extract

Cinn

amom

umcassia

Fried

Extracted

solutio

nFrozen

Alaskap

ollock

Antim

icrobialactiv

itySprayeddiluted

extract(11)

[127]

Alginicacid

hydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Relativev

iscositypHcolor

rheologicalattributes

03

[128]

Chito

sanhydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Viablecellcoun

tsrheological

sensoryattributes

03

[129]

Nisin(N

)and

or

sucrosefattyacid

esters(SFE

)mdash

Steamed

Powdera

ndsolutio

nFrozen

Alaskap

ollock

Viablecellcoun

tantim

icrobial

activ

ityN125120583

gg+

SFE10mg

[130]

Piscicolin

KH1

Carnobacteriu

mmaltalomaticu

mSteamed

Solutio

nCod

fish

Inhibitory

assayproteincontent

antim

icrobialactiv

ity50

AUg

[131]

Zein

andsoyprotein

isolate(SPI)fi

lms

containing

greentea

extract(GTE

)

Zeamays

Glycinem

axCa

melliasin

ensis

Fried

Ediblefilm

(GC-WPI)w

ithGTE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

TBARS

colorm

icrobial

physicalattributes

GTE

1

[132]

Gelidium

corneum

(GC)

-Wheyprotein

isolate(G

C-WPI)

blendfilm

containing

grapefruitseed

extract(GSE

)

Gelidium

corneum

Citru

sparadisiBo

staurus

Not

mentio

ned

Ediblefilm

(GC-WPI)w

ithGSE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

Water

vapo

rpermeability

microbiologicalanalysis

sensory

attributes

GSE

01

[133]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 23

damage to the cell membrane and degradation of ribonucleicacids occurred in the high-pressure-treated cells Malickiet al investigated the use of high hydrostatic pressure toprolong the shelf-life of traditionallymanufactured fish-pastestored under refrigeration (4∘C) for 6 weeks [119] Neitherbacteria nor molds or yeasts were detected in the highhydrostatic pressure-treated fish-paste samples at any timepoint analyzed irrespective of the pressurization conditionsIn conclusion these studies revealed the effectiveness of highhydrostatic pressure to prolong the shelf-life of traditionallymanufactured fish-paste stored under refrigerated conditionsfor up to 6 weeks

Kim et al reported a reduction in the total aerobicbacterial counts in the grilled fish-paste stored at 5∘C andirradiated by gamma rays at a level of 25 kGy or more[120] Additionally the treatment of gamma rays at a levelof 75 KGy at 30∘C showed a significant inhibition in aerobicbacterial growth Cho et al investigated the effect of Co-60 gamma irradiation on fried fish-paste and studied thephysicochemical properties of fish-paste products stored atlow temperature (3 plusmn 1∘C) and room temperature (10ndash20∘C)[121] There was no obvious difference between the vacuum-and air-packed groupsThe irradiation of 3 KGy extended theshelf-life of fish-paste up to 2 times at room temperature and3-4 times at low temperature In both studies the irradiationtreatment caused very little textural degradation and no effecton the sensory characteristics of the samples was observed

Shin et al investigated the effects of chlorine dioxide(ClO2) treatment on the physiochemical andmicrobial prop-

erties of fish-paste products [122] After ClO2treatment

fish-paste samples were individually packed and stored at4∘C The pH and VBN values of fish-paste decreased withincreasing ClO

2concentration ClO

2treatment significantly

reduced the populations of total bacteria yeast and moldduring storage In particular treatment with 50 ppm ClO

2

significantly decreased the total bacterial count the mostamong all ClO

2-treated fish-pastes showing that 50 ppm

chlorine dioxide was the optimum concentration to prolongthe shelf-life of fish-paste products

42 Natural FoodAdditives Theuse of natural food preserva-tives rather than chemical and synthetic food preservatives isofworldwide interest It has been reported that several naturalfood additives could extend the shelf-life of cooked fish andfish products Some examples include onion ethanol extract[183] egg white lysozyme [125] grapefruit seed extract [126]chitosan hydrolysate [129] cinnamon bark extract [127] andred pepper extract [123] as well as mixtures of lysozymessodium hexametaphosphate and sodium pyrophosphate

The shelf-life of fried fish-paste products prepared byadding red pepper ethanol extract was estimated by Yoonet al [123] The shelf-life of the fried fish-paste with added10 red pepper ethanol extract and 5 chopped fresh redpepper was 2 to 3 days longer than that of the commercialfish-paste product thus demonstrating the most effectivepreservation effects According to Ahn et al the extractsof Eugenia caryophyllus Pinus rigida Bletilla striata andPaeonia albiflora exerted strong inhibitory effects on thegrowth of microorganisms isolated from putrefied fish-paste

[124] Notably the ethanol extract was more effective thanwater extract in all tested microorganisms The inhibitionlevel of each extract was evident at 2000 ppm ethanol in thefish-paste

Kim et al investigated the inhibitory effects of lysozymesmixtures of lysozymes and other antibacterial substancessuch as sodium pyrophosphate and sodium hexametaphos-phate on bacterial growth in surimi products [125] Thelysozymes inhibited growth in most of the tested isolatesand themixture of antibacterial substances showed increasedeffects compared with those when they were used individ-ually A mixture of 05 sodium hexametaphosphate 05sodium pyrophosphate and 005 lysozyme in imitationcrab and kamaboko showed the highest inhibitory activ-ity

The stabilizing effects of grapefruit seed extract on fish-paste products were investigated by Cho et al [126] Texturalproperties decreased with increasing storage period Thetreatment of fish products with grapefruit seed extract pro-longed the deterioration of fish-paste product proteins duringstorage up to 4-5 daysThe chemical sensory and rheologicalevaluation revealed that the grapefruit seed extract could beused as an effective additive to extend the shelf-life of fish-paste products

The predominant bacterium in most of the isolatedmicroorganisms from packed and unpacked spoiled fish-paste products is Bacillus sp [127] Notably yeast andmolds are not reported in the vacuum-packed products Ahydrolysate of alginic acid has antimicrobial activity but ithas not been used at industrial scale The alginic acid ata concentration of 03 prolonged shelf-life of fish-pasteproducts by 4 days at 15∘Cand inhibited the growth ofBacillussp isolated from fish-paste products [128] According to theresults of Cho et al the chitosan hydrolysate made withchitosanase from Aspergillus oryzae ATCC 22787 revealedthe strongest antimicrobial activity and inhibited the growthof Bacillus sp isolated from fish-paste products [129] Theaddition of chitosan hydrolysate at a concentration of 03resulted in extended shelf-life of up to 6 days at 15∘C Jeonget al reported that spraying cinnamon bark extract on thesurface of the fried fish-paste products could inhibit thegrowth of spoilage bacteria and mold at room temperatureand resulted in prolonged shelf-life [127]

Yamazaki et al investigated the effects of nisin andsucrose fatty acid esters on the growth of spoilage bacteria infish-paste products [130] Nisin exerted antibacterial activityagainst Bacillus subtilis and Bacillus licheniformis in a liquidmedium at 20∘C and resulted in a longer shelf-life forfish-paste products It was concluded that the addition ofnisin could be used as a potential alternative method toprevent spoilage caused by spore-forming bacteria in fish-paste productsThe bacteriocin produced byCarnobacteriummaltalomaticum had the ability to inhibit both Enterococcussp and Leuconostoc sp which reduce the shelf-life of fish-paste products during preservation [131] The results showedthat the purified bacteriocin piscicolin KH1 andor nisin sig-nificantly inhibited the growth of Leuconostoc mesenteroidesand Enterococcus faecium and could be used as a food-gradepreservative for kamaboko gels

24 Journal of Food Quality

Sakai and Yamaguchi examined the possibility of inhibit-ing lipid oxidation in boiled fish-paste by adding yuzu skinto the surimi [209] The heat-treated control kamabokoand yuzu skin-added kamaboko (citron kamaboko) wererefrigerated at 0∘C for 2 days and after heating the surimithe malonaldehyde content in both kamabokos was reducedThese results suggest that the addition of citron skin sup-pressed lipid oxidation in fish-paste products

Various packing materials and wrapping techniques havealso been employed to keep fish-paste products fresh and freeof contaminants for a longer period of time Lee et al investi-gated the processing conditions and quality stability of retortpouched fried-mackerel fish-paste during storage [210] Themackerel fish-paste was ground with added ingredients friedin soybean oil cooled vacuum-packed in a laminated plasticfilm and finally sterilized at 120∘C for 20min in a hotwater circulating retortThe reported method showed a goodpreservation for 100 days at 25 plusmn 3∘CThe sensory evaluationshowed no significant differences between the prepared fish-paste products and that of products in the market Ha et alexamined the optimum storage conditions for maintainingthe quality of the fried fish-paste in retort pouches [211]Both hardness and gel strength increased with increasingsterilization temperature On the other hand no differenceswere observed in elasticity and water-holding capacity

Lee et al elucidated the antioxidative effects of soyandor zein protein films containing green tea extract on thephysiological properties of fish-paste products during storage[132]The soy protein films showed an increase in yellownesswhile a decrease in yellowness was observed with the zeinfilms The lipid oxidation was retarded at day 2 of storageby wrapping the fried fish-paste products with soy and zeinprotein films containing green tea extract Lim et al prepareda Gelidium corneum whey protein isolate (GC-WPI) blendfilm containing grapefruit seed extract and studied the effectof this film on pathogenic bacterial inhibition during storage[133]TheGC-WPI blend was effective in decreasing the pop-ulations of Salmonella typhimurium Listeria monocytogenesand Escherichia coli on films treated with 01 grapefruitseed extract These studies suggest that packaging fish-pasteproducts in plant-based protein films containing green tea orgrapefruit seed extract could be beneficial to prolong shelf-life

5 Conclusion

The production of surimi dates back to ancient times How-ever advancement in surimi processing technology startedin 1960 with the discovery of cryoprotectants which werehelpful in maintaining the gel quality and functionality offish-paste for relatively longer periods of frozen storage [3]As themarket share of quality-conscious consumers rises thedemand for the use of natural additives rather than chemicalingredients for surimi products will continue to increaseAccording to Park et al the worldwide production of surimi-related products reached around 800000MT by 2011-2012while the main fish sources for surimi products includePacificwhitingAlaska pollock jackmackerel Atkamackerelsouthern blue whiting northern blue whiting and hoki [3]

Surimi is subdivided into high-grade (FA SA and A) andlow-grade (KA KB and RA) types based on the quality ofthe raw fish sources Most of the high-grade surimi is soldin Japan for the production of kamaboko and other high-quality surimi products and in Korea for the production ofpremium crabsticks Low-grade surimi is sold in Europe andthe United States for the manufacturing of crab sticks andin Korea and Japan for the preparation of other fried fishproducts [3] With the technological advancements in thesurimi processing industry it has been possible to use low-grade surimi for the production of fish cakes fish balls andother surimi products

With increasing demand and new processing techniques(eg the pH-shift method) the use of other seafoodresources such as small pelagic species and giant squid forthe production of surimi and surimi products was possible[212] Notably the production of surimi products is cheaperinKorea than elsewhere but industry professionals are alwayssearching for the most inexpensive surimi seafood sourcesHence the production of surimi from aquaculture fish suchas catfish and carp is growing in demand

Food additives from animal and seafood sources suchas fish chicken beef plasma proteins and egg white areconsidered the most effective protease inhibitors for surimiHowever with the outbreak of avian influenza mad cow dis-ease undesirable resulting characteristics and some religiousconstraints there is limited use of these food additives Addi-tionally vegetarians in some parts of the world would notwish to consume surimi-based products containing additivesderived from animals or even from seafood sources Hencethere is a need to identify more effective and alternative food-grade ingredients (eg plant sources seaweed and microal-gae) to be used in the preparation of fish-paste products

Surimi is mainly used for human consumption As suchthe challenges of production cost composition nutritionalvalue and the shelf-life of surimi products can never beneglected This review has provided an overview of nat-ural and synthetic food additives and preservatives usedto enhance the quality functionality and shelf-life of fish-paste products In addition the improvements in the fish-paste product quality and functionality by various foodadditives from seafood plants mushrooms animal sourcesand functional materials were discussed

For decades surimi and surimi-based products have beenwell known in East Asian countries such as Japan and KoreaHowever with advancements in technology they are attract-ing attention in other Asian as well as European countriesWith the increasing consumption worldwide the manufac-turing and processing of fish-paste products may requirenew and improved additives to enhance their acceptability inthe market Continuous scientific innovations and improvedprocessing technology will aid in further advancements andimprovements in this area

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article and regarding thefunding received

Journal of Food Quality 25

Authorsrsquo Contributions

Khawaja Muhammad Imran Bashir and Jin-Soo Kim con-tributed equally to this work

Acknowledgments

This research was a part of the Project no PJT200885entitled ldquoDevelopment andCommercialization of TraditionalSeafood Products Based on the Korean Coastal MarineResourcesrdquo funded by the Ministry of Oceans and FisheriesSouth Korea

References

[1] H-J Hwang S-Y Choi and S-C Lee ldquoPreparation andquality analysis of sodium-reduced fried fish cakesrdquo PreventiveNutrition and Food Science vol 18 no 3 pp 222ndash225 2013

[2] KFDA Food code Article 1-5-12 Korea Food and Drug Admin-istration Seoul Korea 2012

[3] J W Park H Nozaki T Suzuki and J-L Beliveau ldquoHistoricalreview of surimi technology and market developmentsrdquo inSurimi and Surimi seafood J W Park Ed pp 3ndash24 CRC PressNew York NY USA 2013

[4] J A Ramırez R Dıaz-Sobac O G Morales and M VazquezldquoEvaluation of freeze-dried surimi from tilapia and fat sleeper asemulsifiers [Evaluacion de surimi liofilizado de tilapia y dormi-dor como emulsificantes evaluacion de surimi liofilizado detilapia e dormidor como emulsificantes]rdquo Ciencia y TechnologiaAlimentaria vol 2 no 4 pp 210ndash214 1999

[5] J M Aguilera and D W Stanley ldquoFood structuringrdquo inMicrostructural Principles of Food Processing and Engineeringvol 12 p 246 AN Aspen Publishers Gaithersburg MarylandUSA 1999

[6] A P Stone and D W Stanley ldquoMechanisms of fish muscle gela-tionrdquo Food Research International vol 25 no 5 pp 381ndash3881992

[7] S Nakamura and M Ogawa ldquoBiomolecular strategies forpreparation of high quality surimi-based productsrdquo PreventiveNutrition and Food Science vol 10 no 2 pp 191ndash197 2005

[8] M Okada ldquoHistory of surimi technology in Japanrdquo in Surimitechnology T C Lanier and C M Lee Eds pp 3ndash22 MarcelDekker Inc New York NY USA 1992

[9] MIFAFF ldquoStatistics of fisheries processingrdquo Ministry of FoodAgriculture Forestry and Fisheries Seoul Korea 2011

[10] T C Lanier ldquoMeasurement of surimi composition and junc-tional propertiesrdquo in Surimi technology T C Lanier and C MLee Eds pp 123ndash166 Marcel Dekker Inc New York NY USA1992

[11] K-H Chung and C-M Lee ldquoRelationships between physico-chemical properties of nonfish protein and textural propertiesof protein-incorporated surimi gelrdquo Journal of Food Science vol55 pp 972ndash975 1990

[12] M TMorrissey JWWuD Lin andHAn ldquoProtease inhibitoreffects on torsionmeasurements and autolysis of Pacific whitingsurimirdquo Journal of Food Science vol 58 no 5 pp 1050ndash10541993

[13] J W Park ldquoFunctional protein additives in surimi gelsrdquo Journalof Food Science vol 59 no 3 pp 525ndash527 1994

[14] S Benjakul W Visessanguan and C Srivilai ldquoGel propertiesof bigeye snapper (Priacanthus tayenus) surimi as affected by

setting and porcine plasma proteinsrdquo Journal of Food Qualityvol 24 no 5 pp 453ndash471 2001

[15] D D Hamann P M Amato M C Wu and E A FoegedingldquoInhibition of modori (gel weakening) in surimi by plasmahydrolysate and egg whiterdquo Journal of Food Science vol 55 pp665ndash669 1990

[16] K D Reppond and J K Babbitt ldquoProtease inhibitors affectphysical properties of arrowtooth flounder and walleye pollocksurimirdquo Journal of Food Science vol 58 pp 96ndash98 1993

[17] V C Weerasinghe M T Morrissey and H An ldquoCharacteriza-tion of active components in food-grade proteinase inhibitorsfor surimi manufacturerdquo Journal of Agricultural and FoodChemistry vol 44 no 9 pp 2584ndash2590 1996

[18] C-Y Yang ldquoEffect of the addition of bovine plasma on thequality properties of steamed fish pasterdquo The Korean Journal ofFood and Nutrition vol 21 pp 518ndash523 2008

[19] K Duangmal and A Taluengphol ldquoEffect of protein additivessodium ascorbate and microbial transglutaminase on the tex-ture and colour of red tilapia surimi gelrdquo International Journalof Food Science amp Technology vol 45 no 1 pp 48ndash55 2010

[20] S BenjakulW Visessanguan and C Chantarasuwan ldquoEffect ofporcine plasma protein and setting on gel properties of surimiproduced from fish caught inThailandrdquo LWT- Food Science andTechnology vol 37 no 2 pp 177ndash185 2004

[21] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoCysteine proteinase inhibitor from chicken plasma Fractiona-tion characterization and autolysis inhibition of fish myofibril-lar proteinsrdquo Food Chemistry vol 101 no 4 pp 1647ndash1657 2007

[22] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoEffect of chicken plasma protein and some protein additiveson proteolysis and gel-forming ability of sardine (SardinellaGibbosa) surimirdquo Journal of Food Processing and Preservationvol 31 no 4 pp 492ndash516 2007

[23] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoRheological and textural properties of pacific whiting surimigels as influenced by chicken plasmardquo International Journal ofFood Properties vol 11 no 4 pp 820ndash832 2008

[24] M Sugiyama T Mishiro Y Tsukamasa T Suzuki and KTakama ldquoPuncture properties of kamaboko with ovomucoidpasteurized at several temperaturesrdquo Nippon Suisan Gakkaishivol 64 no 1 pp 76ndash81 1998

[25] M Sugiyama T Mishiro Y Tsukamasa et al ldquoPhysical prop-erties of Kamaboko with ovomucoid pasteurized at severaltemperaturesrdquo Nippon Suisan Gakkaishi vol 64 no 1 pp 82ndash87 1998

[26] J Yongsawatdigul and P Piyadhammaviboon ldquoInhibition ofautolytic activity of lizardfish surimi by proteinase inhibitorsrdquoFood Chemistry vol 87 no 3 pp 447ndash455 2004

[27] L Campo-Deano and C Tovar ldquoThe effect of egg albumen onthe viscoelasticity of crab sticks made from Alaska pollock andPacific whiting surimirdquo Food Hydrocolloids vol 23 no 7 pp1641ndash1646 2009

[28] A Hunt J W Park and A Handa ldquoEffect of various types ofegg white on characteristics and gelation of fish myofibrillarproteinsrdquo Journal of Food Science vol 74 no 9 pp C683ndashC6922009

[29] S Rawdkuen and S Benjakul ldquoWhey protein concentrateAutolysis inhibition and effects on the gel properties of surimiprepared from tropical fishrdquo Food Chemistry vol 106 no 3 pp1077ndash1084 2008

26 Journal of Food Quality

[30] Y Ruttanapornvareesakul K Somjit A Otsuka et al ldquoCry-oprotective effects of shrimp head protein hydrolysate on gelforming ability and protein denaturation of lizardfish surimiduring frozen storagerdquo Fisheries Science vol 72 no 2 pp 421ndash428 2006

[31] D K Li H Lin and SM Kim ldquoEffect of rainbow trout (Oncor-hynchus mykiss) plasma protein on the gelation of Alaska pol-lock (Theragra chalcogramma) surimirdquo Journal of Food Sciencevol 73 no 4 pp C227ndashC234 2008

[32] A Hernandez-Briones G Velazquez M Vazquez and J ARamırez ldquoEffects of adding fish gelatin onAlaska pollock surimigelsrdquo Food Hydrocolloids vol 23 no 8 pp 2446ndash2449 2009

[33] T Yin Z H Reed and J W Park ldquoGelling properties of surimias affected by the particle size of fish bonerdquo LWT- Food Scienceand Technology vol 58 no 2 pp 412ndash416 2014

[34] T Yin and J W Park ldquoTextural and rheological properties ofPacific whiting surimi as affected by nano-scaled fish bone andheating ratesrdquo Food Chemistry vol 180 pp 42ndash47 2015

[35] M R Fowler and J W Park ldquoEffect of salmon plasma proteinon Pacific whiting surimi gelation under various ohmic heatingconditionsrdquo LWT- Food Science and Technology vol 61 no 2pp 309ndash315 2015

[36] M R Fowler and J W Park ldquoSalmon blood plasma Effectiveinhibitor of protease-laden Pacific whiting surimi and salmonmincerdquo Food Chemistry vol 176 pp 448ndash454 2015

[37] S Klomklao S Benjakul H Kishimura K Osako and BK Simpson ldquoTrypsin inhibitor from yellowfin tuna (Thunnusalbacores) roe Effects on gel properties of surimi from bigeyesnapper (Priacanthus macracanthus)rdquo LWT- Food Science andTechnology vol 65 pp 122ndash127 2016

[38] N K Vate and S Benjakul ldquoEffect of the mixtures of squid inktyrosinase and tannic acid on properties of sardine surimi gelrdquoJournal of Food Science and Technology vol 53 no 1 pp 411ndash420 2016

[39] T Yamashita ldquoEffects of commercial soybean protein andwheat gluten as subsidiary materials on physical properties ofkamabokordquo Nippon Shokuhin Kogyo Gakkaishi vol 38 no 12pp 883ndash890 1991

[40] K H Chung and C M Lee ldquoFunction of nonfish proteins insurimi-based gel productsrdquo Korean Journal of Society of FoodScience vol 10 pp 146ndash150 1994

[41] K-H Chung and C-M Lee ldquoEvaluation of wheat gluten andmodified starches for their texture-modifying and freeze-thawstabilizing effects on surimi based-productsrdquo Journal of FoodScience and Nutrition pp 190ndash195 1996

[42] S Benjakul S Karoon and A Suwanno ldquoInhibitory effects oflegume seed extracts on fish proteinasesrdquo Journal of the Scienceof Food and Agriculture vol 79 no 13 pp 1875ndash1881 1999

[43] S Benjakul W Visessanguan and P Thummaratwasik ldquoInhi-bition of gel weakening of threadfin bream surimi using Thailegume seed proteinase inhibitorsrdquo Journal of Food Biochem-istry vol 24 no 5 pp 363ndash380 2000

[44] A Oujifard S Benjakul M Ahmad and J Seyfabadi ldquoEffect ofbambara groundnut protein isolate on autolysis and gel prop-erties of surimi from threadfin bream (Nemipterus bleekeri)rdquoLWT- Food Science and Technology vol 47 no 2 pp 261ndash2662012

[45] Y Luo RKuwaharaMKaneniwa YMurata andMYokoyamaldquoEffect of soy protein isolate on gel properties of Alaska pollockand common carp surimi at different setting conditionsrdquoJournal of the Science of Food and Agriculture vol 84 no 7 pp663ndash671 2004

[46] Y Luo H Shen D Pan and G Bu ldquoGel properties of surimifrom silver carp (Hypophthalmichthys molitrix) as affected byheat treatment and soy protein isolaterdquo Food Hydrocolloids vol22 no 8 pp 1513ndash1519 2008

[47] C Cardoso B Ribeiro and R Mendes ldquoEffects of dietary fibreandmicrobial transglutaminase addition on the rheological andtextural properties of protein gels from different fish speciesrdquoJournal of Food Engineering vol 113 no 4 pp 520ndash526 2012

[48] T Kudre S Benjakul and H Kishimura ldquoEffects of proteinisolates from black bean and mungbean on proteolysis and gelproperties of surimi from sardine (Sardinella albella)rdquo LWT-Food Science and Technology vol 50 no 2 pp 511ndash518 2013

[49] S Klomklao and S Benjakul ldquoEffect of trypsin inhibitor inadzuki bean (Vigna angularis) on proteolysis and gel propertiesof threadfin bream (Nemipterus bleekeri)rdquo LWT- Food Scienceand Technology vol 63 no 2 pp 906ndash911 2015

[50] S Konoo H Ogawa and N Iso ldquoEffects of addition of amyloseand amylopectin on the breaking strength of fish meat gelrdquoNippon Suisan Gakkaishi vol 64 no 1 pp 69ndash75 1998

[51] C-S Kong H Ogawa and N Iso ldquoRheological analysis of theeffect of gelatinization of starch added to fish-meat gel based onvolume changesrdquo Fisheries Science vol 65 no 6 pp 930ndash9361999

[52] B-Y Kim W-W Kim and B Yoo ldquoEffect of native and acety-lated sweet potato starch on rheological properties of compositesurimi solrdquo Journal of Food Science and Nutrition vol 13 no 3pp 245ndash248 2008

[53] B-J Yoo ldquoThe effects of alkaline treatment and potato-starchcontent on the quality of fishmeat paste products prepared fromPacific sandlance Ammodytes personatus Girardrdquo Fisheries andAquatic Sciences vol 14 no 3 pp 161ndash167 2011

[54] S M Cho M S Yoon and S-B Kim ldquoEffects of rice flourmilling types and addition methods on rheological and sensoryproperties of surimi productsrdquo Korean Journal of Fisheries andAquatic Sciences vol 46 no 2 pp 139ndash146 2013

[55] Y-M Kwon and J-S Lee ldquoA study on the quality characteristicsof fish cakes containing rice flourrdquo Korean Journal of HumanEcology vol 22 no 1 pp 189ndash200 2013

[56] M Yoon J-S Kim D Kim J Jo and S Cho ldquoOptimization ofthe processing conditions for the preparation of surimi productscontaining rice flourrdquo Fisheries and Aquatic Sciences vol 17 no2 pp 167ndash173 2014

[57] J A Ramırez M Barrera O G Morales and M VazquezldquoEffect of xanthan and locust bean gums on the gelling prop-erties of myofibrillar proteinrdquo Food Hydrocolloids vol 16 no 1pp 11ndash16 2002

[58] A M Barrera J A Ramırez J J Gonzalez-Cabriales and MVazquez ldquoEffect of pectins on the gelling properties of surimifrom silver carprdquo Food Hydrocolloids vol 16 no 5 pp 441ndash4472002

[59] S Benjakul W Visessanguan S Phatchrat and M TanakaldquoChitosan affects transglutaminase-induced surimi gelationrdquoJournal of Food Biochemistry vol 27 no 1 pp 53ndash66 2003

[60] M A Iglesias-Otero J Borderıas and C A Tovar ldquoUse ofKonjac glucomannan as additive to reinforce the gels from low-quality squid surimirdquo Journal of Food Engineering vol 101 no3 pp 281ndash288 2010

[61] S-H Eom J-A Kim B-Y Son et al ldquoEffects of carrageenanon the gelatinization of salt-based surimi gelsrdquo Fisheries andAquatic Sciences vol 16 no 3 pp 143ndash147 2013

Journal of Food Quality 27

[62] S H Choi and S M Kim ldquoQuality properties of giant squid(Dosidicus gigas) surimi-based product manufactured withAmorphophallus konjac flourrdquo Korean Journal of Food Scienceand Technology vol 44 no 4 pp 422ndash427 2012

[63] D Cando B Herranz A J Borderıas and H M MorenoldquoEffect of high pressure on reduced sodium chloride surimigelsrdquo Food Hydrocolloids vol 51 pp 176ndash187 2015

[64] D-S Kim and Y-H Park ldquoEffect of food humectants onlowering water activity of casing kamaboko 1 Effect of loweringwater activity of sodium chloride sugars and polyolsrdquo Bulletinof the Korean Fisheries Society vol 14 pp 139ndash147 1981

[65] D-S Kim and Y-H Park ldquoEffect of food humectant on lower-ingwater activity of casing kamaboko 2 Effect of loweringwateractivity of starch glycine and sodium lactate and prediction ofthe water activity lowing ability of humectantsrdquo Bulletin of theKorean Fisheries Society vol 15 pp 74ndash82 1982

[66] G L Sanchez Pascua M R Casales and M I Yeannes ldquoInflu-ence of water and glycerol contents on the aw of fish pastesrdquoJournal of Aquatic Food Product Technology vol 10 no 1 pp89ndash100 2001

[67] E Niwa K Tsujimoto and S Kanoh ldquoKamaboko gel-strength-ening effect of polyuronides and other polysaccharidesrdquoNipponSuisan Gakkaishi vol 58 pp 85ndash88 1992

[68] R Yoshinaka M Shiraishi and S Ikeda ldquoEffect of AscorbicAcid on theGel Formation of FishMeatrdquoBulletin of the JapaneseSociety for the Science of Fish vol 38 no 5 pp 511ndash515 1972

[69] H G Lee C M Lee K H Chung and S A Lavey ldquoSodiumascorbate affects surimi gel-forming propertiesrdquo Journal of FoodScience vol 57 pp 1343ndash1347 1992

[70] Y Park S D Kelleher D J McClements and E A DeckerldquoIncorporation and stabilization of omega-3 fatty acids insurimi made from cod Gadus morhuardquo Journal of Agriculturaland Food Chemistry vol 52 no 3 pp 597ndash601 2004

[71] E Okazaki Y Yamashita and Y Omura ldquoEmulsification of fishoil in surimi by high-speed mixing and improvement of gel-forming abilityrdquo Nippon Suisan Gakkaishi vol 68 no 4 pp547ndash553 2002

[72] H Fukushima E Okazaki S Noda and Y Fukuda ldquoChangesin physical properties water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oilrdquoNippon Shokuhin Kagaku Kogaku Kaishi vol 54 no 1 pp 39ndash44 2007

[73] B N Pietrowski R Tahergorabi and J Jaczynski ldquoDynamicrheology and thermal transitions of surimi seafood enhancedwith 120596-3-rich oilsrdquo Food Hydrocolloids vol 27 no 2 pp 384ndash389 2012

[74] A K Balange S Benjakul and S Maqsood ldquoGel strengtheningeffect of wood extract on surimi produced frommackerel storedin icerdquo Journal of Food Science vol 74 no 8 pp C619ndashC6272009

[75] N Buamard and S Benjakul ldquoImprovement of gel properties ofsardine (Sardinella albella) surimi using coconut husk extractsrdquoFood Hydrocolloids vol 51 pp 146ndash155 2015

[76] A K Balange and S Benjakul ldquoEffect of oxidised phenolic com-pounds on the gel property of mackerel (Rastrelliger kanagurta)surimirdquo LWT- Food Science and Technology vol 42 no 6 pp1059ndash1064 2009

[77] A Balange and S Benjakul ldquoEnhancement of gel strength ofbigeye snapper (Priacanthus tayenus) surimi using oxidisedphenolic compoundsrdquo Food Chemistry vol 113 no 1 pp 61ndash702009

[78] Y A Arfat and S Benjakul ldquoEffect of zinc sulphate on gellingproperties of phosphorylated protein isolate from yellow stripetrevallyrdquo Food Chemistry vol 141 no 3 pp 2848ndash2857 2013

[79] M-S Bae and S-C Lee ldquoQuality characteristics of fried fishpaste containing anchovy powderrdquo Journal of the Korean Societyof Food Science and Nutrition vol 36 no 9 pp 1188ndash1192 2007

[80] M-S Bae J-U Ha and S-C Lee ldquoQuality properties of highcalcium fish paste containing anchovyrdquo Korean Journal of Foodand Cookery Science vol 23 pp 561ndash566 2007

[81] H-S Cho and K-H Kim ldquoQuality characteristics of fish pastecontaining skate (Raja kenojei) powderrdquo Journal of the EastAsian Society of Dietary Life vol 21 pp 808ndash813 2011

[82] Y H Park E Y Bum E R Jeon and LH Jung ldquoEffect of addedskate (Raja kenojei) on the quality characteristics of steamedfishmeat pasterdquo Food Science and Biotechnology vol 23 no 5 pp1453ndash1458 2014

[83] S-M Park B-B Lee Y-M Hwang and S-C Lee ldquoQualityproperties of fish paste containing Styela clavardquo Journal of theKorean Society of Food Science and Nutrition vol 35 pp 908ndash911 2006

[84] S-Y Choi E-Y Choi K-E Lee A-S Song S-H Park and S-C Lee ldquoPreparation and quality analysis of fish paste containingStyela clava tunicrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 41 no 11 pp 1591ndash1595 2012

[85] S-M Park H-K Seo and S-C Lee ldquoPreparation and qualityproperties of fish paste containing Styela plicatardquo Journal of theKorean Society of Food and Nutrition vol 35 pp 1256ndash12592006

[86] J-S Seo and H-S Cho ldquoQuality characteristics of fish pastewith shrimp powderrdquo Korean Journal of Food Preservation vol19 pp 519ndash524 2012

[87] H-S Cho and K-H Kim ldquoQuality properties of fish pastecontaining green laver powderrdquo Journal of the Korean Societyof Food Culture vol 29 pp 421ndash427 2014

[88] I-D Park ldquoQuality characteristics of fish paste containingLagocephalus lunaris powderrdquo Journal of the Korean Society ofFood Culture vol 28 pp 657ndash663 2013

[89] I Park ldquoQuality properties of fish paste containingCapsosiphonfulvescens powderrdquo Journal of The Korean Society of FoodCulture vol 31 no 4 pp 357ndash363 2016

[90] B-M Kim J-H Jung M-J Jung D-S Kim J-Y Jun and I-H Jeong ldquoThe quality characteristics and processing of fishpaste containing red snow crabChionoecetes japonicus leg-meatpowderrdquo Korean Journal of Fisheries and Aquatic Sciences vol49 pp 1ndash6 2016

[91] Y-J Shin and G-S Park ldquoQuality characteristics of fish-pastecontaining mulberry leaf powderrdquo Journal of the East AsianSociety of Dietary Life vol 15 pp 738ndash745 2005

[92] Y-J Shin ldquoQuality characteristics of fish paste containing lotus(Nelumbo nucifera) leaf powderrdquo Korean Journal of Food andCookery Science vol 23 pp 947ndash953 2007

[93] A D Thorat V R Joshi A U Pagarkar and A K BalangeldquoMicrowave pasteursation of fish paste product-Kamabokowith Beetroot and Spinachrdquo Ecology Environment and Conser-vation vol 13 no 1 pp 113ndash118 2007

[94] M-O Yang and E-J Cho ldquoQuality properties of surimi withadded citrus fruitsrdquo Journal of East Asian Society of Dietary Lifevol 17 pp 58ndash63 2007

[95] F Alakhrash U Anyanwu and R Tahergorabi ldquoPhysicochemi-cal properties of Alaska pollock (Theragra chalcograma) surimigels with oat branrdquo LWT- Food Science and Technology vol 66pp 41ndash47 2016

28 Journal of Food Quality

[96] J-S Kim and G-I Byun ldquoMaking fish paste with yam (Dios-corea japonica Thumb) powder and its characteristicsrdquo KoreanJournal of Culinary Research vol 15 pp 57ndash69 2009

[97] Y-J Shin J A Lee and G-S Park ldquoa Quality characteristics offish pastes containing Lycii fructus powderrdquo Journal of the EastAsian Society of Dietary Life vol 18 pp 22ndash28 2008

[98] D-W Shim J Jiang J-H Kim et al ldquoEffects of size adjustedwith red ginseng powders on quality of fish pastesrdquo Journal ofthe Korean Society of Food Science and Nutrition vol 41 no 10pp 1448ndash1453 2012

[99] Y-J Shin J A Lee and G-S Park ldquoQuality characteristics offish paste containing Angelicae gigantis Radix powderrdquo KoreanJournal of Food and Cookery Science vol 24 pp 699ndash705 2008

[100] S Choi ldquoQuality characteristics of fish paste containing Cur-cuma longa L powderrdquo The Korean Journal of Food and Nutri-tion vol 25 no 4 pp 833ndash841 2012

[101] J-A Jang H-A Kim and S-K Choi ldquoQuality characteristicsof fish cake made with silver pomfret (Pampus argenteus) withadded wasabi powderrdquo Journal of the East Asian Society ofDietary Life vol 20 pp 103ndash112 2010

[102] Y-J Shin K-S Kim and G-S Park ldquoTexture and sensorycharacteristics of fish paste containing white Poria cocos wolfpowderrdquo Korean J Food Cookery Sci vol 25 pp 119ndash125 2009

[103] J-U Ha S-G Koo H-Y Lee Y-M Hwang and S-C LeeldquoPhysical properties of fish paste containing Agaricus bisporusrdquoKorean Journal of Food Science and Technology vol 33 pp 451ndash454 2001

[104] S-G Koo Y-K Ryu Y-M Hwang J-U Ha and S-C LeeldquoQuality properties of fish-paste containing enoki mushroom(Flammuilna velutipes)rdquo Journal of the Korean Society of FoodScience and Nutrition vol 30 pp 288ndash291 2001

[105] M-H Son S-Y Kim J-U Ha and S-C Lee ldquoTexture prop-erties of surimi gel containing shiitake mushroom (Lentinusedodes)rdquo Journal of the Korean Society of Food Science andNutrition vol 32 pp 859-853 2003

[106] S-Y Kim M-H Son J-U Ha and S-C Lee ldquoPreparationand characterization of fried surimi gel containing king oystermushroom (Pleurotus eryngii)rdquo Journal of the Korean Society ofFood Science and Nutrition vol 32 pp 855ndash858 2003

[107] S I Chung S Y Kim Y J Nam andM Y Kang ldquoDevelopmentof surimi gel from king oyster mushroom and cuttlefish meatpasterdquo Food Science and Biotechnology vol 19 no 1 pp 51ndash562010

[108] S K Jin J H Park and S J Hur ldquoEffect of substituting surimiwith spent laying hen meat on the physicochemical character-istics of fried fish pasterdquo Food and Bioprocess Technology vol 7no 3 pp 901ndash908 2014

[109] A Debusca R Tahergorabi S K Beamer K E Matak and JJaczynski ldquoPhysicochemical properties of surimi gels fortifiedwith dietary fiberrdquo Food Chemistry vol 148 pp 70ndash76 2014

[110] H-S Yook J-W Lee H-J Lee B-S Cha S-Y Lee and M-W Byun ldquoQuality properties of fish paste prepared with refineddietary fiber from ascidian (Halocynthia roretzi) tunicrdquo Journalof the Korean Society of Food Science and Nutrition vol 29 pp642ndash646 2000

[111] A Debusca R Tahergorabi S K Beamer S Partington andJ Jaczynski ldquoInteractions of dietary fibre and omega-3-rich oilwith protein in surimi gels developed with salt substituterdquo FoodChemistry vol 141 no 1 pp 201ndash208 2013

[112] C Sell S Beamer J Jaczynski and K E Matak ldquoSensorycharacteristics and storage quality indicators of surimi franks

nutritionally enhanced with omega-3 rich flaxseed oil andsalmon oilrdquo International Journal of Food Science amp Technologyvol 50 no 1 pp 210ndash217 2015

[113] T Chang C Wang X Wang L Shi H Yang and M CuildquoEffects of soybean oil moisture and setting on the textural andcolor properties of surimi gelsrdquo Journal of Food Quality vol 38no 1 pp 53ndash59 2015

[114] J-S Kim M-L Cho and M-S Heu ldquoQuality improvement ofheat-induced surimi gel using calcium powder of cuttle Sepiaesculenta bone treated with acetic acidrdquo Journal of the KoreanFisheries Society vol 36 pp 198ndash203 2003

[115] G-W Kim G-H Kim J-S Kim et al ldquoQuality characteristicsof fried fish paste of Alaska pollack meat paste added withpropolisrdquo Journal of the Korean Society of Food Science andNutrition vol 37 no 4 pp 485ndash489 2008

[116] G-W Kim G-H Kim J-S Kim et al ldquoQuality of fried fishpaste prepared with sand-lance (Hypoptychus dybowskii) meatand propolis additiverdquo Journal of the Korean Fisheries Societyvol 41 pp 170ndash175 2008

[117] B Park H Cho and S Park ldquoStudy on quality characteristicsof fish paste containing cheonggukjang powderrdquo Journal of TheKorean Society of Food Culture vol 30 no 2 pp 213ndash219 2015

[118] SMiyao T Shindoh KMiyamori and T Arita ldquoEffects of highpressurization on the growth of bacteria derived from surimi(fish paste)rdquo Nippon Shokuhin Kogyo Gakkaishi vol 40 pp478ndash484 1993

[119] A Malicki Z Sysak S Bruzewicz J Zrodłowska-Danek andM Szpak ldquoApplication of high hydrostatic pressure to extendthe shelf-life of traditionally produced fish pasterdquo MedycynaWeterynaryjna vol 66 pp 695ndash698 2010

[120] J-H Kim J-Y Jeon S-R Ryu et al ldquoMicrobial quality andphysiochemical changes of grilled fish paste in a group-mealservice affected by gamma-irradiationrdquo Korean Journal of FoodPreservation vol 11 pp 522ndash529 2004

[121] H-O Cho J-H Kwon M-W Byun and M-K Lee ldquoPreserva-tion of fried fish-paste by Irradiationrdquo Korean Journal of FoodScience and Technology vol 17 pp 474ndash481 1985

[122] H-Y Shin Y-J Lee I-Y Park J-Y Kim S-J Oh and K BSong ldquoEffect of chlorine dioxide treatment onmicrobial growthand qualities of fish paste during storagerdquo Journal of the KoreanSociety for Applied Biological Chemistry vol 50 pp 42ndash47 2007

[123] S S YoonH Kim YM Lee E J Jeong andY J Cha ldquoShelf-lifeextension effects of fish paste product by adding pepper extractrdquoin Proceedings of the Korean Nutrition Society Conference p 216Seoul Korea 2001

[124] E-S Ahn M-S Kim and D-H Shin ldquoScreening of natu-ral antimicrobial edible plant extract for dooboo fish pastemakkoli spoilage microorganismrdquo Korean Journal of FoodScience and Technology vol 26 pp 733ndash739 1994

[125] Y-M Kim B-H Lee S-H Lee I-S Shin and T-S LeeldquoThe preservative effect of egg white lysozyme added surimiproductsrdquo Bulletin of the Korean Fisheries Society vol 21 pp269ndash275 1988

[126] S-H Cho I-S Joo I-W Seo and Z-W Kim ldquoPreservativeeffect of grapefruit seed extract on fish meat productrdquo Journalof Food Hygiene and Safety vol 6 pp 67ndash72 1991

[127] E-T Jeong M-Y Park E-W Lee U-T Park and D-S ChangldquoAntimicrobial characteristics against spoilage microorganismsand food preservative effect of cinnamon (Cinnamomum cassiaBlume) bark extractrdquo Korean Journal of Life Science vol 8 pp648ndash653 1998

Journal of Food Quality 29

[128] D-S Chang H-R Cho H-S Lee M-Y Park and S-M LimldquoDevelopment of alginic acid hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 823ndash826 1998

[129] H-R Cho D-S Chang W-D Lee E-T Jeong and E-WLee ldquoUtilization of chitosan hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 817ndash822 1998

[130] K Yamazaki T Tashiro S Shirahama J-Y Jun and Y KawaildquoGrowth inhibition of spore-forming bacteria in fish-pasteproducts by Nisinrdquo Nippon Shokuhin Kagaku Kogaku Kaishivol 61 no 2 pp 70ndash76 2014

[131] K Hashimoto M L Bari Y Inatsu S Kawamoto and J ShimaldquoBiopreservation of kamaboko (steamed surimi) using pisci-colin KH1 produced by Carnobacteriummaltalomaticum KH1rdquoJapanese Journal of FoodMicrobiology vol 28 pp 193ndash200 2011

[132] S H Lee M S Lee S K Park D H Bae S D Ha and K BSong ldquoPhysical properties of protein films containing green teaextract and its antioxidant effect on fish paste productsrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1063ndash1067 2004

[133] G-O Lim Y-H Hong and K B Song ldquoIncorporating grape-fruit seed extract into Gelidium corneum-whey protein isolateblend packaging film increases the shelf life of fish paste -Research noterdquo Journal of Food Science and Nutrition vol 13no 4 pp 370ndash374 2008

[134] T C Lanier J Yongsawatdigul and P Carvajal-RondanellildquoSurimi gelation chemistryrdquo in Surimi and Surimi Seafood J WPark Ed pp 101ndash139Marcel Dekker NewYork NYUSA 2013

[135] M Kinoshita H Toyohara and Y Shimizu ldquoPurification andproperties of a novel latent proteinase showing myosin heavychain-degrading activity from threadfin-bream musclerdquo TheJournal of Biochemistry vol 107 no 4 pp 587ndash591 1990

[136] D H Wasson J K Babbitt and J S French ldquoCharacterizationof a heat stable protease from arrowtooth flounder Atheresthesstomiasrdquo Journal of Aquatic Food Product Technology vol 1 no3-4 pp 167ndash182 1993

[137] T A Seymour M T Morrissey M Y Peters and H An ldquoPuri-fication and characterization of pacific whiting proteasesrdquoJournal of Agricultural and Food Chemistry vol 42 no 11 pp2421ndash2427 1994

[138] H An V Weerasinghe T A Seymour and M T MorrisseyldquoCathepsin degradation of Pacific whiting surimi proteinrdquoJournal of Food Science vol 59 pp 1013ndash1017 1994

[139] AFDF Ground fish quality chart Alaska fisheries departmentfoundation Anchorage Alaska 1992

[140] G Sylvia S Larkin and M T Morrissey ldquoQuality and resourcemanagement bioeconomic analysis of the Pacific whitingindustryrdquo in Recent Advances inMarine Science and TechnologyO Bellwood H Choat and N Saxena Eds James CookUniversity Townsville QS Australia 1994

[141] S H Choi and S M Kim ldquoDevelopment of giant squid(Ommastrephes bartrami) surimi-based products with gel tex-ture enhancers and the effects of setting on gel qualityrdquo Journalof the Korean Society of Food Science and Nutrition vol 41 no7 pp 975ndash981 2012

[142] J A Ramırez R M Uresti G Velazquez and M VazquezldquoFood hydrocolloids as additives to improve the mechanicaland functional properties of fish products A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1842ndash1852 2011

[143] S-K Kim H-G Byun P-J Park and F Shahidi ldquoAngiotensinI converting enzyme inhibitory peptides purified from bovine

skin gelatin hydrolysaterdquo Journal of Agricultural and FoodChemistry vol 49 no 6 pp 2992ndash2997 2001

[144] I Kimura M Sugimoto K Toyoda N Seki K-I Arai andT Fujita ldquoA study on the cross-links reaction of myosin inkamaboko rsquosuwarirsquo gelsrdquo Nippon Suisan Gakkaisi vol 57 pp1386ndash1396 1991

[145] H An M Y Peters and T A Seymour ldquoRoles of endogenousenzymes in surimi gelationrdquo Trends in Food Science amp Technol-ogy vol 7 no 10 pp 321ndash327 1996

[146] R Nopianti N Huda andN Ismail ldquoA review on the loss of thefunctional properties of proteins during frozen storage and theimprovement of gel-forming properties of Surimirdquo AmericanJournal of Food Technology vol 6 no 1 pp 19ndash30 2011

[147] A M Martın-Sanchez C Navarro J A Perez-Alvarez and VKuri ldquoAlternatives for efficient and sustainable production ofsurimi A reviewrdquo Comprehensive Reviews in Food Science andFood Safety vol 8 no 4 pp 359ndash374 2009

[148] Korea Agro-Fisheries and Food Trade Corporation Processedfood segmented market survey-fish cake market Korea Agro-Fisheries and Food Trade Corporation Seoul Korea 2014

[149] D Kraft and A DerMarderosian The A-Z guide to food asmedicine CRC Press Boca Raton Fla USA 2016

[150] C V Morr and E A Foegeding ldquoComposition and function-ality of commercial whey and milk protein concentrates andisolates a status reportrdquo Food Technology vol 44 pp 100ndash1121990

[151] A Saiga T Okumura T Makihara et al ldquoAngiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chickenbreast muscle extractrdquo Journal of Agricultural and Food Chem-istry vol 51 no 6 pp 1741ndash1745 2003

[152] B Li F Chen X Wang B Ji and Y Wu ldquoIsolation and iden-tification of antioxidative peptides from porcine collagenhydrolysate by consecutive chromatography and electrosprayionization-mass spectrometryrdquo Food Chemistry vol 102 no 4pp 1135ndash1143 2007

[153] A Trampuz R M Prabhu T F Smith and L M BaddourldquoAvian Influenza A New Pandemic Threatrdquo Mayo ClinicProceedings vol 79 no 4 pp 523ndash530 2004

[154] M C Gomez-Guillen B Gimenez M E Lopez-Caballeroand M P Montero ldquoFunctional and bioactive properties ofcollagen and gelatin from alternative sources A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1813ndash1827 2011

[155] D Li X Fu and S M Kim ldquoProduction of chum salmoncystatin from the recombinant Saccharomyces cerevisiae opti-mized using response surface methodologyrdquo Biotechnology andBioprocess Engineering vol 15 no 2 pp 314ndash323 2010

[156] H Akazawa Y Miyauchi K Sakurada H Wasson and K DReppond ldquoEvaluation of protease inhibitors in Pacific whitingsurimirdquo Journal of Aquatic Food Product Technology vol 2 no3 pp 79ndash95 1994

[157] A Hunt K J K Getty and J W Park ldquoRoles of starch in surimiseafood A reviewrdquo Food Reviews International vol 25 no 4 pp299ndash312 2009

[158] T Suzuki Fish and Krill Protein Processing Technology AppliedScience Publishers London UK 1981

[159] C M Lee ldquoSurimi process technologyrdquo Food Technology vol38 pp 69ndash80 1984

[160] M C Wu D D Hamann and T C Lanier ldquoRheological andcalorimetric investigations of starch-fish protein systems duringthermal processingrdquo Journal of Texture Studies vol 16 pp 53ndash74 1985

30 Journal of Food Quality

[161] M C Wu T C Lanier and D D Hamann ldquoRigidity and vis-cosity changes of croaker actomyosin during thermal gelationrdquoJournal of Food Science vol 50 no 1 pp 14ndash19 1985

[162] S-K Kim S-T Yang and E-H Lee ldquoThe starch content of fish-paste products onmarketrdquo Journal of the Korean Society of FoodScience and Nutrition vol 7 pp 41-42 1978

[163] G AMacDonald T C Lanier and P A Caruajal ldquoStabilizationof protein in surimirdquo in Surimi and Surimi Seafood J W ParkEd pp 91ndash125 Marcel Dekker Inc New York NY USA 2000

[164] J A Ramırez I A Santos O G Morales M T Morrisseyand M Vazquez ldquoApplication of microbial transglutaminaseto improve mechanical properties of surimi from silver carputilizacionde transglutaminasa microbiana paramellora-las-propiedades mecanicas de surimide carpaplateada utiliza-cionde transglutaminasamicrobiana paramejorarlaspropieda-des mecanicas de surimide carpaplateadardquo Ciencia y TecnologıaAlimentaria vol 3 no 1 pp 21ndash28 2000

[165] M C Gomez-Guillen A J Borderıas and P MonteroldquoSalt nonmuscle proteins and hydrocolloids affecting rigiditychanges during gelation of giant squid (Dosidicus gigas)rdquoJournal of Agricultural and Food Chemistry vol 45 no 3 pp616ndash621 1997

[166] J W Park ldquoIngredient technology and formulation develop-mentrdquo in Surimi and Surimi Seafood J W Park Ed pp 91ndash125Marcel Dekker Inc New York NY USA 2000

[167] F Garcıa-Ochoa V E Santos J A Casas and E Gomez ldquoXan-than gum production recovery and propertiesrdquo BiotechnologyAdvances vol 18 no 7 pp 549ndash579 2000

[168] A I Rodrıguez-Hernandez and A Tecante ldquoDynamic vis-coelastic behavior of gellan- 120580 -carrageenan and gellan-xanthangelsrdquo Food Hydrocolloids vol 13 no 1 pp 59ndash64 1999

[169] J A Casas and F Garcıa-Ochoa ldquoSophorolipid production byCandida bombicola Medium composition and culture meth-odsrdquo Journal of Bioscience and Bioengineering vol 88 no 5 pp488ndash494 1999

[170] H J Lim ldquoA study on the calcium and sodium intakes andurinary calcium excretion of preschool children in BusanrdquoKorean Journal of Nutrition vol 34 pp 786ndash796 2001

[171] WHO ldquoDiet nutrition and the prevention of chronic diseasesReport of a joint WHOFAO expert consultationrdquo Tech RepWHO World Health Organization Geneva Switzerland 2003

[172] L K Dahl ldquoPossible role of salt intake in the development ofessential hypertensionrdquo International Journal of Epidemiologyvol 34 no 5 pp 967ndash972 2005

[173] H-K Jeong D-S Kim S-J Chun K-S Jo and Y-H ParkldquoEffect of food humectant on lowering water activity of casingKamaboko 3rdquo Bulletin of the Korean Fisheries Society vol 16 pp88ndash96 1983

[174] J Han E Kim M Cheong S Chee and K Chee ldquoBioavailabil-ity and digestibility of organic calcium sources by bone healthindexrdquo Journal of Nutrition and Health vol 43 no 1 pp 12ndash252010

[175] M K Lee ldquoA study of the bio-functional evaluation of Rajaskates caught in Huksando areardquo Journal of the Kwangju HealthCollege vol 21 pp 253ndash265 1996

[176] S H Cho Extraction and characterization of gelatin andantimicrobial peptide from skate (Raja kenojei) skins ChonnamNational University Gwangju Korea 2003

[177] J H Choi ldquoIsolation and purification of in chondroitin sulfatefrom skate cartilagerdquo Tech Rep Pukyong National UniversityBusan Korea 2004

[178] Y G Jo ldquoThe sterol composition of Styela clavardquo Journal of theKorean Fisheries Society vol 11 pp 97ndash101 1978

[179] S H Ahn ldquoExtraction of glycosaminoglycans from Styela clavatunicrdquo Biotechnology and Bioprocess Engineering vol 18 pp180ndash185 2003

[180] J J Kim S J Kim S H Kim H R Park and S C LeeldquoAntioxidant and anticancer activities of extracts from Styelaclava according to the processing methods and solventsrdquoJournal of the Korean Society of Food Science and Nutrition vol35 pp 278ndash283 2006

[181] T Aoki K Takata and N Kunisaki ldquoComparison of nutrientcomponents of six species of wild and cultured fishesrdquo Bulletinof the Japanese Society for the Science of Fish vol 57 pp 1927ndash1934 1991

[182] Committee Donguibogam Translated Donguibogam Bubin-munwha Press Seoul Korea 1999

[183] Y-K Park H-J Kim and M-H Kim ldquoQuality characteristicsof fried fish paste added with ethanol extract of onionrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1049ndash1055 2004

[184] G L Dong J J Hyun and E-R Woo ldquoAntimicrobial prop-erty of (+)-lyoniresinol-3120572-O-120573-D- glucopyranoside isolatedfrom the root bark of Lycium chinense Miller against humanpathogenic microorganismsrdquo Archives of Pharmacal Researchvol 28 no 9 pp 1031ndash1036 2005

[185] C C Wang S C Chang B S Inbaraj and B H ChenldquoIsolation of carotenoids flavonoids and polysaccharides fromLycium barbarum L and evaluation of antioxidant activityrdquoFood Chemistry vol 120 no 1 pp 184ndash192 2010

[186] Z Zhang X Liu T Wu et al ldquoSelective suppression of cervicalcancer Hela cells by 2-O-120573-d- glucopyranosyl-l-ascorbic acidisolated from the fruit of Lycium barbarum Lrdquo Cell Biology andToxicology vol 27 no 2 pp 107ndash121 2011

[187] J S Kil M G Kim H M Choi et al ldquoInhibitory effects ofAngelicae GigantisRadix on osteoclast formationrdquo PhytotherapyResearch vol 22 no 4 pp 472ndash476 2008

[188] ANiranjan andD Prakash ldquoChemical constituents and biolog-ical activities of turmeric (Curcuma longa L) - a reviewrdquo Journalof Food Science and Technology vol 45 pp 109ndash116 2008

[189] K S Kim M G Choung and S H Park ldquoQuantitativedetermination and stability of curcuminoid pigments fromturmeric (Curcuma longaL) rootrdquo Korean Journal of CropScience vol 50 pp 211ndash215 2005

[190] I S Shin and J M Lee ldquoStudy on antimicrobial and antimuta-genic activity of horseradish (Wasabia japonica) root extractsrdquoJournal of the Korean Fisheries Society vol 31 pp 835ndash841 1998

[191] Y J ChoA study on the antioxidative and antimicrobial activitiesof wasabi (Wasabia koreana Cruciferae) extracts [PhD thesis]Sungshin Womens University Seoul Korea 2008

[192] A-S Kang T-S Kang H-R Shon et al ldquoStudies on improve-ment of artificial cultivation and antioxidative activity of Poriacocosrdquo The Korean Journal of Mycology vol 27 pp 378ndash3801999

[193] J-H Lee Y J Lee J-K Shin et al ldquoEffects of triterpenoidsfrom Poria cocos Wolf on the serotonin type 3A receptor-mediated ion current in Xenopus oocytesrdquo European Journal ofPharmacology vol 615 no 1ndash3 pp 27ndash32 2009

[194] K R Im M J Kim T K Jung and K S Yoon ldquoAnalysisof isoflavonoid contents in Astragalus membranaceus Bungecultivated in different areas and at various agesrdquo The KoreanSociety for Biotechnology and Bioengineering vol 25 pp 271ndash276 2010

Journal of Food Quality 31

[195] Y E Lee and S H Hong Oriental Medicine Food MaterialsKyomunsa Seoul Korea 2003

[196] D H Kim ldquoQuality characteristics of fish paste prepared withAstragalus membranaceus powderrdquo Food Engineering Progressvol 15 pp 362ndash369 2011

[197] S-E Kim B S Hwang J-G Song S W Lee I-K Lee andB-S Yun ldquoNew bioactive compounds from Korean nativemushroomsrdquoMycobiology vol 41 no 4 pp 171ndash176 2013

[198] National Institute of Agricultural Science The Mushrooms inKorea Dongbang Media Co Ltd Seoul Korea 2004

[199] Y-J Gao M Zhang and W-P Chen ldquoStudy on processing offish paste with waste of grass carprdquo Journal of Food Science andBiotechnology vol 31 pp 1031ndash1038 2012

[200] S Tolasa C M Lee and S Cakli ldquoPhysical and oxidativestabilization of omega-3 fatty acids in surimi gelsrdquo Journal ofFood Science vol 75 no 3 pp C305ndashC310 2010

[201] B N Pietrowski R Tahergorabi K E Matak J C Tou andJ Jaczynski ldquoChemical properties of surimi seafood nutrifiedwith 120596-3 rich oilsrdquo Food Chemistry vol 129 no 3 pp 912ndash9192011

[202] S H Kim J L Yang and Y S Song ldquoPhysiological function ofcheonggukjangrdquo Food Industry and Nutrition vol 4 pp 40ndash461999

[203] R Walker ldquoToxicology of sorbic acid and sorbatesrdquo Food Addi-tives amp Contaminants Part A vol 7 no 5 pp 671ndash676 1990

[204] B R Thakur and T R Patel ldquoSorbates in fish and fish productsmdasha reviewrdquo Food Reviews International vol 10 no 1 pp 93ndash1071994

[205] C-Y Wang H-W Huang C-P Hsu and B B Yang ldquoRecentadvances in food processing using high hydrostatic pressuretechnologyrdquo Critical Reviews in Food Science and Nutrition vol56 no 4 pp 527ndash540 2016

[206] J H Kwon M W Byun and J S Kim ldquoMicrobiological andorganoleptic qualities of boiled-dried anchovies during post-irradiation periodrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 25 pp 283ndash287 1996

[207] J Noh and J H Kwon ldquoThe quality and thermoluminescenceproperties of dried pollack during storage following irradia-tionrdquo Korean Journal of Food Science and Technology vol 36pp 711ndash716 2004

[208] I Tukenmez M S Ersen A T Bakioglu A Bicer and VPamuk ldquoDose dependent oxidation kinetics of lipids in fish dur-ing irradiation processingrdquo Radiation Physics and Chemistryvol 50 no 4 pp 407ndash414 1997

[209] T Sakai and T Yamaguchi ldquoEffects of yuzu peel addition onthe lipid oxidation in kamaboko Effects of yuzu peel additionon the lipid oxidation in kamabokordquo Bulletin of the Faculty ofAgriculture Miyazaki University vol 57 pp 101-102 2011

[210] E-H Lee K-S Oh J-G Koo H-S Park S-Y Cho and Y-J Cha ldquoStudies on processing and keeping quality of retortpouched foods (3) Preparation and keeping quality of retortpouched fried mackerel meat pasterdquo Bulletin of the KoreanFisheries Society vol 17 pp 373ndash382 1984

[211] J-H Ha E-H Lee J-S Kim S-G Ji and J-G Koo ldquoA study onthe thermal treatment conditions of retort pouched fried fish-paste 1 Influence of thermal treatment conditions on qualityrdquoBulletin of the Korean Fisheries Society vol 20 pp 573ndash581 1987

[212] P Guenneugues and J Ianelli ldquoSurimi resources and marketrdquoin Surimi and surimi seafood J W Park Ed pp 25ndash53 MarcelDekker Inc New York NY USA 2013

Research ArticleDevelopment of a Chemically Defined Medium forBetter Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31

Wenli Liu12 Lanwei Zhang23 and Huaxi Yi3

1College of Chemistry and Environmental Engineering Shenzhen University Shenzhen Guangdong 518060 China2School of Food Science amp Technology Harbin Institute of Technology 73 HuangHe Avenue Harbin Heilongjiang 150090 China3College of Food Science and Engineering Ocean University of China Yushan Road 5 Qingdao Shandong 266100 China

Correspondence should be addressed to Lanwei Zhang zhanglwhiteducn and Huaxi Yi yihxouceducn

Received 31 March 2017 Revised 17 July 2017 Accepted 2 August 2017 Published 6 September 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Wenli Liu et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The macro- and micronutrients in traditional medium such as MRS used for cultivating lactic acid bacteria especially forbacteriocin production have not been defined preventing the quantitative monitoring of metabolic flux during bacteriocinbiosynthesis To enhance Enterocin Y31 production and simplify steps of separation and purification we developed a simplifiedchemically definedmedium (SDM) for the growth of Enterococcus faeciumY31 and production of its bacteriocin Enterocin Y31Wefound that the bacterial growthwas unrelated toEnterocinY31 production inMRS therefore both the growth rate and theEnterocinY31 production were set as the index for investigation Single omission experiments revealed that 5 gL NaCl five vitamins twonucleic acid basesMgSO

4sdot7H2OMnSO

4sdot4H2OKH

2PO4 K2HPO4 CH3COONa fourteen amino acids and glucosewere essential

for the strainrsquos growth and Enterocin Y31 production Thus a novel simplified and defined medium (SDM) was formulated with30 components in total Consequently Enterocin Y31 production yield was higher in SDM as compared to either MRS or CDMSDM improved the Enterocin Y31 production and simplified the steps of purification (only two steps) which has broad potentialapplications

1 Introduction

Bacteriocins are ribosomally synthesised antimicrobial pro-teins or protein complexes that inhibit other bacteria andthey either have a narrow antimicrobial spectrum (againstthe same species) or broad antimicrobial spectrum (againstacross genera) [1 2] Bacteriocin produced by lactic acidbacteria (LAB) is generally regarded as safe (GRAS) andQualified Presumption of Safety (QPS) status [3 4] andit is a desirable trait as a food additive for extending theshelf-life of the fermented food and controlling the safetyof foods [5 6] Based on their molecular structure bac-teriocins can be divided into four groups class I bacte-riocins contain posttranslational modifications (lantibioticsand molecular weight le 5 kDa) class II bacteriocins areunmodified and include small heat-stable nonlanthionine-containing peptides [7] The third class includes large

heat-labile bacteriocins Finally the fourth class comprisescomplex bacteriocins containing a protein moiety with oneor more other lipids or carbohydrates [8] Most bacteriocinsproduced by the Enterococcus faecium group of LAB are classII bacteriocins One subgroup class IIa contains bacteriocinswith certain sequence motifs in their N-terminal halves andis active against the food pathogen Listeria monocytogenes[9] Class IIa bacteriocins have become a focus of researchowing to their low molecular weight good dispersity andhigh thermostability This is also a case of Enterocin Y31produced by E faecium Y31 in the current work [10]

Enterocin Y31 is a class IIa bacteriocin produced byE faecium Y31 [11] Previous research results showed thatEnterocin Y31 had broad spectrum inhibition activity againstBacillus subtilis ATCC 6633 Escherichia coli ATCC 25922Listeria monocytogenes ATCC 19111 Bacillus cereus CICC20463 Staphylococcus aureus and Salmonella enterica serovar

HindawiJournal of Food QualityVolume 2017 Article ID 9017452 8 pageshttpsdoiorg10115520179017452

2 Journal of Food Quality

TyphimuriumATCC 14028The isoelectric point of EnterocinY31 was 825 it was stable in both acidity and alkalescenceconditions hence Enterocin Y31 has a broad applicationprospect (not published) However two main drawbacks ofEnterocin Y31 with regard to application in foods are asfollows (1) bacteriocins are secreted in very small quan-tities in the production media and (2) the media used togrow the bacteriocin-producing strains are very complex[12] as the LAB are fastidious organisms requiring aminoacids B vitamins and various minerals for their growthThese components are normally provided by sources such assoybean meal yeast extract and meat extract All of thesesources contain proteins and peptides as sources of aminoacids which are often very closely related to the bacteriocinproduced Therefore purification of bacteriocin from sucha complex medium requires a series of steps At each stepthere is some loss and sometimes after the final purificationthe antimicrobial activity may be completely lost Complexmedia do not allow the examination of all individual mediumfactors [13 14] affecting bacteriocin production

Ricciardi reported a modified chemically defined med-ium to promote the growth of Lactobacillus casei and Lacto-bacillus plantarum groups [15] In the present study weimproved the chemically defined medium to improve theyield of Enterocin Y31 produced by E faecium Y31 Thereare four objectives of this study (1) to develop a newand improved production method for Enterocin Y31 (pro-duced by E faecium Y31) (2) to determine the macro- andmicronutrients necessary for cultivating E faecium Y31 andimproving Enterocin Y31 production (3) to develop a noveland simple separation and purificationmethod for EnterocinY31 (avoiding a series of chromatography steps and the lossof Enterocin Y31 activity) and (4) to compare Enterocin Y31production in a defined medium with that in a complexmediumThis is feasible using a completely defined mediumand a minimal medium for bacteriocin production can thusbe established

2 Materials and Methods

21 Strains and Growth Conditions The bacteriocin-pro-ducer strain E faecium Y31 isolated from Chinese traditionalfermented foods (fermented vegetable juice from Lanzhou)was previously found to produce class IIa bacteriocin [10]which wasmaintained as stock cultures inMRSmediumwith18 glycerol at minus80∘C

Escherichia coli ATCC 25922 was selected as a sensitivestrain for antimicrobial activity assays because the bacte-riocin produced by E faecium Y31 has the highest activityagainst E coli ATCC 25922 in gram-negative bacteria

22 Medium The growth of E faecium Y31 and productionof Enterocin Y31 in a defined medium in a fermenter werecompared with those in MRS (reference medium) used forthe optimisation of the growth of E faecium Y31 and theproduction of Enterocin Y31 This medium CDM consistedof 44 components described by Khan et al [12] (listed inTable 1) All chemicals used for the preparation of the definedmedium were of analytical grade and obtained from either

Sigma-Aldrich (St Louis MO USA) or BDH ChemicalsLtd (Poole UK) For all the experiments aqueous stocksolutions of the individual components were prepared inthe appropriate concentrations and sterilized by autoclav-ing with the exception of the heat-sensitive componentsThe heat-sensitive amino acids (asparagine glutamine andtryptophan) all of the B vitamins and FeSO

4were filter-

sterilized (pore size 022120583m membrane Millipore CorpBillerica MA USA) All the stock solutions were then storedat 4∘C except FeSO

4which was freshly prepared before each

experiment because it is prone to oxidation during storage Inaddition to the defined medium MRS medium was used asa reference for comparison with the defined medium beforeeach experiment

23 Determination of the Antimicrobial Activity of EnterocinY31 The antimicrobial activity of bacteriocin was monitoredusing the agar well diffusion assay (AWDA) as describedpreviously [16] with some modifications E faecium Y31 wascultured for two or three generations and then the cell-free supernatants (CFSs) of E faecium Y31 were preparedby centrifuging for 30min at 10000timesg Aliquots (80 120583L) ofthe cell-free supernatants (CFSs) of E faecium Y31 wereadded to the wells (6mm diameter) on double-layer agarplates previously inoculated with 02mL overnight cultureof the indicator strain E coli ATCC 25922 Plates were keptstatic at room temperature for 3 h to allow diffusion of theCFSs evenly in the agar and then the plates were incubatedfor 24 h at 37∘C The bacteriocin titre was determined byeliminating the effect of the organic acid eliminating theeffect of H

2O2 and protease verificationThe diameter of the

zone of inhibition (not including the wells) was measuredusing a Vernier caliper An arbitrary unit (AUmL) wasdefined as the reciprocal of the highest dilution that producedan inhibition zone Specific activity was expressed as that unitper milligram of protein

24 Protein Concentration Determination Protein concen-tration was determined by the BCA (bicinchoninic acid)microassay method (Pierce Rockford IL USA) [17]

25 Monitoring of the Growth of E faecium Y31 The ODvalue of the fermentation liquid of E faecium Y31 wasmonitored with UV spectrophotometry at 600 nm each hourSterile culture medium was used as blanks to subtract thebackground value Samples having an OD600 nm value ofmore than 07 were diluted with the sterile culture mediumand the corrected OD value was obtained by multiplying thedilution factor ODmax (600 nm) represents the maximumOD value of the growth of E faecium Y31 ODmax (600 nm)was calculated before any centrifugation

26 Determination of the Relative Growth Rate The relativegrowth rate was calculated according to Monod [18] Thefollowing equation was used to calculate the growth rate

120583 = [(lnOD2minus lnOD

1) divide (1199052minus 1199051)] divide 120583CDM (1)

where 120583 is the relative growth rate (hminus1) ln is the symbol fornatural logarithm and OD

1and OD

2are the corrected OD

Journal of Food Quality 3

Table 1 Composition of CDM and SDMmedium

Constituent ContentCDM SDM

Amino acids (g Lminus1)L-Asparagine 100 100L-Aspartic acid 100 mdashL-Glutamic acid 100 100L -Glutamine 100 mdashL-Cys 100 100L-Alanine 100 mdashL-Arginine 100 100Glycine 100 100L-Histidine 100 100L-Isoleucine 100 100L-Leucine 100 100L-Lysine 100 100L-Methionine 100 100L-Phenylalanine 100 100L-Proline 100 mdashL-Serine 100 100L-Threonine 100 100L-Tryptophan 100 100L-Tyrosine 100 mdashL-Valine 100 mdash

Nucleic acid bases (g Lminus1)AdemomeSO

4002 002

Guanine 002 mdashInosine 002 mdashXanthine 002 mdashUracil 002 002Thymine 002 mdashOrotic acid 002 mdash

B vitamins (mgsdotLminus1)Biotin 2000 2000Para-aminobenzoic acid 1000 mdashNicotinic acid 200 200Ca-pantothenic acid 2000 2000Riboflavin 200 200Folic acid 200 200Cyanocobalamin 200 mdashThiamine 1000 mdashPyridoxal 2000 mdash

Minerals (gsdotLminus1)Manganese sulfate 005 005Magnesium sulfate 01 010Ferrous sulfate7H

2O 002 mdash

CaCl2

mdash mdashSodium citrate 500 500Potassium dihydrogen phosphate 200 200Dipotassium hydrogen phosphate 700 700

Table 1 Continued

Constituent ContentCDM SDM

Carbon source (gsdotLminus1)Glucose 1500 1500

Others (gsdotLminus1)Tween 80 100 100Glycerol mdash mdashNaCl mdash 500

27 Effects of NaCl CaCl2 and Glycerol on the Growth of Efaecium Y31 and Enterocin Y31 Production To determine theeffects of these components 5 gL 10 gL 15 gL and 20 gLNaCl 10 gL CaCl

2 and 50 gL glycerol were individually

added to 1000mLCDM andCDMmediumwith no addtionswas used as a control wherein the inoculum size was 2fermentation temperature was 37∘C and inoculum time was24 h The culturing liquid was then centrifuged for 20minat 10000timesg and then the CFSs were used to determineEnterocin Y31 activity and ODmax (24 h)

28 Effects of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth ofE faecium Y31 and Enterocin Y31 Production According tothe Leave One Out (LOO) technique each amino acid Bvitamin mineral and nucleic acid base was sequentially andindividually omitted from 1000mLCDMmedium andCDMwithout additions was used as a control The inoculum sizewas 2 fermentation temperature was 37∘C and inoculationtime was 24 h The culture liquid was then centrifugedfor 20min at 10000timesg and then the CFSs were used todetermine Enterocin Y31 activity and ODmax (24 h)

The following terms were used to describe the rela-tionship between each medium component and growth asdetermined by the single omission technique A constituentwas considered essential if its omission resulted in less thanhalf the maximum strain growth rate and production ofbacteriocin of the positive control stimulatory when itsabsence resulted in the fact that the growth rate and thebacteriocin production was between 50 and 80 of thatobserved in complete CDM and nonessential if the growthrate and Enterocin Y31 production was 80 (or more) of thatobtained in the complete CDM

29 Purification of Enterocin Y31 E faecium Y31 was allowedto grow in the SDM (Table 1) for 24 h The cells were thenremoved by centrifugation (11800timesg 25min) The CFSswere then filtered through a 022 120583m filter (low-protein-binding HVLP filter Millipore Corp) to remove any remain-ing cells These filtered CFSs were referred to as crude bacte-riocin The crude bacteriocin was subjected to ultrafiltrationof 1 kDa and 30 kDa The retentate from the 1 kDa step wasthen subjected to Tricine-SDS-PAGE

210 Statistical Analyses All experiments were preformedseparately three times and mean plusmn standard deviation (SD)values were calculated from triplicate determinations All

4 Journal of Food Quality

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 320002

0604

081012141618202224

ODpHInhibition zone diameter (mm)

Time (h)

OD

35404550556065707580

pH

0

2

4

6

8

10

12

14

Inhi

bitio

n zo

ne (

mm

)

Figure 1 Relationship between the growth of the bacteriocinogenicstrain and Enterocin Y31 production

data were subjected to one-way analysis of variance (one-way ANOVA) Comparison of means was performed withDuncanrsquos multiple range tests Statistical significance was setat 119875 lt 005

3 Results and Discussion

31 Relationship between the Growth of the Strain andEnterocin Y31 Activity The growth of E faecium Y31 wasunrelated to EnterocinY31 activity inMRSmedium as shownin Figure 1 The result was consistent with the result ofBacterocin J23 produced by Lactobacillus paracasei J23 asdescribed by Huaxi Yi in our research group (not published)whichwas inconsistentwith the result of Salivaricin producedby L salivarius CRL 1328 [19] thus the growth rate of EfaeciumY31 and Enterocin Y31 activity were used as detectionindexes for developing a novel chemical defined mediumEnterocin Y31 activity could be detected at the exponentialphase of the producing strain (9 h) and reached its highestvalue of 1126 plusmn 036mm at stationary phase of producingstrain (24 h) ODmax remained stable at 16 h of fermentationof strain Y31 thus ODmax (16 h) was used as an index of thestrain growth status

32 Effect of NaCl Concentration on the Growth of E faeciumY31 and Enterocin Y31 Production Theeffect of NaCl at 5 gL10 gL 15 gL and 20 gL was determined in CDMwith CDMwith no additives as the control The results indicated thatthe growth of E faecium Y31 and production of EnterocinY31 were not significant difference when adding 5 gL or10 gL NaCl and 0 gL and 15 gL NaCl had no effect onthe growth of strain Y31 and production of Enterocin Y31When the concentration of NaCl was 20 the growth of Efaecium Y31 and production of Enterocin Y31 reduced whichshowed the significant difference when compared to 0 gLand 15 gL NaCl We can conclude that 20 gL NaCl have anegative effect on the growth of strain Y31 and the productionof Enterocin Y31 When the adding concentration of NaClwas 5 gL the ODmax (16 h) of E faecium Y31 was highest

150

155

160

165

170

175

180

Enterocin Y31 production (AUmg protein)

CDM

(con

trol)

bc c

bc

ab

a

b b bab

a

GR

(16B

)

ODmax (16 B)

10A

L N

aCl

15A

L N

aCl

20A

L N

aCl

5A

L N

aCl 0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 2 Effect of NaCl concentration on the growth of Enterococ-cus faecium Y31 and Enterocin Y31 production Means not sharing acommon superscript letter are significantly different fromeach other(119875 lt 005)

172 plusmn 001 and the antibacterial activity also reached themaximum value 128364 plusmn 4140AUmg protein Based thesignificant difference analysis we could conclude that 5 gLNaCl stimulated the growth of strain Y31 (119875 lt 005) andhad no effect on the production of Enterocin Y31 (Figure 2)Similar results have been reported in a study of nutritionalrequirements of L salivarius CRL 1328 producing Salivaricin[19] Considering that the condition for the growth of Efaecium Y31 was crucial 5 gL NaCl was added to the novelchemically defined medium SDM (the medium ingredientsof SDM were listed in Table 1)

33 Effect of CaCl2 and Glycerol on the Growth of E faeciumY31 and Enterocin Y31 Production The results shown inTable 2 indicated that adding 10 gL CaCl

2to CDM had no

effect on the growth of E faecium Y31 but had a negativeeffect on the production of Enterocin Y31 (119875 lt 005) whereasadding 50 gL glycerol had a slight negative effect on thegrowth of E faecium Y31 (119875 lt 005) and a negative influenceon Enterocin Y31 production (119875 lt 005)

34 Effect of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth of Efaecium Y31 and Enterocin Y31 Production According to theLeaveOneOut (LOO) technique each amino acid B vitaminmineral and nucleic acid base was sequentially omitted ina series of prepared formulations along with CDM as acontrol The results shown in Table 3 indicated that L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser and L-Cys areessential amino acids which had an effect on the growth ofE faecium Y31 and Enterocin Y31 production and the stim-ulatory amino acids mainly included L-Asn L-Glu L-Iso L-Lys and L-Try Omitting the stimulatory amino acids resultedin the slow growth of E faecium Y31 and low production

Journal of Food Quality 5

Table 2 Effects of CaCl2and glycerol on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Added components ODmax (600 nm) after 16 h Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003b 124224 plusmn 4141c

10 gL CaCl2

170 plusmn 002b 28986 plusmn 4141a

50 gL glycerol 153 plusmn 003a 56591 plusmn 4181b

Note CDM is explained in Table 1 and means in the same row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

Table 3 Effect of omitting a single amino acid on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Omitted amino acid ODmax (16 h) Relative growth rate Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003h 100 124224 plusmn 4141cd

L-Ala 150 plusmn 005g 90 122843 plusmn 6325cd

L-Arg 076 plusmn 002c ng mdasha

L-Asp 143 plusmn 004g 93 117322 plusmn 6325cd

L-Asn 091 plusmn 003d 60 122843 plusmn 8225cd

L-Cys 100 plusmn 004de 44 mdasha

L-Glu 152 plusmn 004g 72 110420 plusmn 2391c

L-Gln 171 plusmn 004h 84 124224 plusmn 5686d

L-Gly 061 plusmn 003ab ng mdasha

L-His 066 plusmn 003bc ng mdasha

L-Iso 106 plusmn 004ef 79 66252 plusmn 8251b

L-Leu 071 plusmn 003bc ng mdasha

L-Lys 116 plusmn 004f 80 62111 plusmn 4140b

L-Met 053 plusmn 002a ng mdasha

L-Phe 077 plusmn 002c ng mdasha

L-Pro 181 plusmn 003h 71 110420 plusmn 6545cd

L-Ser 049 plusmn 003a ng mdasha

L-Thr 068 plusmn 002bc ng mdasha

L-Try 112 plusmn 003ef 80 57322 plusmn 2391b

L-Tyr 170 plusmn 007h 100 120082 plusmn 3487cd

L-Val 196 plusmn 008i 98 122843 plusmn 6582cd

Note ldquongrdquo represents that the strain did not grow and ldquomdashrdquo represents that there was no inhibition activity CDM is explained in Table 1 and means in thesame row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

of Enterocin Y31 Therefore the essential amino acids andstimulatory amino acids were included in the SDM (listedin Table 1) A previous study reported the similar results asZhang et al found that six amino acids (arginine histidineisoleucine leucine methionine and valine) were necessaryfor the lactococci enterococci and streptococci [20]

Pyridoxal and pantothenic acid are essential B vitaminswhich had an effect on the growth of E faeciumY31 and Ente-rocin Y31 production and the stimulatory B vitamins mainlyincluded niacin and riboflavin Wherein the stimulatory Bvitamins could not result in the growth arrest of E faeciumY31 and the biosynthesis arrest of Enterocin Y31 they couldcause low growth rate and low biosynthesis volume There-fore the essential and stimulatory B vitamins were neededin the SDM Omitting folic acid would cause a reduction of80 in the ODmax (16 h) of E faecium Y31 therefore folicacid is also needed for the growth of E faecium Y31 and theproduction of Enterocin Y31 (Figure 3) It has been reported

that nutritional requirements of L delbrueckii ssp lactis CRL581 growthwere nicotinic acid and pyridoxal and pantothenicacid whereas the growth of L delbrueckii ssp lactis CRL654 requires niacin and pantothenic acid and riboflavinand cyanocobalamin were found to be stimulatory for bothstrains [21] Research results about S thermophilus strains(ST1 ST7 ST8 ST11 ST18 and ST21) indicated that riboflavinwas essential for the growth of all strains whereas Ca-pantothenic acid and nicotinic acid were also required [22]

In the present study MgSO4sdot7H2O was an essential min-

eral andMnSO4sdot4H2OKH

2PO4 K

2HPO4 andCH

3COONa

were stimulatory minerals which had an effect on the growthof E faecium Y31 and Enterocin Y31 production (Figure 4)The necessity of magnesium and phosphate has previouslybeen reported by other researchers for various LAB species[20 23 24]

Adenine and uracil are stimulatory nucleic acids whichhad an effect on the growth of E faecium Y31 and Enterocin

6 Journal of Food Quality

Non

e (CD

M)

Pyrid

oxal

Thia

min

e

Nia

cin

D-B

iotin

Ribo

flavi

n

Cyan

ocob

alam

in

Folic

acid

p-A

min

oben

zoic

acid

Pant

othe

nic a

cid

02040608101214161820

Omitted vitamins

f

b

f

c

f

d

e ef

a

d

b

d

b

ccd

cdcd

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 3 Effect of individually omitting each B vitamin on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Y31 production (Figure 5) No nucleic acid was essential forthe growth of E faecium Y31 and Enterocin Y31 production

35 Comparison of Enterocin Y31 Production onMRSMediumand SDM A novel chemical defined medium (SDM) wasdeveloped (Table 1 and Figures 3 4 and 5) and SDMcontainedNaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

and uracil Strain Y31 grew better on SDM than on MRSmedium (Figure 6) As shown in Figure 7 Enterocin Y31production on SDM was 16 times than that on MRS

36 Purification and Characterization of Enterocin Y31 Afterthe removal of cells from the defined medium the cell-free supernatant was subjected to ultrafiltration through a30 kDa ultrafiltration membrane The active permeate liquorwas then subjected to a second ultrafiltration step using a1 kDa NMWL The antimicrobial activity was again foundin the retentate (10240AUL) Enterocin Y31 was purified byTricine-SDS-PAGE and its molecular weight was 674 kDa(showed in Figure 8)

4 Conclusion

When culturing E faecium Y31 using novel chemical definedmedium (SDM) Enterocin Y31 production increased 16times than that on MRS The ingredients were composedof NaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-ThrL-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

Non

e (CD

M)

Am

mon

ium

citr

ate d

ibas

ic

MnS

O4 middot 4

H2O

MgS

O4 middot 7

H2O

KH2P

O4

K2H

PO4

Sodi

um ac

etat

e

0204060810121416182022

Omitted minerals

d d

b

a

b

c ce e

b

a

c

d d

Enterocin Y31 production (AUmg protein)$

GR

(16B

)$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

Figure 4 Effect of individually omitting each a mineral on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Non

e (CD

M)

Aden

ine

Gua

nine

Inos

ine

Xant

hine

Oro

tic ac

id

Ura

cil

Thym

ine

14

15

16

17

18

19

20

Omitted nucleic acid bases

d

a

c

d d d

b

d

d

abbc

d d d

a

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

Figure 5 Effect of individually omitting each a nucleic acid baseon the growth of Enterococcus faecium Y31 and Enterocin Y31production Means not sharing a common superscript letter aresignificantly different from each other (119875 lt 005)

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

uracil and glucose which were the macro- and micronu-trients needed by biosynthesis of Enterocin Y31 SDM washelpful to the growth of E faecium Y31 and EnterocinY31 production improvement In addition SDM avoided aseries of chromatography steps and the loss of Enterocin Y31

Journal of Food Quality 7

0 5 10 15 20 25 30 3500020406081012141618202224

Time (h)

SDMMRS

GR

(16B

)

Figure 6 Growth of Enterococcus faecium Y31 on MRS and SDM

0 5 10 15 20 25 30 3502468

10121416182022

Time (h)

Inhi

bitio

n zo

ne d

iam

eter

(mm

)

SDMMRS

Figure 7 Enterocin Y31 productions on MRS and SDM

Enterocin Y31

M 140 +$

30+$

20 +$

10 +$

46 +$

17 +$

Figure 8 Tricine-SDS-PAGE of Enterocin Y31 M protein marker1 Enterocin Y31

activity only two steps of ultrafiltration and Tricine-SDS-PAGE were needed to separate and purify Enterocin Y31Therefore chemically defined medium has better potentialfor improving the bacteriocin production and reducing thesteps of separation and purification Chemically definedmedia is useful for purification of not only large bacteriocinssuch as Enterocin Y31 but also small peptide bacteriocinsThe alternative use of a chemically defined medium meetsthe nutritional requirements of strains producing bacteri-ocins and therefore is an excellent alternative to reduce theload of contaminating peptides from the medium therebydecreasing the purification steps To our knowledge no suchstudies have been conducted to improve class IIa bacteriocinEnterocin Y31 production and purify Enterocin Y31

Ethical Approval

This study complies with the research ethics guidelines and itdoes not contain any studies with human or animal subjects

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article

Acknowledgments

This work was financially supported by the 60th Finan-cial Grant from China Postdoctoral Science Foundation(Grant no 2016M602534) the Youth Innovation TalentsProject of General Higher School in Guangdong Province(2016KQNCX144) and theNationalNatural Science Founda-tion of China (Grants nos 31571850 31771988 and 31701621)

References

[1] R C R Martinez M Wachsman N I Torres J G LeBlancS D Todorov and B D G D M Franco ldquoBiochemical anti-microbial and molecular characterization of a noncytotoxicbacteriocin produced by Lactobacillus plantarum ST71KSrdquo FoodMicrobiology vol 34 no 2 pp 376ndash381 2013

[2] I M Aasen T Moslashretroslash T Katla L Axelsson and I StorroslashldquoInfluence of complex nutrients temperature and pH on bacte-riocin production by Lactobacillus sakei CCUG 42687rdquo AppliedMicrobiology andBiotechnology vol 53 no 2 pp 159ndash166 2000

[3] P Alvarez-Sieiro M Montalban-Lopez D Mu and O PKuipers ldquoBacteriocins of lactic acid bacteria extending thefamilyrdquo Applied microbiology and biotechnology vol 100 no 7pp 2939ndash2951 2016

[4] F A C Martinez E M Balciunas A Converti P D Cotterand R P De Souza Oliveira ldquoBacteriocin production by Bifido-bacterium spp A reviewrdquo Biotechnology Advances vol 31 no 4pp 482ndash488 2013

[5] E F OrsquoShea P D Cotter R P Ross and C Hill ldquoStrategiesto improve the bacteriocin protection provided by lactic acidbacteriardquo Current Opinion in Biotechnology vol 24 no 2 pp130ndash134 2013

[6] A-M Zouhir E Kheadr I Tahiri J Ben Hamida and IFliss ldquoCombination with plant extracts improves the inhibitoryaction of divergicin m35 against Listeria monocytogenesrdquo Jour-nal of Food Quality vol 31 no 1 pp 13ndash33 2008

8 Journal of Food Quality

[7] J Pei Y Yuan and T Yue ldquoPrimary characterization of bacteri-ocin paracin C - A novel bacteriocin produced by Lactobacillusparacaseirdquo Food Control vol 34 no 1 pp 168ndash176 2013

[8] D Drider and S Rebuffat ldquoClassification of Bacteriocins fromGram-Positive Bacteriardquo in Prokaryotic Antimicrobial Peptidespp 29ndash53 Springer New York NY USA 2011

[9] T Aymerich H Holo L S Havarstein M Hugas M Garrigaand I F Nes ldquoBiochemical and genetic characterization of ente-rocin A from Enterococcus faecium a new antilisterial bac-teriocin in the pediocin family of bacteriocinsrdquo Applied andEnvironmental Microbiology vol 62 no 5 pp 1676ndash1682 1996

[10] W Liu L Zhang H Yi et al ldquoQualitative detection of class IIabacteriocinogenic lactic acid bacteria from traditional Chinesefermented food using a YGNGV-motif-based assayrdquo Journal ofMicrobiological Methods vol 100 no 1 pp 121ndash127 2014

[11] W Liu L Zhang J Shi et al ldquoAssessment of the safety and appli-cations of bacteriocinogenic Enterococcus faecium Y31 as anadjunct culture in North-eastern Chinese traditional fermen-tation paocairdquo Food Control vol 50 pp 637ndash644 2015

[12] H Khan S H Flint and P-L Yu ldquoDevelopment of a chemicallydefined medium for the production of enterolysin A fromEnterococcus faecalis B9510rdquo Journal of Applied Microbiologyvol 114 no 4 pp 1092ndash1102 2013

[13] M Silva d M Andrade d S A Bauermeister et al ldquoA SimpleDefined Medium for the Production of True Diketopiperazinesin Xylella Fastidiosa and Their Identification by Ultra-FastLiquidChromatography-Electrospray Ionization IonTrapMassSpectrometryrdquoMolecules vol 22 no 6 p 985 2017

[14] E Texeira J Checa A Rıal et al ldquoA New Chemically DefinedMedium for Cultivation of Streptococcus Pneumoniae SerotyperdquoJournal of Biotech Research vol 6 p 54 2015

[15] A Ricciardi R G Ianniello E Parente and T Zotta ldquoModifiedchemically definedmedium for enhanced respiratory growth ofLactobacillus casei and Lactobacillus plantarum groupsrdquo Journalof Applied Microbiology vol 119 no 3 pp 776ndash785 2015

[16] U Schillinger and K Lucke F ldquoAntibacterial activity of Lacto-bacillus sake isolated from meatrdquo Applied and EnvironmentalMicrobiology vol 55 no 8 pp 1901ndash1906 1989

[17] P K Smith R I Krohn G Hermanson et al ldquoMeasurement ofprotein using bicinchoninic acidrdquo Analytical biochemistry vol150 no 1 pp 76ndash85 1985

[18] J Monod ldquoThe Growth of Bacterial Culturesrdquo Annual Reviewsin Microbiology vol 3 no 1 pp 371ndash394 1949

[19] E V Pingitore EMHebert F Sesma andM E Nader-MacıasldquoInfluence of vitamins and osmolites on growth and bacteriocinproduction by Lactobacillus salivarius CRL 1328 in a chemicallydefinedmediumrdquoCanadian Journal of Microbiology vol 55 no3 pp 304ndash310 2009

[20] G Zhang D AMills and D E Block ldquoDevelopment of chemi-cally defined media supporting high-cell-density growth ofLactococci Enterococci and Streptococcirdquo Applied and Environ-mental Microbiology vol 75 no 4 pp 1080ndash1087 2009

[21] E M Hebert R R Raya and G S De Giori ldquoNutritionalrequirements of Lactobacillus delbrueckii subsp lactis in achemically defined mediumrdquo Current Microbiology vol 49 no5 pp 341ndash345 2004

[22] C Letort and V Juillard ldquoDevelopment of a minimal chemi-cally-defined medium for the exponential growth of Streptococ-cus thermophilusrdquo Journal of AppliedMicrobiology vol 91 no 6pp 1023ndash1029 2001

[23] N Terrade and R Mira de Orduna ldquoDetermination of theessential nutrient requirements of wine-related bacteria fromthe genera Oenococcus and Lactobacillusrdquo International Journalof Food Microbiology vol 133 no 1-2 pp 8ndash13 2009

[24] F M Saguir and M C M De Nadra ldquoImprovement of a chem-ically definedmedium for the sustained growth of Lactobacillusplantarum nutritional requirementsrdquo Current Microbiologyvol 54 no 6 pp 414ndash418 2007

Research ArticleLipid Oxidation Color Changes and MicrobiologicalQuality of Frozen Beef Burgers Incorporated with ShiraziThyme Cinnamon and Rosemary Extracts

Hadi Hashemi Gahruie Seyed Mohammad HashemHosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan Shad

Department of Food Science and Technology School of Agriculture Shiraz University Shiraz Iran

Correspondence should be addressed to Mohammad Hadi Eskandari eskandarshirazuacir

Received 3 January 2017 Revised 17 March 2017 Accepted 11 April 2017 Published 21 May 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Hadi Hashemi Gahruie et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In this study the oxidative stability of beef burgers incorporated with Shirazi thyme cinnamon and rosemary extracts wascompared with that of BHT-incorporated and antioxidant-free samples The chemical composition TBARS metmyoglobin pHcolor and microbial and sensory characteristics were evaluated during storage at minus18∘C for 2 months The results indicated thatShirazi thyme and cinnamon extracts did not change the colorimetric properties significantly (119875 lt 005) Incorporating naturalantioxidants led to a significant (119875 lt 005) reduction in TBARS (3658ndash4634) and metmyoglobin (1625ndash1847) as compared tocontrol Except for the control sample total microbial counts of burgers were lower than the maximum allowed limit Burgersformulated with Shirazi thyme revealed the lowest amount of total count Regarding the sensory characteristics the overallacceptability of different samples decreased in the order of cinnamon gt BHT gt Shirazi thyme gt rosemary gt control Finally theresults showed that these plant extracts can be utilized as an alternative to synthetic antioxidants in formulation of burgers

1 Introduction

Meat and meat products are among the most importantprotein sources in the daily diet of people living in developedcountries Beef burger is almost the most popular meatproduct consumed by millions of people from all over theworld The common processes (such as mincing cookingand salt addition) applied in the production of burgersenhance the formation of reactive oxygen species thereforethe resultant product is highly vulnerable to oxidation [1]Lipid and protein oxidations have been reported as theprincipal reason for the decreased quality of burgers duringstorage resulting in decreasing the shelf life [2ndash4]

Application of antioxidants is the best strategy to pre-vent oxidation reactions [5] Synthetic antioxidants such asBHT TBHQ and BHA have various adverse human healtheffects including allergy headache asthma and dermatitis

Therefore the application of natural antioxidants (such asherbal essential oils and extracts) is of interest and canbe observed in a growing number of research works [6ndash8](Aliakbarlu et al 2016)Moreover consumers are increasinglydemanding for green-labeled food products such as thosecontaining natural antioxidant Natural compounds can beobtained from natural sources such as plants fruits vegeta-bles oil seeds spices team honey bee pollen and cereals[9] A lot of extracts have been approved as GRAS (GenerallyRecognized as Safe) that is the addition of these chemicals orsubstances into food is considered safe by experts and theirapplication is exempted from the usual Federal Food Drugand Cosmetic Act (FFDCA) [10]

The potential of natural antioxidants in preventing thelipid oxidation in different food products has been evaluatedby many researchers around the world [11] It has beenreported that the extracts of kinnow rind pomegranate rind

HindawiJournal of Food QualityVolume 2017 Article ID 6350156 9 pageshttpsdoiorg10115520176350156

2 Journal of Food Quality

Hamburger ingredients Extracts (20 g herb + 500 ml water)

Preparation of base batter

Formula 1without additives

(control)

Formula 2with BHT(100 ppm)

Formula 3with Shirazi thyme

(22 mlkg)

Formula 4with rosemary

(28 mlkg)

Formula 5with cinnamon

(73 mlkg)

Analysis (0 15 30 45 and 60 days)

Chemical analysis

Chemical compotation(i) Moisture

(ii) Protein(iii) Fat(iv) Carbohydrate(v) Ash

Deterioration criteria(i) TBARS

(ii) pH(iii) Metmyoglobin

Microbiological analysis(i) Total aerobic bacterial count

Sensory analysis(i) Appearance

(ii) Texture(iii) Taste(iv) Odor(v) Overall acceptance

Color analysis(i) Llowast

(ii) alowast

(iii) blowast

(iv) ΔE

Production and storage at minus18∘C

Figure 1 Schematic diagram of experimental design

and seed powders were significantly able to decrease the lipidoxidation in goat meat patties [12] The effects of natural(sage and rosemary) and synthetic (BHT) antioxidants onprotein oxidation discoloration and texture of refrigeratedpatties produced from pig liver have been studied by Estevezet al [13] Authors reported that the antioxidant propertiesof natural and synthetic antioxidants were similar In treatedsamples the increase in the carbonyl content as a result ofoxidation was significantly (P lt 005) lower than controlsamples Moreover antioxidants could successfully protectheme molecules from degradation Among different naturalantioxidants it has been reported that the extracts of Shirazithyme cinnamon and rosemary reveal substantial antioxi-dant capacity [14]

The main objective of the current study was to comparethe effects of Shirazi thyme cinnamon and rosemary extracts(denoted as natural antioxidants) with those of BHT on pro-tein and lipid oxidations and physicochemicalmicrobial andsensory characteristics of frozen beef burgers during storageThe results of this study may have potential implications

in substituting the synthetic antioxidants with nature-madeones

2 Materials and Methods

A schematic representation of beef burger production isshown in Figure 1

21 Materials Beef flanks (18 fat) from freshly slaughteredanimals (24 hours post slaughter)were purchased froma localmarket (Shiraz Iran) and transported to the laboratory ininsulated polystyrene ice-boxes The meat was ground (MeatGrinder Philips HR2743 AmsterdamNetherlands) througha perforated plate with a hole diameter of 5mm Thiobar-bituric acid (Sigma-Aldrich St Louis MO USA) 1133-tetraethoxypropane (Sigma-Aldrich St Louis MO USA)and diphenyl-2-picrylhydrazyl (DPPH∙) (Sigma-Aldrich StLouisMOUSA) soy protein isolate (SPI 90 protein SonicCo India) onions salt spices and ruskwere also used in thisstudy

Journal of Food Quality 3

22 Plant Extracts Shirazi thyme (Zatariamultiflora) cinna-mon (Cinnamomum zeylanicum) and rosemary (Rosmarinusofficinalis) were purchased from a local grocery The genusand species were certified by experts from the Herbariumof Biology Department (Shiraz University Shiraz Iran)Dried plants were powdered with a mill and then kept inpolyethylene bags at room temperature before extraction

221 Extract Preparation Plant powder (20 g) was thor-oughly mixed with boiling distilled water (500mL) for5min followed by filtration through Whatman grade No 1filter papers and concentration in rotary evaporator (BuchiRotavapor R Switzerland) at 50∘C [15]

222 DPPH Radical Scavenging Activity Antioxidant activ-ity of natural extracts and BHT was calculated using DPPHfree radicalmethod described by Cam et al [16]The amountsof extracts required to replace BHT were calculated basedon the IC50 of BHTThe required amounts of natural extractsshould have equal antioxidant activity to BHT

23 Beef Burger

231 Burger Preparation and Storage The formulation ofbeef burger used in this study was composed of beef (70)onions (134) rusk (4) water (8) SPI (3) salt (1)black (03) and red (02) peppers Ground meat saltwater and minced onion were mixed together After thatSPI was added and then mixed for 15min to obtain ahomogenousmixture Rusk and spices were added in the nextstep Finally natural extracts andor BHT were incorporatedinto the homogenate and thenmixing process was continuedThe concentration of BHT was 100 ppm A burger maker(9 cm internal diameter) was used to shape the mixture intopatties of approximately 90 g and 5mm thickness Burgers(15 patties per treatment) were then packed in light-resistantpolyethylene containers and frozen at minus18∘C Analyses wereperformed during 15-day intervals for two months Beforeanalysis the samples were thawed at +4∘C and then hand-mixed for 30 s

232 Chemical Analysis Moisture protein fat and ashcontents of burgers were determined according to the AOACmethods [17] Carbohydrate content was estimated by sub-tracting the total amounts of moisture protein fat and ashfrom 100

233 pH Measurement Meat sample (10 g) was homog-enized with 50mL deionized water for 1min pH wasmeasured at room temperature using a digital pH meter(Suntex TS-1 Taiwan) equipped with a probe-type combinedelectrode (Ingold) through direct immersion of electrode intothe mixture [17]

234 Instrumental Color Evaluation Color attributes of beefburgers were measured by 119871lowast119886lowast119887lowast method described byYam and Papadakis [18] The values of 119871lowast (brightness) 119886lowast(redness-greenness) and 119887lowast (yellowness-blueness) weremea-sured on the whole outer surfaces of beef burger A wooden

box (50 times 50 times 60 cm3) equipped with a natural daylightsource (6500K) and a digital camera (CanonPowershotA540of six megapixels resolution) in a vertical position and adistance of 25 cm from the samples was used for takingphotos Adobe PhotoshopCS6 was applied to determine theaverage surface color

235 Determination of Lipid Oxidation Lipid oxidationwas monitored by measuring thiobarbituric acid reactivesubstances (TBARS) Meat sample (4 g) was homogenizedwith 20mL trichloroacetic acid solution (20 wv) and thencentrifuged at 3000119892 for 10min The supernatant (2mL) wasmixed with 2mL thiobarbituric acid solution (01 wv indouble distillated water) followed by heating in a water bathat 100∘C for 30min and then cooling to room temperatureTherefore TBARS were extracted in chilled atmosphere Theabsorbance of each extract was measured at 520 nm in aspectrophotometer (spec 1650PC Shimadzu Japan) 1133-tetraethoxypropane was used to develop the standard curvefor TBARS assay TBARS values were reported as mg ofmalonaldehyde per kg of beef burger [7]

236 Metmyoglobin Measurement A modified method ofAn et al [19] was used to measure the metmyoglobincontent in raw beef burgers The sample (4 g) was mixedin a homogenizer with 20mL of phosphate buffer (004MpH 68) and then stored at 1∘C for 1 h The mixture wasthen centrifuged at 3500119892 and 4∘C for 30min Finally thesupernatant was filtered through Whatman grade No 1filter paper The absorbance of the solution was measuredat 525 572 and 700 nm Metmyoglobin () was calculatedaccording to the following equation

Metmyoglobin () = [1395 minus [(119860572 minus 119860700)(119860525 minus 119860700)]]times 100

(1)

Total Aerobic Bacterial Count Total aerobic bacteria werequantified every 15 days using the method described byAliakbarlu et al (2016) Beef burgers (10 g) were asepti-cally transferred into individual stomaching bags containing90mL of sterile saline (09) and homogenized for 2minSerial 10-fold dilutions were prepared in saline and 100 120583Lfrom appropriate dilutions was spread on the surface of platecount agar for total aerobic count (TMC) and then incubatedat 35∘C for 24 h

237 Sensory Evaluation Sensory analyses have been per-formed by 20 trained panelists from the Department of FoodScience and Technology (Shiraz University) Panelists wereboth male and female in the age range of 23ndash28 years oldPanelists were selected based on their previous experiences inconsuming traditional beef burgers Moreover they receivea preparatory session before the sensory test to train themhow to describe all evaluated factors completely Burgers werefried at 150∘C in a forced draft oven to a core temperatureof 72∘C and kept warm in the oven for 3ndash8min until thesensory testing [20] Rectangular pieces of approximately

4 Journal of Food Quality

2 cm were cut from the center of each burger and then servedat room temperature Each panelist randomly evaluated threepieces of all formulations and asked to give a numericalvalue between 1 and 9 for the following attributes taste 1(imperceptible) to 9 (extremely intense) texture attributesand juiciness 1 (extremely dry) to 9 (extremely moist)appearance 1 (extremely soft) to 9 (extremely tough) andodor 1 (imperceptible) to 9 (extremely intense) Tap waterwas provided for panelists to rinse their mouth betweendifferent samples At the end of evaluation each panelist wasasked to give an overall score from 1 (dislike very much) to9 (like very much) for the overall acceptability of differentformulations

24 Statistical Analysis A completely randomized blockdesign with five treatments (including antioxidant-free (con-trol) treatment and those incorporated with BHT cinnamonrosemary and Shirazi thyme extracts) was used in this studyExperiments were performed during a 60-day storage periodat 15-day intervals (0 15 30 45 and 60) Independent blocks(developed from three different batches) were replicatedthree times at each sampling point A two-way analysisof variance (ANOVA) and Duncanrsquos multiple range tests(SAS 80 software SAS Institute Inc Cary NC USA) wereperformed to analyze the effect of treatments storage periodand their interaction on the physicochemical microbial andsensory characteristics of beef burgers at a confidence levelof 005 In the analysis models the treatments storage timesand their interaction were assigned as fixed effects and thereplications as random effects

The given scores of different sensory attributes werecompared between the treatments using general linear model(GLM) Duncanrsquos multiple range tests were used for compar-ison of means at a confidence level of 005 Treatments andassessors were considered as main effects and the replicationsas random effects Data was reported as mean plusmn standarderror (SE)

3 Results and Discussion

31 Antioxidant Activity of Extracts The IC50 values (definedas the concentration of an antioxidant required to reduce theinitial DPPH concentration by 50 using DPPH free radicalmethod described by Cam et al [16]) of natural extracts(including Shirazi thyme cinnamon and rosemary) andsynthetic BHT were 0022 0373 0062 and 0107mgmLrespectively Therefore the amounts of Shirazi thyme cinna-mon and rosemary concentrated extracts required to replace100 ppm BHT in formulation were 22 73 and 28mL per kgof beef burger respectively Cinnamon is a source of bioactivecompounds such as cinnamaldehyde eugenol and coumarin[21] The effect of cinnamon extract as direct scavengersof free radicals has been studied by Roussel et al [22]Carnosic acid and carnosol are the main bioactive com-pounds present in the rosemary extract [23] According toSharififar et al [24] the major chemical compounds presentin Shirazi thyme were carvacrol (3365) thymol (3759) p-cymene (772) 120574-terpinene (388) and 120573-caryophyllene(206)

40

45

50

55

60

65

70

75

80

Met

myo

glob

in (

)

15 30 45 600Storage period (days)

ControlBHTCinnamon extract

Rosemary extractShirazi thyme extract

Figure 2 Effect of incorporating Shirazi thyme cinnamon androsemary extracts on the metmyoglobin () developed in raw beefburgers during frozen storage at minus18∘C

32 Physicochemical Properties of Beef Burger The resultsindicated that the samples contained 5913 moisture 19protein 12 fat 772 carbohydrate and 2 ash

33 Color Stability When assessing meat a consumer paysa great attention to its color which as a visual impressionis induced mainly by the presence of pigments but it alsodepends on tissue composition and meat structure Hencethe color of fresh meat is an important quality parameterthat determines a consumerrsquos response and decision to buyor not to buy that product at retail Changes in 119871lowast 119886lowast and119887lowast values of beef burgers during frozen storage are shown inTable 1 No significant difference (119875 gt 005) was observedbetween the samples incorporated with natural antioxidantsand those incorporated with BHT at production time (day 0)resulting in low Δ119864 values at early stages of storage All of theformulations showed significant decrease in 119886lowast during frozenstorage Formulation incorporated with rosemary extractshowed lower amounts of 119886lowast at the end of storage timeThe significant decrease in 119886lowast values indicated the red colorreduction of products during storage this is despite the factthat BHT- and extract-incorporated treatment significantlyreduced the Met-mb development ratio in comparison tocontrol one (Figure 2) During the first 30 days of storage119871lowast values increased significantly (119875 lt 005) then remainedconstant During frozen storage changes in the amountsof 119871lowast in cinnamon- (642) or Shirazi thyme-incorporatedsamples (597) were less than those in other formulationsSamples incorporated with rosemary extract showed the leastredness (433)

A significant decrease in 119886lowast values of raw pork pat-ties containing grape seed extract and bearberry has beenreported over a 12-day storage by Carpenter et al [25]however 119887lowast values (particularly of control samples) increasedsignificantly (119875 lt 005) Similarly Nunez de Gonzalez et al[26] reported that 119886lowast value of beefs stored under refrigeration

Journal of Food Quality 5

Table 1 Effect of addition of Shirazi thyme cinnamon and rosemary extracts and BHT on 119871lowast 119886lowast 119887lowastand Δ119864 values of raw beef burgersduring frozen storage at minus18∘CParameter Sample Storage period (days)

0 15 30 45 60

119871lowastControl 6033 plusmn 088 glowastlowast 5800 plusmn 058 hi 7133 plusmn 034 abc 7167 plusmn 034 ab 7267 plusmn 067 aBHT 5867 plusmn 088 ghi 5733 plusmn 034 i 6833 plusmn 034 de 6933 plusmn 034 cd 7067 plusmn 067 abc

Cinnamon extract 6033 plusmn 067 g 5433 plusmn 034 j 5967 plusmn 067 gh 6533 plusmn 067 f 6800 plusmn 058 deRosemary extract 5733 plusmn 034 i 5433 plusmn 082 i 6967 plusmn 088 bcd 7133 plusmn 088 abc 7167 plusmn 034 ab

Shirazi thyme extract 5733 plusmn 146 i 5667 plusmn 067 i 5700 plusmn 058 i 6700 plusmn 058 ef 6833 plusmn 067 de

119886lowastControl 1133 plusmn 034 a 833 plusmn 034 de 833 plusmn 034 de 767 plusmn 034 ef 667 plusmn 034 fghBHT 1100 plusmn 058 ab 667 plusmn 034 fgh 767 plusmn 067 ef 700 plusmn 058 fg 667 plusmn 034 fgh

Cinnamon extract 933 plusmn 034 cd 733 plusmn 034 efg 667 plusmn 034 fgh 567 plusmn 034 hij 533 plusmn 034 ijkRosemary extract 1167 plusmn 034 a 533 plusmn 034 ijk 533 plusmn 034 ijk 467 plusmn 034 jk 433 plusmn 034 k

Shirazi thyme extract 1000 plusmn 058 667 plusmn 034 fgh 633 plusmn 034 ghi 567 plusmn 034 hij 533 plusmn 034 ijk

119887lowastControl 2333 plusmn 034 kl 2500 plusmn 058 ij 3233 plusmn 034 bc 3267 plusmn 067 b 3400 plusmn 058 aBHT 2233 plusmn 034 lmn 2333 plusmn 034 kl 3100 plusmn 058 cd 3133 plusmn 067 bcd 3167 plusmn 067 bcd

Cinnamon extract 2167 plusmn 034 mno 2267 plusmn 034 lm 2533 plusmn 034 ij 2600 plusmn 058 i 2767 plusmn 034 hRosemary extract 2033 plusmn 0340 2100 plusmn 058 no 2900 plusmn 058 fgh 3067 plusmn 034 de 3133 plusmn 067 bcd

Shirazi thyme extract 2300 plusmn 000 klm 2433 plusmn 034 jk 2833 plusmn 034 gh 2933 plusmn 034 efg 3033 plusmn 034 def

Δ119864lowastlowastlowastControl 000 plusmn 000 f 1700 plusmn 025 aBHT 272 plusmn 069 e 1409 plusmn 018 bc

Cinnamon extract 282 plusmn 072 e 1078 plusmn 095 dRosemary extract 442 plusmn 104 e 1559 plusmn 102 ab

Shirazi thyme extract 354 plusmn 030 e 1229 plusmn 080 cdlowastlowastData represent averages of three independent repeats plusmn standard errorslowastlowastMeans with different letters are significantly different (119875 le 005)lowastlowastlowastFor each storage time the color difference (Δ119864) was calculated by comparing the color attributes of different formulations with those of control sample

for 10 weeks decreased significantly (119875 lt 005) The resultsof the current study showed that high antioxidant activity ofnatural extracts can be potentially used to develop naturalcolor stabilizers particularly for controlling 119871lowast and 119887lowast valuesin frozen beef burger

As mentioned already samples incorporated with BHTand natural extracts did not show any significant differencein Δ119864 value at the beginning of the storage time However atthe end of storage the lowest and highest changes in Δ119864wereobserved in cinnamon-incorporated and control samplesRedmeat color is an important property of visual appearanceand could influence meat purchasing decisions more thanany other quality parametersThe color of meat products andmeat is influenced by metmyoglobin percentage in muscleInitially the myoglobin was changed into oxymyoglobin(light pink color) which could result in brighter redmeat andthen oxymyoglobin was oxidized into metmyoglobin duringstorage [7]

34 Metmyoglobin Content Assay The amount of metmyo-globin has been positively linked to the extent of proteinoxidation in meat products The heme complex of heme(in) proteins consists of iron in the ferrous state (Fe+2)which turns into the ferric state (Fe+3) via a process calledautoxidation [27] The effects of natural extracts on thechanges of metmyoglobin content are shown in Figure 2Themaximum amount of metmyoglobin (7426) was measuredin antioxidant-free samples The presence of antioxidantsresulted in a significant decrease (1625ndash1847) in the

amounts of metmyoglobin developed during storage whichwas attributed to the strong antioxidant activity An etal [19] evaluated the percent metmyoglobin of the porkjerky samples incorporated with different kimchi powderconcentrations It has been reported that the metmyoglobincontents () of the samples prepared with various kimchipowder levels (ranged from 81 to 83) were significantly(119875 lt 005) lower than that of control sample (85) [19]There was no significant difference between the amounts ofmetmyoglobin under the influence of natural extracts or BHTindicating that these natural extracts can be utilized as asubstitute for BHT to prevent discoloration

The myoglobin reactions with peroxides result in theformation of lipid oxidation promoting compounds [28]The lowest amount of metmyoglobin was measured in thesamples formulated with cinnamon extract indicating thatit was more effective than the other antioxidants (eithernatural or synthetic) in preventing metmyoglobin formationA reverse relationship between the metmyoglobin level and119886lowast value was observed in this study A decrease in 119886lowast valuescorresponding to the decreased redness of lamb meat as aresult of myoglobin oxidation (metmyoglobin formation) hasbeen reported previously [29 30]

Metmyoglobin content increased during storage Thelowest increasing rate was observed in the samples incor-porated with rosemary extract The highest amount of met-myoglobin was observed in the control sample at the endof storage Changes in the metmyoglobin content of controlsample became significant after 15 days

6 Journal of Food Quality

Table 2 Thiobarbituric acid reactive substances (TBARS) values (mg malonaldehyde per kg) of beef burger during frozen storage at minus18∘CSample Storage period (days)

0 15 30 45 60Control 012 plusmn 001lowast 015 plusmn 002 020 plusmn 002 023 plusmn 001 041 plusmn 004BHT 010 plusmn 001 013 plusmn 001 015 plusmn 002 018 plusmn 001 023 plusmn 002Cinnamon extract 011 plusmn 001 013 plusmn 001 016 plusmn 001 017 plusmn 002 024 plusmn 002Rosemary extract 011 plusmn 001 013 plusmn 002 017 plusmn 002 019 plusmn 002 022 plusmn 002Shirazi thyme extract 012 plusmn 001 014 plusmn 002 017 plusmn 002 018 plusmn 001 026 plusmn 002lowastData represent averages of three independent repeats plusmn standard errors

35 Oxidative Stability Initiation is the step in which afatty acid radical is produced Two notable initiators inoxidative stability are OH∙ and HOO∙ which combines witha hydrogen atom to make water and a fatty acid radical Thefatty acid radical is not a very stable molecule so it reactsreadily with molecular oxygen thereby creating a peroxyl-fatty acid radical This radical is also an unstable species thatreacts with another free fatty acid producing a different fattyacid radical and a lipid peroxide or a cyclic peroxide if ithad reacted with itself This cycle continues as the new fattyacid radical reacts in the same wayThe radical reaction stopswhen two radicals react and produce a nonradical speciesThe lipid oxidation leads to produce of some componentscausing off-flavors and reduced nutritional quality such asmalondialdehyde and 4-hydroxynonenal

Thiobarbituric acid test can be used to determine thesecondary products of lipid oxidation in different foods suchas meat and its products [31] Thiobarbituric acid reactivesubstances (TBARS) values of different formulations (as afunction of storage time) are shown in Table 2 Exceptfor control sample the variations in TBARS values of theother formulations revealed a similar pattern Due to theabsence of antioxidant in formulation the observed changesin TBARS values of control were significantly (119875 lt 005)higher than others (8636 higher than rosemary) Natu-ral extracts were as effective as BHT for preventing lipidoxidation in beef burgers This observation indicated thatnatural herbal extracts are suitable replacers for syntheticantioxidant It has been reported that rosemary oleoresin(7704) and a mixture of BHT and BHA (7869) wasequally efficient in inhibiting the lipid oxidation of breakfastsausage containing 25 turkey meat [32] These findings arealso in good agreement with those of Mielnik et al [33] whoreported lower TBARS values after cooking of mechanicallydeboned turkey meat already stored in dark cold and treatedwith rosemary (8834) and grape seed extracts (8383)Sanchez-Escalante et al [34] reported that incorporatingrosemary essential oil into beef patties led to a significant(119875 lt 005) decrease (6400) in TBARS values during coldstorage The essential oil of rosemary was also effective inpreventing (7243) the rancidity of heat-treated turkeymeatproducts [35] It has also been reported that rosemary extractaddition into deboned poultry meat can protect (9820) theproduct from cooking-induced oxidation [36]

Regardless of sample type examined TBARS valuesincreased significantly during the frozen storage and reached

43

45

47

49

51

53

55

57

59

Tota

l aer

obic

bac

teria

l cou

nt (l

og cf

ug)

15 30 45 600Storage period (Days)

52

53

54

55

56

57

58

59

6

61

pH

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

Figure 3 Total aerobic bacterial count (log cfug) (solid symbols)and pH value (open symbols) of different beef burger formulationsas a function of storage time

to a maximum amount of 041mg malonaldehyde per kg inantioxidant-free (control) sample after 60 days At TBARSvalues of 20 off-flavors are definitely detectable and themeatis considered to be unacceptable [37]

36 Changes in pH Values Changes in pH values of beefburgers during frozen storage are shown in Figure 3 Allformulations revealed relatively similar pH values just afterproduction ranging from 588 to 593 coinciding with theISIRI 2008 Mohamed and Mansour [38] similarly reportedthat no significant differences (119875 gt 005) were observed in thepH values of beef patties after incorporating natural herbalextracts

A downward pattern of different rates was observed in thepH values of all formulations during frozen storage As nomicrobial growth was expected during storage the decreasein the pH values could be attributed to the microbial growthduring thawing (by consuming sugar and producing organicacids) Control sample had the lowest pH (551) at the end ofstorage Emiroglu et al [39] reported that the pH values of

Journal of Food Quality 7

all fresh ground beef patty samples treated with thyme andoregano generally decreased after sixth day of storage (119875 gt005)

Also the result showed that to decrease pH amount oflipid oxidation and metmyoglobin significantly increasedLapidot et al (2005) evaluated lipid peroxidation of grilledred turkey muscle (Donor Kabab) as affected by pH In thisstudy they show indeed that lipid peroxidation and myo-globin of a real fast food (turkey Doner Kebab shawarma) issignificantly more rapidly oxidized at pH 30 than at pH 50

37 Microbial Growth As shown in Figure 3 total aerobicbacterial counts of antioxidants-incorporated formulationswere not significantly (119875 lt 005) different The highestamount of total count was observed in control sample(Figure 3) Shirazi thyme-incorporated beef burgers had thelowest microbial count which could be attributed to thehigh antimicrobial properties resulting from thymol and car-vacrol The antibacterial mechanism of thymol and carvacrolis the disruption of the cytoplasmic membrane which raisesits permeability and depolarizes its potential Total countof frozen raw beef burger should be lower than 6 log cfug[40] Except for the control sample the microbial counts ofbeef burgers were lower than the maximum allowed countA relatively good correlation was observed between the pHvalues and total aerobic counts For example control samplehad the lowest pH and the highestmicrobial count Rosemaryextract (1000 ppm) inhibitory effect on the microbial growthof surface-applied beef steaks has been reported by Djenaneet al [41] However Sanchez-Escalante et al [34] reportedthat rosemary did not affect the microbial counts of beefpatties during storage (3 logCFUg)

An increase in the microbial counts was observed duringstorage but not beyond the standard range As a rule ofthumb in good manufacturing and hygienic practices duringpreparation of beef burger and its related products rapidand proper storage is important for decreasing the microbialgrowth and enhancing the shelf life

Vieira et al [42] studied the effect of frozen storage condi-tions (temperature and length of storage) on microbiologicaland sensory quality of rustic crossbred beef at different statesof ageing The result showed that psychrotrophic bacteriaincreased (138 logCFUg) significantly during 90-day storage38 Sensory Properties Color flavor and texture are themostimportant sensory attributes which influence the acceptabil-ity of meat products by consumers [43] Sensory evaluationresults of cooked beef burgers are shown in Figure 4 Gener-ally incorporating Shirazi thyme cinnamon and rosemaryextracts into beef burger formulations had no significantinfluence on the sensory properties Although samples for-mulated with Shirazi thyme and cinnamon extracts with6944 and 7167 acceptability obtained the highest tastescores by panelists (119875 lt 005) The antioxidant prop-erties of natural extracts were the main reason for theincreased sensory scores of natural extract-incorporatedformulations through preventing the formation of oxidation-mediated off-flavors and off-odors (short-chain aldehydes

4

45

5

55

6

65

7Appearance

Taste

OdorTexture

Overall

ControlBHTRosemary extract

Shirazi thyme extractCinnamon extract

Figure 4 Sensory evaluation of different beef burger formulationsa 9-point descriptive scale (1 = extremely poor and 9 = highlyacceptable) was used during evaluation

and ketones) during storage Moreover the presence ofpleasant volatile constituents in natural extracts (particu-larly in cinnamon and Shirazi thyme) led to an increasedsensory score in comparison to the BHT-incorporatedformulation

A significant increase in the flavor scores of beef pattiesincorporated with antioxidant mechanically deboned poul-try meat during frozen storage was similarly reported byMohamed and Mansour [38]

4 Conclusion

This work aimed to study the possible replacement ofsynthetic antioxidant BHT with natural extracts (includingShirazi thyme cinnamon and rosemary extracts) in beefburger formulation Different samples were prepared thendifferent characteristics such as protein and lipid oxidationand physicochemical microbial and sensory properties wereevaluated during frozen storage Herbal extracts could inhibitthe lipid oxidation in formulated burgers Moreover it wasdemonstrated that natural herbal extracts were generallybetter than BHT in preventing the lipid and protein oxi-dations as well as improving the sensory attributes of beefburgersTherefore it can be concluded that natural extracts ofShirazi thyme (0022mgmL) cinnamon (0373mgmL) androsemary (0062mgmL) can be used as natural substitutesfor BHT (0107mgmL)This substitutionmay have potentialimplication for developing green-labeled meat product Infuture studies it would be informative to study the effect ofmixed extracts and their possible synergistic or antagonisticeffects in extending the shelf life of meat products

8 Journal of Food Quality

Additional Points

Practical Applications Beef burger containing natural antiox-idant is one of themost important functional food for humanconsumption attributable to its nutritional properties andhealth effects However the nutraceutical properties of thisfood have improved due to alternative BHT with extractsThe present investigation demonstrated the effects of addingvarious natural antioxidants to the beef burger so as tomonitor the changes that occur to the physicochemicalantimicrobial and sensorial properties of the beef burger

Conflicts of Interest

The authors declare that they have no conflicts of interest

Acknowledgments

This research project was financially supported by ScientificAffairs Shiraz University and Department of Food Scienceand Technology Shiraz University Shiraz Iran

References

[1] D Ladikos and V Lougovois ldquoLipid oxidation in muscle foodsa reviewrdquo Food Chemistry vol 35 no 4 pp 295ndash314 1990

[2] C JMussinan andM JMorello ldquoFlavor analysis developmentsin isolation and characterizationrdquo American Chemical Societypp 343ndash358 1998

[3] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWTmdashFoodScience and Technology vol 68 pp 385ndash390 2016

[4] G Comi E Tirloni D Andyanto M Manzano and LIacumin ldquoUse of bio-protective cultures to improve the shelf-life and the sensorial characteristics of commercial hamburg-ersrdquo LWTmdashFood Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[5] F Shahidi ldquoAntioxidants in food and food antioxidantsrdquoFoodNahrung vol 44 pp 158ndash163 2000

[6] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[7] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[8] H H Hashemi Gahruie M H Eskandari G Mesbahi andM A Hanifpour ldquoScientific and technical aspects of yogurtfortification a reviewrdquo Food Science and Human Wellness vol4 no 1 pp 1ndash8 2015

[9] K Yamazaki S Kawamorita H Ohmiya and M SawamuraldquoDirected ortho borylation of phenol derivatives catalyzed by asilica-supported iridium complexrdquo Organic Letters vol 12 no18 pp 3978ndash3981 2010

[10] A Roberts and L A Haighton ldquoA hard look at FDArsquos review ofGRAS noticesrdquo Regulatory Toxicology and Pharmacology vol79 pp S124-S128 2016

[11] H H Hashemi Gahruie E Ziaee M H Eskandari andS M Hosseini ldquoCharacterization of basil seed gum-basededible films incorporated with Zataria multiflora essential oilnanoemulsionrdquo Carbohydrate Polymers vol 166 pp 93ndash1032017

[12] S K Devatkal K Narsaiah and A Borah ldquoAnti-oxidant effectof extracts of kinnow rind pomegranate rind and seed powdersin cooked goatmeat pattiesrdquoMeat Science vol 85 no 1 pp 155ndash159 2010

[13] M Estevez R Ramırez S Ventanas and R Cava ldquoSage androsemary essential oils versus BHT for the inhibition of lipidoxidative reactions in liver paterdquo LWTmdashFood Science andTechnology vol 40 no 1 pp 58ndash65 2007

[14] E Abdollahzadeh M Rezaei and H Hosseini ldquoAntibacterialactivity of plant essential oils and extracts the role of thymeessential oil nisin and their combination to control listeriamonocytogenes inoculated in minced fish meatrdquo Food Controlvol 35 no 1 pp 177ndash183 2014

[15] A Alaklabi I A Arif A Ahamed R Surendra Kumar andA Idhayadhulla ldquoEvaluation of antioxidant and anticanceractivities of chemical constituents of the saururus chinensis rootextractsrdquo Saudi Journal of Biological Sciences 2017

[16] M Cam Y Hısıl and G Durmaz ldquoClassification of eightpomegranate juices based on antioxidant capacity measured byfourmethodsrdquo FoodChemistry vol 112 no 3 pp 721ndash726 2009

[17] AOAC Association of Official Agricultural Chemists ldquoOfficialmethods of analysis of AOAC Internationalrdquo in AgricultureChemicals Contaminants Drugs vol 1 AOAC InternationalArlington VA USA 16th edition 1995

[18] K L Yam and S E Papadakis ldquoA simple digital imagingmethodfor measuring and analyzing color of food surfacesrdquo Journal ofFood Engineering vol 61 no 1 pp 137ndash142 2004

[19] K-I An J-H Choi Y-S Choi et al ldquoEffects of kimchi powderon quality characteristics of semi-dried pork jerkyrdquo KoreanJournal for Food Science of Animal Resources vol 30 no 2 pp198ndash205 2010

[20] B Kodal Coskun E Calikoglu Z Karagoz Emiroglu and KCandogan ldquoAntioxidant active packaging with soy edible filmsand oregano or thyme essential oils for oxidative stability ofground beef pattiesrdquo Journal of Food Quality vol 37 no 3 pp203ndash212 2014

[21] B Shan Y Z Cai M Sun and H Corke ldquoAntioxidant capacityof 26 spice extracts and characterization of their phenolicconstituentsrdquo Journal of Agricultural and Food Chemistry vol53 no 20 pp 7749ndash7759 2005

[22] A-M Roussel I Hininger R Benaraba T N Ziegenfuss andR A Anderson ldquoAntioxidant effects of a cinnamon extract inpeople with impaired fasting glucose that are overweight orobeserdquo Journal of the American College of Nutrition vol 28 no1 pp 16ndash21 2009

[23] S Moreno T Scheyer C S Romano and A A VojnovldquoAntioxidant and antimicrobial activities of rosemary extractslinked to their polyphenol compositionrdquo Free Radical Researchvol 40 no 2 pp 223ndash231 2006

[24] F Sharififar M H Moshafi S H Mansouri M Khodashenasand M Khoshnoodi ldquoIn vitro evaluation of antibacterial andantioxidant activities of the essential oil and methanol extractof endemic Zataria multiflora Boissrdquo Food Control vol 18 no7 pp 800ndash805 2007

[25] R Carpenter M N OrsquoGrady Y C OrsquoCallaghan N M OrsquoBrienand J P Kerry ldquoEvaluation of the antioxidant potential of grape

Journal of Food Quality 9

seed and bearberry extracts in raw and cooked porkrdquo MeatScience vol 76 no 4 pp 604ndash610 2007

[26] M T Nunez de Gonzalez B S Hafley R M Boleman R KMiller K S Rhee and J T Keeton ldquoAntioxidant propertiesof plum concentrates and powder in precooked roast beef toreduce lipid oxidationrdquo Meat Science vol 80 no 4 pp 997ndash1004 2008

[27] M P Richards and M A Dettmann ldquoComparative analysisof different hemoglobins autoxidation reaction with peroxideand lipid oxidationrdquo Journal of Agricultural and FoodChemistryvol 51 no 13 pp 3886ndash3891 2003

[28] J Everse and N Hsia ldquoThe toxicities of native and modifiedhemoglobinsrdquo Free Radical Biology and Medicine vol 22 no6 pp 1075ndash1099 1997

[29] C Kennedy D J Buckley and J P Kerry ldquoInfluence of differentgas compositions on the short-term storage stability of mother-packaged retail-ready lamb packsrdquo Meat Science vol 69 no 1pp 27ndash33 2005

[30] J P Kerry M G OrsquoSullivan D J Buckley P B Lynch andP A Morrissey ldquoThe effects of dietary 120572-tocopheryl acetatesupplementation and modified atmosphere packaging (MAP)on the quality of lamb pattiesrdquo Meat Science vol 56 no 1 pp61ndash66 2000

[31] J Fernandez J A Perez-Alvarez and J A Fernandez-LopezldquoThiobarbituric acid test for monitoring lipid oxidation inmeatrdquo Food Chemistry vol 59 no 3 pp 345ndash353 1997

[32] S Barbut D B Josephson and A J Maurer ldquoAntioxidantproperties of rosemary oleoresin in Turkey sausagerdquo Journal ofFood Science vol 50 no 5 pp 1356ndash1359 1985

[33] M B Mielnik K Aaby and G Skrede ldquoCommercial antioxi-dants control lipid oxidation in mechanically deboned turkeymeatrdquoMeat Science vol 65 no 3 pp 1147ndash1155 2003

[34] A Sanchez-Escalante D Djenane G Torrescano J A Beltranand P Roncales ldquoThe effects of ascorbic acid taurine carnosineand rosemary powder on colour and lipid stability of beef pattiespackaged in modified atmosphererdquoMeat Science vol 58 no 4pp 421ndash429 2001

[35] M B Mielnik S Sem B Egelandsdal and G Skrede ldquoBy-products from herbs essential oil production as ingredient inmarinade for Turkey thighsrdquo LWTmdashFood Science and Technol-ogy vol 41 no 1 pp 93ndash100 2008

[36] J H Macneil P S Dimick and M G Mast ldquoUse of chemicalcompounds and a rosemary spice extract in quality mainte-nance of deboned poultry meatrdquo Journal of Food Science vol38 no 6 pp 1080-1081 1973

[37] E TEC ldquoMeat technology update 1-6 2009rdquo[38] H M H Mohamed and H A Mansour ldquoIncorporating

essential oils of marjoram and rosemary in the formulation ofbeef patties manufactured with mechanically deboned poultrymeat to improve the lipid stability and sensory attributesrdquoLWTmdashFood Science and Technology vol 45 no 1 pp 79ndash872012

[39] Z K Emiroglu G P Yemis B K Coskun and K CandoganldquoAntimicrobial activity of soy edible films incorporated withthyme and oregano essential oils on fresh ground beef pattiesrdquoMeat Science vol 86 no 2 pp 283ndash288 2010

[40] ISIR Raw frozen hamburgermdashSpecifications vol 2304 Instituteof standards and industrial research of Iran Karaj Iran 3rdedition 2008

[41] DDjenane A Sanchez-Escalante J A Beltran andP RoncalesldquoAbility of 120572-tocopherol taurine and rosemary in combination

with vitamin C to increase the oxidative stability of beef steakspackaged in modified atmosphererdquo Food Chemistry vol 76 no4 pp 407ndash415 2002

[42] C Vieira M T Diaz B Martınez and M D Garcıa-CachanldquoEffect of frozen storage conditions (temperature and lengthof storage) on microbiological and sensory quality of rusticcrossbred beef at different states of ageingrdquo Meat Science vol83 no 3 pp 398ndash404 2009

[43] J Aliakbarlu and S Khalili Sadaghiani ldquoEffect of avishaneshirazi (zataria multiflora) and clove (syzygium aromaticum)essential oils on microbiological chemical and sensory proper-ties of ground sheep meat during refrigerated storagerdquo Journalof Food Quality vol 38 no 4 pp 240ndash247 2015

Research ArticleOptimization of Ultrasound Extraction of Cactus Pear(Opuntia ficus indica) Seed Oil Based on AntioxidantActivity and Evaluation of Its Antimicrobial Activity

Mariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-CansinoErnesto Alaniacutes-Garciacutea Luis Delgado-Olivares Joseacute Alberto Ariza-OrtegaEsther Ramiacuterez-Moreno and Joseacute de Jesuacutes Manriacutequez-Torres

Centro de Investigacion Interdisciplinario Area Academica de Nutricion Instituto de Ciencias de la Salud Universidad Autonoma delEstado de Hidalgo Circuito Actopan-Tilcuautla SN Ex Hacienda La Concepcion 42160 San Agustın Tlaxiaca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 20 February 2017 Accepted 9 April 2017 Published 27 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Marıa de los Angeles Ortega-Ortega et alThis is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The purpose of the present study was to determine the optimal ultrasound conditions (amplitude level and time) for the extractionof cactus pear seed oil with the highest antioxidant activity using a closed system Seed oil was analyzed for yield antioxidant activityby ABTS and DPPH and antimicrobial activity Conventional extraction methods were assessed for comparison Amplitude levelsignificantly affected antioxidant activity in linear terms (p lt 00001 DPPH and p lt 0001 ABTS resp) so at lower amplitudes thehigher antioxidant activity was achieved The optimum ultrasound extraction conditions were of 78 amplitude for 10min andyielded antioxidant activity values of 6625mg AAE100 g and 289120583mol TE100 g for ABTS and DPPH respectively Comparedwith conventional extraction methods ultrasound exhibited lower oil yield and antioxidant activity but had the potential toachieve comparable results if multiple ultrasound extractions are performed in the time needed by conventional methods Seed oilsshowed similar antimicrobial activity despite the extraction method and were more effective against Escherichia coli The resultsdemonstrated that ultrasound can be an alternative extraction method of seed oils from fruits such as cactus pear

1 Introduction

Cactus pear fruit (Opuntia ficus indica) is common in aridand semiarid regions around the world [1] This fruit that ismainly consumed fresh in Mexico [2] is composed by pulppeel and seeds [3] According to several studies cactus pearfruit has bioactive compounds [4 5] with high antioxidantand antimicrobial activity [6 7] Some of these compoundsare found in the seeds [8] which comprise 3 to 15 of thecactus pear pulp [9] and are usually considered waste afterpulp processing [7] Seeds also have a high content of oil(988 gkg) [10] characterized by high levels of linoleic andoleic acids [7] and other components as phenols [11] all whichmay contribute to humanhealth [12] Currently seed oils havebeen used as natural agents for food preservation [13] andmany have exhibited antimicrobial and antioxidant activity

some of these oils are from pumpkin [14] apple [15] blackcumin [16] and basil [17] among other seeds Cactus pearseeds fromOpuntia dillenii also have a high antioxidant activ-ity derived from bioactive compounds such as polyphenolsand polyunsaturated fatty acids [18] Some polyunsaturatedfatty acids have also been identified in seeds from Opuntiaficus indica [19 20] implying that these seeds may also havehigh antioxidant activity

Seed oil is usually extracted by means of conventionalmethods such as Soxhlet and maceration using heat agita-tion or long extraction times [21] Microwave supercriticalfluids and ultrasonic assisted extraction are unconventionalmethods that exert a physical effect on the sample [22]Ultrasound has been used to extract antioxidants frommanyfood materials including seeds Ultrasound and ultrasound-assisted extractions use sound waves to produce cavitation

HindawiJournal of Food QualityVolume 2017 Article ID 9315360 9 pageshttpsdoiorg10115520179315360

2 Journal of Food Quality

microbubbles that collapse violently in the sample and facili-tate the release and extraction of several compounds [23ndash25]Some researchers had evaluated ultrasound-assisted extrac-tion in an open system using a sonicator probe directly onthe liquid sample to obtain seed oil fromflaxseed [26] Koreanpine [27] and pomegranate [28] The purpose of the presentstudy was to optimize the extraction conditions of cactuspear seed oil using ultrasound in a closed system based onantioxidant activity and using response surfacemethodologyYield extraction and antioxidant and antimicrobial activitywere compared with conventional methods

2 Materials and Methods

21 Sample Green cactus pear (Opuntia ficus indica) Reynavariety was provided by the Mexican Association CoMeN-Tuna (Consejo Mexicano del Nopal y la Tuna AC ofActopanHidalgoMexico) in spring of 2012Thegreen cactuspear seeds were obtained after several washes with water thatremoved the pulp and residues The seeds were leaved todry at ambient temperature until they reached a moisture of643 After the seeds were crushed using an industrial mill(Cyclotec 1093 Tecator Hoganas AB Sweden) the powderwas passed through a mesh sieve to obtain a particle size ofapproximate 05mm and then stored in sealed plastic bags atroom temperature and dark conditions

22 Ultrasound Extraction Ultrasound (VCX-1500 Sonic ampMaterials Inc Newtown CTUSA) at 1500Wwith a constantfrequency of 20 kHz and a probe of 25mm was used forthe extraction of green cactus pear seeds oil Extractionfrom milled and sieved seeds (20 g) was carried out at anamplitude and time ranges of 80 to 90 and 5 to 15minrespectively and a fixed outlet temperature of 25∘C A sampleof 400mL was introduced in a jacketed vessel with waterat 4∘C circulating through the secondary layer [29] Afterextraction the aqueous and solid phases were separatedby filtration using a vacuum pump (DOA-P704-AA GASTManufacturing Inc BentonHarbor MI USA) Both phasesaqueous and solid (this last was dried) (Weston 74-1001-wWeston Products LLC Strongsville OH USA) were mixedwith hexane for 30min and then separated from the solventby filtration The aqueous phase was centrifuged (Allegra25R Beckman Couler CA USA) at 10000 rpm for 30minat 4∘C and was stored in plastic containers and kept frozenuntil analysis The solid phase was stored in hermeticallysealed bags in the dark The solvent obtained from the twophaseswas evaporated (BUCHILabortechnikAG Flawil SGSwitzerland) at 40∘C to obtain the oil

23 Soxhlet Extraction Soxhlet extraction was performedaccording to the AOAC [30] Milled and sieved seeds (5 g)hexane (120mL) and a universal fat extraction system (BuchiLabortechnik AG Flawil SG Switzerland) were used

24 Maceration Extraction Milled and sieved seeds (10 g)were introduced in a previously defatted cotton bag andthen immersed in 200mL of hexane in a closed glass at atemperature of asymp25∘C After the sample was stored in a dark

place for 24 hrs the oil was obtained after solvent evaporationusing a rotary evaporator (BUCHI Labortechnik AG FlawilSG Switzerland) at 40∘C

25 Yield Oil yield was determined according to Chouguiet al [31] using the following equation

Oil () = (1198721 minus11987201198722 ) times 100 (1)

where1198720 is the weight of the empty Eppendorf tube (g)1198721is the weight of the Eppendorf tube after evaporation (g) and1198722 is the weight of the milled seeds (g)

The oil was stored in 2mL amber Eppendorf tubes atminus32∘C until analysis

26 Determination of Antioxidant Activity

261 ABTS Assay Antiradical capacity by ABTS was mea-sured according to Kuskoski et al [32] The radical cation221015840azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) diam-monium salt (ABTS∙+) was produced by reacting 7mMABTSstock solution with 245mM potassium persulfate in thedark at room temperature for 16 hrs before being used TheABTS∙+ solution was diluted with deionized water to anabsorbance of 070 plusmn 010 at 754 nm An aliquot of 20120583L ofsample was added to 980120583L of the diluted ABTS∙+ solutionand absorbance readings were taken after 7min incubationat room temperature The absorbance of the mixture wasmeasured at 754 nm in themicroplate reader (PowerWaveXSUV-Biotek software KC Junior VT USA) and antioxidantcapacity was expressed as mg ascorbic acid equivalent per100 g of oil (mg AAE100 g)

262 DPPH Assay Antiradical activity was measured using11-diphenyl-2-picrylhydrazyl (DPPH∙) radical as describedby Morales and Jimenez-Perez [33] A methanol-acetatesolution (74mg100mL) of the stable DPPH∙ radical wasprepared A sample aliquot of 100120583Lwas placed into vials and500 120583L of DPPH∙ solution was added before the mixture wasleft to sit at room temperature for 1 hr Finally absorbancewasmeasured at 520 nm in the microplate reader (Power WaveXS UV-Biotek software KC JuniorWinooski VT USA) andantioxidant activity was expressed as 120583mol of Trolox equiva-lents per 100 g of oil (120583mol TE100 g)

27 Experimental Design

271 Optimization The optimization of the ultrasoundextraction conditions was performed using the responsesurface methodology (RSM) with a central composite rotat-able design for two independent extraction variables at fivelevelsThe independent extraction variables (amplitude level80ndash90 time 5ndash15min) were determined based on prelimi-nary experiments where higher antioxidant activity by ABTSand DPPH was observed Design consisted in thirteen com-binations with five central points replicates (Table 1) Exper-imental data were subjected to multiple nonlinear regression

Journal of Food Quality 3

Table 1 Experimental design matrix

Numbera Pattern Amplitude level () Time (min)119883119894 119883119895

(1) 00 85 10(2) +minus 90 5(3) ++ 90 15(4) 00 85 10(5) A0 92 10(6) minusminus 80 5(7) 00 85 10(8) a0 78 10(9) 0A 85 17(10) minus+ 80 15(11) 00 85 10(12) 00 85 10(13) 0a 85 3aNonrandomized

analysis (JMP 702 SAS Institute Inc Cary NC USA) fittedto a second-order polynomial model

119884 = 1205730 +2

sum119894=1

120573119894119883119894 +2

sum119894=1

1205731198941198941198832119894 +sum119894

sum119895=119894+1

120573119894119895119883119894119883119895 (2)

where 119884 is the predicted response 1205730 is the constant coeffi-cient120573119894 is the lineal coefficient120573119894119894 is the quadratic coefficientand120573119894119895 is the interaction coefficients In thismodel119883119894 and119883119895are the independent extraction variables amplitude level ()and time (min) respectively

The adequacy of themathematicalmodel was determinedusing the coefficient 1198772The significance of the model regres-sion coefficients was evaluated using an analysis of varianceThree-dimensional curves from the response surface plotswere obtained to interpret the effects of the interactionbetween independent variables on the response variablesContour plots were generated to represent the extrapolationand interpret the optimization of the extraction variablesusing the Sigma Plot 123 graphing software (SYTAT softwareInc Richmond CA USA)

272 Treatment Comparison Comparison between extrac-tion methods (ultrasound-optimized Soxhlet and macera-tion) was carried out by a one-way analysis of variance(ANOVA) All determinations were performed in triplicateand significant differences between means were determinedby Duncan test (p le 005) using the SPSS program (150 SPSSInc Chicago IL USA)

28 Scanning Electron Microscopy Scanning electron micro-scopy (SEM) was used to examine the morphological alter-ations caused to the cactus pear seeds before and after theultrasound extraction Samples deposited on the siliconwaferwere coated with a thin layer of gold (Denton VacuumDesk V Moorestown NJ USA) applying 20 millitorr and

20mA during 4min Samples were observed in a scanningelectronic microcopy (JEOL JSM-6300 Peabody MA USA)at 1000 and 500 amplifications and micrographs were takento establish the structural comparison between both samples

29 Antimicrobial Activity The green cactus pear seed oilwas tested against one Gram-positive bacteria Staphylococ-cus aureus (ATCC 1654) and two Gram-negative bacteriaEscherichia coli (ATCC 25922) and Pseudomonas aeruginosa(ATCC 27853) All microorganisms were obtained from theMexicanMicrobial Culture Collection of CINVESTAV of theNational Polytechnic Institute (Mexico) For each microor-ganism bacterial suspensions were made in a soybean-casein digest medium to a concentration of approximately108 CFUmL

To evaluate the antimicrobial activity and the mini-mum inhibitory concentration (MIC) the disk diffusionmethod was used Each bacterial suspension (100 120583L fromthe 108 CFUmL) was spread on prepared agar plates (sterileStandardMethodsAgar for bacteria) Filter sterile paper discs(6mm in diameter) were impregnated with 6667 50 3333and 1667 120583L of the undiluted oil and were placed on theinoculated plates The negative control was hexane whileampicillin (10 120583g) and streptomycin (10 120583g) were used aspositive controls The plates where incubated at 37∘C (ArsaAR-130 Felisa Jalisco Mexico) for 24 hrs The diameters ofthe inhibition zones were measured in millimeters and theresults of MIC were expressed as 120583g120583L

3 Results and Discussion

31 Extraction Yield Table 2 shows the oil yields achievedby the ultrasound treatments The extraction yield variedfrom 375 to 6 and the maximum yield was obtained at thehighest amplitude level of 92 Oil yield strongly dependedon amplitude level probably because at high amplitudes thecavitation effect increases [21] and induces physical changeson the structure of the seed such as disruption of the cell wallsreduction of the particle size and increase of exposure areaThese conditions may facilitate the penetration of the solventand thus the extraction of oil [26 28 34] The maximumyield was achieved after 10min of treatment and longertimes (15min) at high amplitudes (90) did not increase oilextraction (Table 2) Albeit time is an important variable afteryield reaches a peak a longer treatment does not maximizeextraction the same was described by Zhang et al [27] forKorean pine seed who demonstrated that oil yield increasedwith time but when it reached amaximum yield equilibratedand then decreased gradually This may be attributed to aninitial complete fracture of the cell walls during the firstminutes of the cavitation effect [26 28 34]

32 Antioxidant Activity of Green Cactus Pear Seed OilExtracted by Ultrasound Due to the complexity of theoxidation processes it is advisable to performmore than onemethod to obtain the antioxidant profile of a sample [35]In order to determine the antioxidant activity of the green

4 Journal of Food Quality

Table 2 Extraction yield and antioxidant activity of green cactus pear seed oil extracted by ultrasound under different conditions

Extraction conditions Antioxidant activity

Amplitude level () Time (min) Oil yield () ABTS DPPHmg AAE100 g 120583mol TE100 g

85 10 575 plusmn 003 6615 plusmn 407 24610 plusmn 09290 5 415 plusmn 001 5598 plusmn 313 14176 plusmn 39090 15 485 plusmn 002 5993 plusmn 445 16702 plusmn 11485 10 525 plusmn 001 6812 plusmn 659 23601 plusmn 32292 10 600 plusmn 006 5584 plusmn 236 10163 plusmn 46880 5 525 plusmn 001 6607 plusmn 217 26707 plusmn 73785 10 375 plusmn 000 6837 plusmn 392 24505 plusmn 23778 10 540 plusmn 010 6599 plusmn 501 28926 plusmn 02685 17 560 plusmn 006 6578 plusmn 037 26009 plusmn 13380 15 540 plusmn 000 6691 plusmn 320 28496 plusmn 09385 10 575 plusmn 000 6773 plusmn 040 27755 plusmn 17185 10 530 plusmn 010 6744 plusmn 389 24508 plusmn 29285 3 550 plusmn 010 6763 plusmn 000 25005 plusmn 199plusmn standard deviation

Table 3 Antioxidant activity regression coefficients of the ultra-sound extraction conditions

Coefficient ABTS DPPH1205730 67562964a 24996199a

120573119894 minus3927762b minus6357459a120573119895 02724311 71702572120573119894119895 077572 18421052120573119894119894 minus3719624b minus2977102b120573119895119895 minus0826106 004258041198772adj 093 096120573119894 amplitude level 120573119895 time significance levels a119901 lt 00001 b119901 lt 0001

cactus pear seed oil two parameters were evaluated antiox-idant and scavenging capacity by ABTS and DPPH respec-tively The results and experimental design are described inTable 2 Antioxidant activity ranged from 5584 to 6837mgAAE100 g for ABTS and 10163 to 28926120583mol TE100 g forDPPH A 1198772 value closest to one or at least of 080 indicates agood fit of themodel [36]The1198772 values for ABTS andDPPHwere 093 and 096 respectively (Table 3) indicating thatthe averages obtained adjusted to the mathematical responsesurface model

33 Effect of Ultrasound Extraction Conditions on the Antiox-idant Activity of Cactus Pear Seed Oil In this study asecond-order polynomial model for predicting the antiox-idant activity of green cactus pear seed oil was obtainedby multiple linear regression analysis of the experimentaldata Table 3 shows the regression coefficients and significantprobabilities of the linear quadratic and interaction effects ofthe ultrasound conditions on the seed oil antioxidant activityBoth ABTS and DPPH values were significantly affected byamplitude level in linear term (120573119894) at 119901 lt 00001 DPPH and119901 lt 0001 ABTS respectively as well as in its quadratic term

(120573119894119894) at 119901 lt 0001 DPPH and ABTS The three-dimensionalsurface plots constructed to observe the effect of ultrasoundprocessing (Figure 1) demonstrated that antioxidant activitywas higher when the applied amplitude decreased

34 Optimization of the Ultrasound Extraction Conditions ofCactus Pear Seed Oil Optimal extraction conditions wereselected from the overlapped contour plots inwhich the effectof amplitude level and time on the antioxidant activity ofgreen cactus pear seed oil was considered

Figure 2 shows the optimal zone where the highestantioxidant activity by ABTS and DPPH was achieved Theconditions corresponded to amplitude of 78 applied for10min In this zone the values for antioxidant activity wereof 6625mg AAE100 g and 289 120583mol TE100 g for ABTS andDPPH respectively

35 Comparison between Methods

Extraction Yield and Antioxidant Activity Figure 3 comparesthe oil yields obtained by the three extraction methodsThe results revealed that the yield obtained using the opti-mized ultrasound extraction was significantly lower than theobtained with the Soxhlet and maceration procedures Thehigher oil yield obtained by Soxhlet could be attributed to theconstant and extended contact (4 to 6 hrs) of the sample withthe solvent at high temperatures in addition to the repeatedwashing cycles [37] The ultrasound yield was closer to thatof maceration method but this last one required longer time(24 hrs) as compared to 10min ultrasound treatment

The results of antioxidant activity by ABTS andDPPH areshown in Figure 4 Both parameters were significantly higherin the oil extracted by Soxhlet (5433 plusmn 084mg AAE100 gand 26660 plusmn 197 120583mol TE100 g resp) compared to theother extraction methods The ultrasound and macerationextractions exhibited similar antioxidant activity by ABTSwhile DPPH was significantly higher for the ultrasound seed

Journal of Food Quality 5

45

50

55

60

65

70

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(mg

AA

E100

g)A

ntio

xida

nt ac

tivity

(a)

50

100

150

200

250

300

350

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(120583m

ol T

E100

g)A

ntio

xida

nt ac

tivity

(b)

Figure 1 Effect of the ultrasound extraction on the antioxidant activity of green cactus pear seed oil (a) ABTS (b) DPPH

121

109

133145

157

169181

157

169

193

169

181

205

193

205

217

217

205

229

217

229

241

229

241

253

241

253

253

265

265

265

265

277

277

277

265

289

DPPH

5650

5650

557555005425

572558005875

5950

6025

6100

6175

6250

5950

6025

63256400

6175

6250

6250

6325

6475

6325

64006475

6400

6550

6475

6550

6550

6625

6625

6625

6700

6700

6700

6775

6775

6775

6700

6700

6625

6550

6475

6625

ABTS

Optimun condition

4

6

8

10

12

14

16

Tim

e (m

in)

80 82 84 86 88 90 9278Amplitude level ()

Figure 2 Optimal ultrasound extraction conditions of green cactuspear seed oil based on the highest antioxidant activity

oil Albeit the oil extracted by the Soxhlet method presentedhigher yield and antioxidant activity the ultrasound-assistedextraction may be enhanced if multiple extractions arecarried out in a time comparable to the required by theSoxhlet procedure (4ndash6 hrs)

36 Antimicrobial Activity Escherichia coli and Staphylo-coccus aureus are distributed in nature (water soil andvegetation) and are also part of the human intestinal

c

a

b

Ultrasound Soxhlet Maceration0

1

2

3

4

5

6

7

8Yi

eld

()

Figure 3 Cactus pear seed oil yield achieved by different extractionmethods abcDifferent letters mean significant differences betweenmethods (p lt 005)

b a b

b

a

c

Ultrasound Soxhlet Maceration0

255075

100125150175200225250275300

DPPH (120583mol TE100 g)ABTS (mg AAE100 g)

Figure 4 Antioxidant activity by ABTS and DPPH of cactus pearseed oil extracted by different methods abcDifferent letters meansignificant differences between methods (p lt 005)

6 Journal of Food Quality

Table 4 Antimicrobial activity of cactus pear seed oil extracted by different methods

Diameter of inhibition zone (mm)Oillowast (+) control (minus) control

Staphylococcus aureus (Gram-positive)Ultrasound 917 plusmn 029a 1889 plusmn 154 NDSoxhlet 950 plusmn 087a 1878 plusmn 164 NDMaceration 978 plusmn 069a 1811 plusmn 117 NDEscherichia coli (Gram-negative)Ultrasound 778 plusmn 019a 1556 plusmn 212 NDSoxhlet 756 plusmn 019a 1533 plusmn 265 NDMaceration 756 plusmn 038a 1400 plusmn 233 NDPseudomonas aeruginosa (Gram-negative)Ultrasound ND 1256 plusmn 038 NDSoxhlet ND 1222 plusmn 038 NDMaceration ND 1278 plusmn 038 NDlowastSeed oil 6667120583L (+) control ampicillin (disc 10 120583g Staphylococcus aureus and Escherichia coli) and streptomycin (disc 10 120583g Pseudomonas aeruginosa) (minus)control hexane ND not detected plusmn standard deviation a Same superscripts indicates that there is no significant difference (p gt 005)

microbiota [38] Pseudomonas aeruginosa besides beingpresent in the intestinalmicrobiota [39] is a bacteria found inthe soil fertilizers and water used for food production [40]and thus it can contaminate fresh or processed food whichis an indicator of inadequate sanitation or improper han-dling during food production [41] Table 4 summarizes theantimicrobial activity of green cactus pear seed oil Extractionmethod did not have a significant effect on the antimicrobialactivity against Staphylococcus aureus and Escherichia colibut the effect was lower than the positive controls Theseresults may be explained by the similar seed oil concentrationand combined action of compounds on the structure ofmicrobial cells [42 43] despite the extraction method Seedoil did not exhibit antimicrobial activity against Pseudomonasaeruginosa probably due to the oil chemical composition thetype of microorganism and the own characteristics of thebacteria [42ndash44]The antimicrobial activity of oils is generallymore effective against Gram-positive bacteria in comparisonto Gram-negative bacteria which are more resistant mainlybecause their outer membrane is less permeable [42 4345 46] The results suggest that Pseudomonas aeruginosawas more resistant than Escherichia coli probably due tothe lipopolysaccharides present in the outer membrane thatrestrict the diffusion of compounds making it less permeable[45]The resistance can also be caused by systems of exclusionpumps that eject antimicrobial compounds from the inside ofthe bacteria before they can cause damage [39 44]

37 Effect of Ultrasound on the Physical Structure Scanningelectron micrographs of the green cactus pear seeds powderbefore and after the ultrasound treatment at magnificationsfactors of 1000x and 500x are shown in Figure 5 Beforethe ultrasound treatment and despite the previous millingprocess in the control sample it was possible to identify intactstructures of the seeds cell as well as some starch granules

(Figure 5(a)) After the ultrasound treatment the cell struc-tural damage and the variations in the shape and size of theparticles were observed (Figure 5(b)) For instance starchgranules were not observed because sonication fragmentedthese particles while cavitation phenomenon disrupted thecell structures of the seeds [47 48]

4 Conclusions

This study demonstrated that response surface methodologyand a second-order polynomial model were effective tools todetermine the optimumprocessing conditions of ultrasound-assisted extraction based on the maximum values of antiox-idant activity The results demonstrated that cactus pearseed oil has good antioxidant and antimicrobial propertiesUltrasound-assisted extraction was comparable to macera-tion but a single ultrasound process yielded less oil andlower antioxidant activity than solvent extraction (Soxhlet)Ultrasound can be considered an alternative technology forthe extraction of seed oil but further research is required todetermine the uses of the seed oil and the technology withinthe food industry and the potential of several ultrasoundcycles at the optimized conditions

Conflicts of Interest

The authors declare that there are no conflicts of interest

Acknowledgments

This work was financially supported by Programa Integral deFortalecimiento Institucional (PIFI 2014-2015) The authorsacknowledge Mexican Association CoMeNTuna (HidalgoMexico) for providing the plant materials Marıa de losAngeles Ortega-Ortega participated in this research and she

Journal of Food Quality 7

(i) (ii)

A A

(a)

(i) (ii)

(b)

Figure 5 Scanning electron micrographs of green cactus pear seed powder before (a) and after (b) ultrasound treatment (i) 1000x (ii) 500xA The black circle shows a starch granule

received her Bachelorrsquos degree in nutrition in the Universi-dad Autonoma del Estado de Hidalgo Mexico (Act no 12872016)

References

[1] L Lozano ldquoEcofisiologıa de la tuna (Opuntia ficusmdashindica (L)Mill)rdquo Horticultura Argentina vol 30 no 72 pp 37ndash52 2011

[2] LMedina-Torres J A Gallegos-Infante R F Gonzalez-Laredoand N E Rocha-Guzman ldquoDrying kinetics of nopal (Opuntiaficusmdashindica) using three different methods and their effect ontheir mechanical propertiesrdquo LWTmdashFood Science and Technol-ogy vol 41 no 7 pp 1183ndash1188 2008

[3] J A Reyes-Aguero J R Aguirre-Rivera and H M HernandezldquoSystematic notes and a detailed description of Opuntia ficusindica (L)Mill (Cactaceae)rdquoAgrociencia vol 39 no 4 pp 395ndash408 2005

[4] H I Jun M N Cha E I Yang D G Choi and Y S KimldquoPhysicochemical properties and antioxidant activity of Koreancactus (Opuntia humifusa) cladodesrdquoHorticulture Environmentand Biotechnology vol 54 no 3 pp 288ndash295 2013

[5] A Rabhi H Falleh F Limam R Ksouri C Abdelly and ARaies ldquoUpshot of the ripening time on biological activitiesphenol content and fatty acid composition of Tunisian Opuntiaficus-indica fruitrdquo African Journal of Biotechnology vol 12 no40 pp 5875ndash5885 2013

[6] M Kaur A Kaur and R Sharma ldquoPharmacological actions ofOpuntia ficus indica a reviewrdquo Journal of Applied Pharmaceuti-cal Science vol 2 no 7 pp 15ndash18 2012

[7] M R Bhatt and P S Nagar ldquoEvaluation of physicochemicalproperty and fatty acid composition ofOpuntia elatior seed oilrdquoJournal of the Professional Association for Cactus Developmentvol 15 pp 13ndash19 2013

[8] M Ennouri H Fetoui E Bourret N Zeghal F Guermazi andH Attia ldquoEvaluation of some biological parameters of Opuntiaficus indica 2 Influence of seed supplemented diet on ratsrdquo Bio-resource Technology vol 97 no 16 pp 2136ndash2140 2006

[9] SAGARPA Secretarıa de Agricultura Ganaderıa DesarrolloRural Pesca y Alimentacion Pliegos de condiciones para eluso de la marca oficial Mexico calidad suprema en tuna 2005httpwwwmexicocalidadsupremaorgassetsgaleriaPC 0462005 Tunapdf

[10] M F Ramadan and J-TMorsel ldquoOil cactus pear (Opuntia ficus-indica L)rdquo Food Chemistry vol 82 no 3 pp 339ndash345 2003

[11] K El-Mostafa Y Kharrassi A Badreddine et al ldquoNopal Cactus(Opuntia ficus-indica) as a source of bioactive compounds fornutrition health and diseaserdquo Molecules vol 19 no 9 pp14879ndash14901 2014

[12] Z Ghazi M Ramdai M L Fauconnier B El Mahi and RCheikh ldquoFatty acids sterols and Vitamin E composition of seedoil of Opuntia ficus indica and Opuntia dilenii from MoroccordquoJournal of Materials and Environmental Science vol 4 no 6 pp967ndash972 2013

[13] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extrac of Laururs nobillis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

8 Journal of Food Quality

[14] A Nawirska-Olszanska A Kita A Biesiada A Sokol-Łętowska and A Z Kucharska ldquoCharacteristics of antioxidantactivity and composition of pumpkin seed oils in 12 cultivarsrdquoFood Chemistry vol 139 no 1ndash4 pp 155ndash161 2013

[15] V Cervantes-Cardoza N E Rocha-Guzman J A Gallego-Infante M Rosales-Castro L Medina-Torres and R FGonzalez-Laredo ldquoActividad antioxidante de extractos desemilla de tres variedades de manzana (Malus domestica Borkh-Rosaceae-)rdquo Boletın Latinoamericano y del Caribe de PlantasMedicinales y Aromaticas vol 9 no 6 pp 446ndash456 2010

[16] M K M Nair P Vasudevan and K Venkitanarayanan ldquoAnti-bacterial effect of black seed oil onListeriamonocytogenesrdquoFoodControl vol 16 no 5 pp 395ndash398 2005

[17] A I Hussain F Anwar S T H Sherazi and R PrzybylskildquoChemical composition antioxidant and antimicrobial activi-ties of basil (Ocimum basilicum) essential oils depends on sea-sonal variationsrdquo Food Chemistry vol 108 no 3 pp 986ndash9952008

[18] W Liu Y J Fu Y G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[19] M T Labuschagne and A Hugo ldquoOil content and fatty acidcomposition of cactus pear seed compared with cotton andgrape seedrdquo Journal of Food Biochemistry vol 34 no 1 pp 93ndash100 2010

[20] S Zine S Gharby and M El Hadek ldquoPhysicochemical char-acterization of Opuntia ficus-indica seed oil from MoroccordquoBiosciences Biotechnology Research Asia vol 10 no 1 pp 99ndash105 2013

[21] R Azuola and P Vargas ldquoExtraccion de sustancias asistida porultrasonido (EUA)rdquoTecnologıa enMarcha vol 20 no 4 pp 30ndash40 2007

[22] M Gao and C Z Liu ldquoComparison of techniques for theextraction of flavonoids fromcultured cells of SaussureamedusaMaximrdquo World Journal of Microbiology and Biotechnology vol21 no 8-9 pp 1461ndash1463 2005

[23] B Karki B P Lamsal S Jung et al ldquoEnhancing protein andsugar release from defatted soy flakes using ultrasound tech-nologyrdquo Journal of Food Engineering vol 96 no 2 pp 270ndash2782010

[24] F Adam M Abert-Vian G Peltier and F Chemat ldquolsquoSolvent-freersquo ultrasound-assisted extraction of lipids from freshmicroal-gae cells a green clean and scalable processrdquo BioresourceTechnology vol 114 pp 457ndash465 2012

[25] T Allaf V Tomao K Ruiz and F Chemat ldquoInstant controlledpressure drop technology and ultrasound assisted extraction forsequential extraction of essential oil and antioxidantsrdquo Ultra-sonics Sonochemistry vol 20 no 1 pp 239ndash246 2013

[26] Z S Zhang L J Wang D Li S S Jiao X D Chen and ZH Mao ldquoUltrasound-assisted extraction of oil from flaxseedrdquoSeparation and Purification Technology vol 62 no 1 pp 192ndash198 2008

[27] T Zhang Z Wang and X Chen ldquoUltrasound-associatedextraction of seed oil of Korean pinerdquo Journal of Forest Researchvol 16 no 2 pp 140ndash142 2005

[28] A M Goula ldquoUltrasound-assisted extraction of pomegranateseed oilmdashkinetic modelingrdquo Journal of Food Engineering vol117 no 4 pp 492ndash498 2013

[29] Q Y Zafra-Rojas N S Cruz-Cansino A Quintero-Lira etal ldquoApplication of ultrasound in a closed system optimum

condition for antioxidants extraction of blackberry (Rubusfructicosus) residuesrdquoMolecules vol 21 no 7 p 950 2016

[30] AOAC Official Methods of Analysis AOAC InternationalGaithersburg Md USA 18th edition 2005

[31] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[32] EM Kuskoski A G Asuero AM Troncoso J Mancini-Filhoand R Fett ldquoAplicacion de diversos metodos quımicos paradeterminar actividad antioxidante en pulpa de frutosrdquo Cienciae Tecnologia de Alimentos vol 25 no 4 pp 726ndash732 2005

[33] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[34] Y Tian Z Xu B Zheng and Y Martin Lo ldquoOptimization ofultrasonic-assisted extraction of pomegranate (Punica grana-tum L) seed oilrdquo Ultrasonics Sonochemistry vol 20 no 1 pp202ndash208 2013

[35] M L Agudo ldquoTecnicas para la determinacion de compuestosantioxidantes en alimentosrdquo 2010 httpwwwanpebadajozesautodidactaautodidacta archivosnumero 9 archivosl amedinapdf

[36] S K Ho C P Tan Y Y Thoo F Abas and C W HoldquoUltrasound-assisted extraction of antioxidants inMisai Kucing(Orthosiphon stamineus)rdquo Molecules vol 19 no 8 pp 12640ndash12659 2014

[37] S R Kirk R Sawyer and H Egan ldquoMetodos quımicos gen-eralesrdquo inComposicion y Analisis de Alimentos pp 25ndash29 Com-panıa editorial continental Ciudad de Mexico Mexico 2002

[38] S Vazquez S OrsquoNeill and M Legnani ldquoImportancia de loscoliformes en los alimentosrdquo 2013 httpwwwmontevideogubuysitesdefaultfilesimportancia de los coliformes en losalimentospdf

[39] C A Gomez-Alvarez A L Leal-Castro M J Perez de Gonza-lez and M L Navarrete-Jimenez ldquoMecanismos de resistenciaen Pseudomonas aeruginosa entendiendo a un peligroso ene-migordquo Revista de la Facultad de Medicina de la UniversidadNacional de Colombia vol 53 no 1 pp 27ndash34 2005

[40] S D Kominos C E Copeland B Grosiak and B Postic ldquoIntro-duction of Pseudomonas aeruginosa in to a hospital via vegeta-blesrdquo Applied Microbiology vol 24 no 4 pp 567ndash570 1972

[41] NOM Norma Oficial Mexicana NOM-210-SSA1-2014 Pro-ductos y servicios Metodos de prueba microbiologicosDeterminacion de microorganismos indicadores Determina-cion de microorganismos patogenos 2014 httpdofgobmxnota detallephpcodigo=539868ampfecha=26062015

[42] F Reyes-Jurado E Palou and A Lopez-Malo ldquoMetodos deevaluacion de la actividad antimicrobiana y de determinacionde los componentes quımicas de los aceites esencialesrdquo TemasSelectos de Ingenierıa de Alimentos vol 8 pp 68ndash78 2014

[43] D Zekaria ldquoLos aceites esenciales una alternativa a los antimi-crobianosrdquo 2015 httpwwwwpsa-aecaesaeca imgs docswpsa1182855355apdf

[44] DM Livermore ldquoMultiplemechanisms of antimicrobial resist-ance in Pseudomonas aeruginosa our worst nightmarerdquo Clini-cal Infectious Diseases vol 34 no 5 pp 634ndash640 2002

[45] M Viuda-Martos M A Mohamady J Fernandez-Lopez et alldquoIn vitro antioxidant and antibacterial activities of essentials oilsobtained from Egyptian aromatic plantsrdquo Food Control vol 22no 11 pp 1715ndash1722 2011

Journal of Food Quality 9

[46] X Feas L M Estevinho C Salinero et al ldquoTriacylglyc-eride antioxidant and antimicrobial features of virgin camelliaoleiferaC reticulata andC sasanqua oilsrdquoMolecules vol 18 no4 pp 4573ndash4587 2013

[47] R G Earnshaw ldquoUltrasound a new opportunity for foodpreservationrdquo in Ultrasound in Food Processing M J W PoveyandT JMason Eds pp 183ndash192 Editorial BlackAcademic andProfessional New York NY USA 1998

[48] M Vinatoru ldquoAn overview of the ultrasonically assisted extrac-tion of bioactive principles from herbsrdquo Ultrasonics Sonochem-istry vol 8 no 3 pp 303ndash313 2001

Research ArticleAntioxidant and Antimicrobial Properties of CactusPear (Opuntia) Seed Oils

Esther Ramiacuterez-Moreno1 Raquel Carintildeo-Corteacutes2 Nelly del Socorro Cruz-Cansino1

Luis Delgado-Olivares1 Joseacute Alberto Ariza-Ortega1 Vanessa Yelina Montantildeez-Izquierdo3

Mariacutea Manuela Hernaacutendez-Herrero3 and Tomaacutes Filardo-Kerstupp4

1Academic Area of Nutrition Health Sciences Institute Autonomous University of Hidalgo State 42160 Pachuca HGO Mexico2Academic Area of Medicine Autonomous University of Hidalgo State Eliseo Ramırez Ulloa 400 42090 Pachuca HGO Mexico3Department of Food Hygiene Faculty of Veterinary Autonomous University of Barcelona 08193 Bellaterra Spain4Academic Area of Chemistry Basic Science and Engineering Institute Autonomous University of Hidalgo StateCarretera Pachuca-Tulancingo Km 45 Mineral de la Reforma 42183 Pachuca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 23 January 2017 Accepted 5 April 2017 Published 26 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Esther Ramırez-Moreno et alThis is an open access article distributed under the Creative CommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Seed oils from two Mexican varieties of cactus pear (green Opuntia albicarpa and red Opuntia ficus indica) were extracted withdifferent solvents (hexane ethanol and ethyl acetate) to evaluate their antioxidant activity The seed oil with higher antioxidantactivitywas selected to evaluate antimicrobial activityThe fatty acid profilewas analyzed by gas chromatography-mass spectrometry(GC-MS) Oil from green cactus pear seeds obtained with ethanol and ethyl acetate exhibited higher antioxidant activity (119901 lt 005)of 323 and 316 120583mol TE20mg (p lt 005) respectively compared to red cactus pear seed oil (asymp274 and 247 120583mol TE20mgwith ethyl acetate and ethanol resp) The oil obtained with ethanol and higher antioxidant activity was used to determine theantimicrobial activity Both cactus pear oils produced a microbial inhibition zone in most of the microorganisms evaluatedparticularly Saccharomyces cerevisiae which had similar diameter (38ndash40mm) The oil fatty acids profiles of both varieties weresimilar and exhibited a high content of linoleic acid while two fatty acids (linolenic and behenic) found in red cactus pear were notobserved in the green variety

1 Introduction

A relatively untapped source of lipid and protein rawmaterialis the by-product of fruit-processing plants Millions ofpounds of fruit seeds are discarded yearly causing disposalproblems while proper utilization of these waste productscould lead to an important new source of oil and meal [1]Seeds of fruits collect at least some cytoplasmic lipid bodies asmajor storage reserve for lipid accumulation [2] Fruit seedsoils are of great interest because they are edible oils with highdegree of unsaturation antioxidant radical scavenging prop-erties [3ndash8] and a broad spectrum of antimicrobial activity[9ndash15] Therefore the oil from plants can be potentially usedby the food industry for the manufacturing of ldquonaturalrdquo orldquogreenrdquo safe foods [16] and extend shelf-life [17 18]

The oil from cactus pear seed has been found to havean appreciable amount of oil with high levels of unsaturatedfatty acids [19] with antioxidant [20 21] and antimicrobialactivity [22] as well as cardioprotective antithrombotic anti-inflammatory antiarrhythmic hypolipidemic and antihy-perglycemic effect [23 24] These properties are of interestfor the pharmaceutical and food industry However theconcentration and effectiveness of these oils may vary amongcultivars or varieties crop environmental factors (eg lighttemperature and type of soil nutrients) or methods andsolvents used for their extraction Therefore the purpose ofthis research was to determine the antioxidant and antimi-crobial activity and fatty acid profile of the oil obtained fromtwo Mexican varieties of cactus pear (Opuntia albicarpa andOpuntia ficus indica) seeds extracted with different solvents

HindawiJournal of Food QualityVolume 2017 Article ID 3075907 8 pageshttpsdoiorg10115520173075907

2 Journal of Food Quality

2 Materials and Methods

21 Plant Material Two Mexican varieties of cactus pear(Opuntia albicarpa and Opuntia ficus indica) fruit green (cvReyna) and red (cv Rojo Pelon) respectively were providedby theMexican association CoMeNTuna (ConsejoMexicanodel Nopal y la Tuna AC Actopan Hidalgo Mexico) Fruitsfree of external injuries were selected washed and manuallypeeled Cactus pear seeds were obtained after juice wasextracted stirring the pulpwith an industrial blender (38BL52LBC10 Waring Comercial USA) and passing it through aconventional strainer The seeds retained were washed in thestrainer with water until pulp residues were removed

22 Powder Seed and Oil Extraction Green cactus pear seeds(GCPS) and red cactus pear seeds (RCPS)were sun-dried andthen grounded (Cyclotec 1093 Tecator Sweden) to a 1mmdiameter mesh and stored at minus32∘C until further analysisTheseed oil was extracted as follows 25 g of powdered seeds wasmixed with 500mL of solvents with varying polarities (hex-ane ethanol and ethyl acetate) and the obtained residue wasreextracted until extraction solvents become colourless Allthe extracts were filtered through filtration paper Whatmannumber 1 and the filtered extracts were collected for furtherdrying and removal of the remaining solvent at 50∘C using arotary evaporator (BUCHI R-200 Switzerland) All extractswere placed in plastic bottles and then stored at minus20∘C untilused The oils obtained were used to further analysis

23 Free Radical Scavenging Assay The free radical scaven-ging activity was measured using 11-diphenyl-2-picrylhy-drazyl (DPPH∙) radical as described byMorales and Jimenez-Perez [25] A volume of 500 120583L of ethanolic DPPH∙ solution(74mg100mL) was added to a sample aliquot of 100 120583Lplaced in vialsThemixturewas left to sit at room temperaturefor 1 h and then was vortexed and centrifuged at 3000 rpm for10 minutesThe absorbance of the supernatant was measuredat 520 nm in amicroplate reader (PowerWave XSUV-Bioteksoftware KC Junior USA) and 120583mol of Trolox equivalentsper 20 milligram (120583mol TE20mg) of sample was obtainedOil samples with best antioxidant capacity obtained from thedifferent solvents were used for the antimicrobial analysis

24 Antimicrobial Activity Eight standard freeze-dried cul-tures of bacteria Candida albicans (ATCC 10231) Escherichiacoli O58H21 (ATCC 10536) Escherichia coli O157H7(CCUG 44857) Staphylococcus aureus (ATCC 13565) Liste-ria monocytogenes (CCUG 15526) Pseudomonas aeruginosa(ATCC 15442) Saccharomyces cerevisiae (CECT 1942) andSalmonella Typhi (CCUG 29478) were obtained in ther-mosealed vials from the Spanish Type Culture Collection(Autonomous University of Barcelona Barcelona Spain)Freeze-dried cultures were rehydrated in tryptone soy brothat 37∘C for 18 h and then were used to inoculate tryptone soyagar and malt extract agar plates all microorganisms wereincubated at 37∘CexceptCandida albicans and Saccharomycescerevisiae which were incubated at 25∘C Individual colonies

were maintained on specific agar slants stored at 4∘C andsubcultured every 15 days

Disc Diffusion Assay Antimicrobial activity of oil extractedfromGCPS andRCPSwas carried out using the disc diffusionmethod [26] Petri plates were filled with sim20mL of steriletryptone soy agar for bacteria and malt extract agar for fungiThe test cultures were swabbed on the top of the solidifiedmedia and allowed to dry for 10 minutes Serial dilutions(10ndash50 120583gmL) of the seed oil from a stock solution (1mgmL)were prepared in 20 DMSO and 10 120583L loaded onto thesterile blank discs (BBL Sensi-Disc) of 6 millimetersof diameter On the media surface the loaded disks wereplaced and left for 30 minutes at room temperature toallow compound diffusion The seed oil was serially dilutedin MuellerndashHinton broth medium and duplicate tubes ofeach dilution (10ndash100 120583gmL) were inoculated with 5 times106 cells of the test bacteria strain and culturesThe antibioticagents Sensi-Disc streptomycin ampicillin and sulfamethox-azoletrimethoprim (BBL Sensi-Disc) were used as positivecontrols at the same concentration level After plates wereincubated at 37∘C for 24 h the diameters of the inhibitionzones were recorded in millimeters Three independentrepetitions were performed and tests were made in triplicate

25 GC-MS Analysis The GC-MS analysis was performedwith a GC-MS HP-5890 (Hewlett-Packard Company PaloAlto California USA) equipped with a Flame IonizationDetector (FID) and a ZB-WAX fused silica capillary column(60m times 025mm id times 025mm film thickness) packedwith 5 phenylmethylpolysiloxane (Phenomenex TorranceCA) To obtain the methyl esters the cactus pear seed oilswere saponified and derivatized using KOH 1N (IUPAC1969) Changes in the fatty acids of the oils samples werecompared against a standard mixture of 37 components offatty acids methyl esters (FAMEs) (Food Industry FAMEsMix Restek) comprised by methyl esters with chains C40C60 C80 C100 C110 C120 C130 C140 C141 C150C151 C160 C161 C170 C171 C180 C181n9c C181n9tC182n6c C182n6t C183n6 C183n3 C200 C201n9 C202C203n6 C203n3 C204n6 C205n3 C210 C220 C221n9C222 C226n3 C230 C240 and C241n9 The samplevolume injected was of 2 120583L (split ratio 20 2) at an injectorand detector temperatures of 225 and 225∘C respectively N2was used as carrier gas at a flow rate of 12mLsdotminminus1 Fattyacids were calculated as percentage of total FAMEs

26 Statistical Analysis All values were obtained by triplicateand expressed as means plusmn standard deviations (SD) Datawere analyzed using the SPSS V15 software (SPSS InstituteInc Cary NC) An ANOVA was carried out to determinedifferences between oils extracted as well as its antimicrobialactivity that were significant at the 5 level of probability anda Tukey test was used for comparison of data

3 Results and Discussion

31 Yield Comparison between Extraction Solvents Hexaneethanol and ethyl acetate were used to extract the oil from

Journal of Food Quality 3

1183

669

1013

511

106

381

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

2

4

6

8

10

12

14

Oil

yiel

d (

)

Figure 1 Oil yields () extracted from GCPS and RCPS withhexane ethanol and ethyl acetate

cactus pear seeds The extraction yields are compared inFigure 1 which shows that the higher amount of oil () wasobtained from the green cultivar and that yield depended onthe solvent used Oil extraction with hexane was higher forboth fruit varieties (1183 for GCPS and 689 for RCPS)followed by ethanol which reached the same yield as ethylacetate for GCPS (asymp10) Ethyl acetate was the least effectivesolvent for RCPS The extraction yields were similar to thosereported (asymp7 to 11) for several varieties of Opuntia ficusindica [27ndash29] This extraction yields will vary depending onseveral factors as fruit variety harvest period maturationgeographic region percentage of oil in the seed and chemicalcompounds found in the source and by the extractionmethod[30] Researchers have determined that solvent extractioncombinedwith othermethods could increase oil yield as highpressure or supercritical fluid combined with solvent reacheda yield of 933 from tobacco seeds (Nicotiana tabacum L)while sonication and Soxhlet reached a 775 and 1372respectively [31]

32 Free Radical Scavenging Activity Solvent extraction isusually used for isolation of antioxidants the extractiondepends on the solvent selected based on the different antiox-idant compounds with varying polarity [32 33] DPPH is astable free radical that accepts an electron or hydrogen radicalto become a stable diamagnetic molecule [34 35]The DPPHassay has also been used to predict the oxidative stability ofedible oils [36 37] The antioxidant activity determined byDPPH of the oil extracted from RCPS and GCPS is shownin Figure 2 Oil from the GCPS extracted with ethanol andethyl acetate exhibited the higher antioxidant activity (119901 lt005) of 323 and 316 120583mol TE20mg extract respectivelyfollowed by RCPS oil extracted with ethyl acetate (274120583molTE20mg extract) and ethanol (247 120583mol TE20mg extract)These results demonstrate that the extraction solvent hada significant effect on the free radical scavenging capacityof the oil where the hexane had the lower values In ourstudy the green variety exhibited a higher antioxidant activityregardless of solvent Different results may depend mainly

e

d

a

c

ab

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

50

100

150

200

250

300

350

휇m

ol T

E20

mg

extr

act

Figure 2 Antioxidant activity of GCPS and RCPS oils extractedwith different solvents andashdDifferent letters above bars indicate thatsamples are significantly different (119901 lt 005)

on the content and concentration of bioactive compounds inthe oil but other factors such as solvent polarity solubilityof the extracts in different testing systems stereoselectivityof the radicals [38] and strong synergism between fattyacids [6] may affect antioxidant activities Other studies havealso reported diverse antioxidant activity among oils fromdifferent Opuntia varieties [20 39 40]

33 Antibacterial and Antifungal Activity The most recom-mended way to prevent or inhibit microbial growth in foodsis the use of food preservatives Essential oils are secondarymetabolites of plants that have wide applications in thefood flavoring and preservative industry [41] Six differentbacterium and two fungi species were used to screen theantimicrobial potential of the oils extracted from the twovarieties of cactus pear seeds Oil extracted with ethanolexhibited the highest antioxidant activity and therefore itwas used to evaluate the antibacterial and antifungal activityFigure 3 shows the results from the microbial assay wheremost microorganisms showed an inhibition zone whenexposed to GCPS and RCPS oils except Salmonella Typhiand Escherichia coli O157H7 (image not shown) From thesetwo microorganisms the first showed an inhibition zonein the presence of antibiotic agents streptomycin (S) ampi-cillin (AMP) and sulfamethoxazoletrimethoprim (STX) indiameters of 146 113 and 273mm respectively (Table 1)while Escherichia coli O157H7 was only inhibited by SXT(253mm) which agrees with other reports of multiantibi-otic resistance of E coli O157H7 due to the presence ofthe gene cluster AMR-SSuT [42] and production of beta-lactamase [43] On the other hand Saccharomyces cerevisiaewas highly inhibited (38ndash40mm) by the extracted oils butgrew in presence of the antimicrobial agents (Figure 3)Similar results were observed for Candida albicans althoughinhibition zones were smaller and similar for both oilsThese observations demonstrate that certain compounds inthe cactus pear seed oil have antimicrobial activity Otherresearchers also reported similar observations for cactus

4 Journal of Food Quality

Table 1 Diameters of growth inhibition zones (mm) in the presence of oil extracted from cactus pear seeds and conventional antimicrobialsA

Microbial cultures Extract Antimicrobial agentGCPS RCPS S AMP SXT

Saccharomyces cerevisiae (CECT1942) 383 plusmn 42a 403 plusmn 45a ND ND NDEscherichia coli O58H21 (ATCC 10536) 119 plusmn 07d 114 plusmn 09d 195 plusmn 14b 178 plusmn 15c 299 plusmn 09a

Escherichia coli O157H7 (CCUG 44857) NDB ND ND ND 253 plusmn 10Staphylococcus aureus (ATCC 13565) 121 plusmn 10c 111 plusmn 11c 183 plusmn 09b 281 plusmn 15a 333 plusmn 19a

Listeria monocytogenes (CCUG15526) 133 plusmn 15c 114 plusmn 09d 213 plusmn 12a 173 plusmn 08c 376 plusmn 18a

Pseudomonas aeruginosa (ATCC15442) 164 plusmn 21c 151 plusmn 20c 201 plusmn 15b 241 plusmn 25a 366 plusmn 29a

Salmonella typhi (CCUG29478) ND ND 146 plusmn 04b 113 plusmn 18c 273 plusmn 08a

Candida albicans (ATCC 10231) 111 plusmn 10a 110 plusmn 18a ND ND NDAInhibition zone diameters for oil and reference antibiotics are means plusmn SE of three replicas GCPS green cactus pear seed oil extract RCPS red cactus pearseed oil extract S streptomycin (10120583gdisc) AMP ampicillin (10 120583gdisc) and SXT sulfamethoxazoletrimethoprim (10120583gdisc) BND not detected activityandashdDifferent letters in the same row indicate significant differences

RG

SXT

S

AMP

(a)

RG

SXT

S

AMP

(b)

R G

SXTS

AMP

(c)

RG

SXTS

AMP

(d)

RG

SXT

S

AMP

(e)

R G

SXT

S

AMP

(f)

Figure 3 Antimicrobial activity of oil extracted from green cactus pear (G) oil extracted from red cactus pear seeds (R) streptomycin(S) ampicillin (AMP) and sulfamethoxazoletrimethoprim (SXT) Candida albicans (ATCC 10231) (a) Escherichia coli O58H21 (ATCC10536) (b) Staphylococcus aureus (ATCC 13565) (c) Listeria monocytogenes (CCUG15526) (d) Pseudomonas aeruginosa (ATCC15442) (e)Saccharomyces cerevisiae (CECT1942) (f)

pear fruit cv Opuntia stricta [44] and for other plants asfennel (Foeniculum vulgare L) and chamomile (Matricariachamomilla L) [5] Differences in the levels of antimicrobialactivity may be partially attributed to variable chemicalcomposition of the oils [45] Mnayer et al [46] suggestedthat oil compounds can act on different bacterial structureswhile Gill et al [47] mentioned that whole oils have a greater

antibacterial activity than the major component mixed sothat minor components are critical for the activity and exerta synergistic effect [16 48 49]

In the present study the antimicrobial activity of cactuspear seed oil was more effective against fungi comparedto bacteria cultures These interesting results suggest thatthere is a link between the oil chemical contents and the

Journal of Food Quality 5

Table 2 Percentages of FAMEs in crude cactus pear seed oil extracts

FAMEs Green cactus pear seed oil extract Red cactus pear seed oil extractC140 0078 plusmn 000 0066 plusmn 001C160 12327 plusmn 009 12887 plusmn 002C161 0429 plusmn 002 0570 plusmn 001C162 0073 plusmn 000 0540 plusmn 000C170 0060 plusmn 001 0075 plusmn 000C180 3436 plusmn 001 3389 plusmn 007C181 16215 plusmn 003 17061 plusmn 001C182 67448 plusmn 008 65407 plusmn 001C183 Ni 0372 plusmn 001C220 Ni 0160 plusmn 001Means of 3 replicates plusmn SE Ni not identified

140

160

181

182

18017

016

116

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(a)14

0 161

162

170

180

181

182

183

220

160

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(b)

Figure 4 Chromatograms of FAMEs of cactus pear seed oil extract (a) Green cactus pear seed oil extract (b) red cactus pear seed oil extractIn both oils extracts were identified myristic (C140) palmitic (C160) palmitoleic (C161 cis-9) hexadecadienoic (C162 cis-9 12) margaric(C170) stearic (C180) oleic (C181 cis-9) linoleic (C182 cis-9 12) except linolenic (C183 cis-6 9 12) and behenic (C220) fatty acids thatwere identified only in red cactus pear seed

antimicrobial activity The membrane disruption could beone mechanism of action by inactivating microbial adhesionenzymes and proteins transport [15 46] RCPS and GCPSextracts inhibited most of the evaluated bacterial and fungispecies (Table 1) however antimicrobial activity was notdetected for Salmonella Typhi which is a gram-negative bac-terium In general gram-negative bacteria have an effectiveoutermembrane that restricts the penetration of amphipathiccompounds and has a mechanism to extrude toxins across[50]Thismay explain the apparent antimicrobial ineffective-ness of the oils against the permeability barrier in addition tothe presence of multidrug resistance encoding plasmids [51]

34 Fatty Acid Profile FAMEs chromatograms and percent-ages are shown in Figure 4 and Table 2 Cactus pear seed oilscontained saturated and unsaturated fatty acids the linoleicfatty acid being the predominant (674 and 654 in GCPSand RCPS oils resp) Minimal amounts of myristic (C140)palmitoleic (C161) hexadecadienoic (C162) and margaric(C170) fatty acids in both oils were also identified The fattyacids profiles of the two cactus pear varieties were similarhowever theGCPS had a slightly higher content of the linoleicacid (C182)while the fatty acids linolenic (C183) and behenic(C220) were in minimal amounts only in the RCPS

Different studies have established that factors as cultivartype temperature and harvest time have a strong influence inparameter as pH Brix vitamin C sugars and fat content [5253] Oumato et al [52] found differences in linoleic fatty acid(C182) content among cactus pear cultivars In other studythe oleic acid (C181) content was significantly influenced bythe cultivar and location interaction [53] providing uniquecharacteristics to the oil

In comparison with other plants oils the linoleic acid(C182) content of the cactus pear fruit was similar to thelevels reported for sunflower oil (62) [54] and higher thanwheat germ oil (5505) [55] and soybean oil (5270)[56] The contents of other FAMEs in cactus pear varietiessuch as palmitic (C160) oleic (C181) and stearic (C180)were similar to those reported for Castilla blackberry (Rubusglaucus Benth) with 1124 passion fruit (Passiflora edulis)with 1547 [57] and grape (Vitis vinifera) with 35 [58]

Other researchers have reported similar fatty acidsprofile to our findings for different plant materials andhave analyzed the antimicrobial effectiveness against dif-ferent microorganisms For instance fatty acids found inAllium cepa were found to effectively inhibit Staphylococcusaureus Bacillus subtilis Enterococcus faecalis Escherichia coliand Klebsiella pneumoniae [59] Oil extracted from SwieteniaMacrophylla king seed oil inhibited growth of S aureus

6 Journal of Food Quality

S Typhimurium and P aeruginosa [60] These studies de-monstrate that seed oil can inhibit fungi and bacteria buttheir efficacy would depend on their concentration levels andspecific pathogen [15]

4 Conclusions

Oil yield from the green cactus pearwas higher in comparisonto the red cultivar andwas also influenced by the solvent usedHexane exhibited high extraction yield while oils extractedwith ethanol had the better antioxidant activity The resultsdemonstrated that oil extracts from both varieties have anoticeable antimicrobial activity against gram-positive andgram-negative bacteria comparable to antimicrobial com-pounds such as ampicillin streptomycin and sulfamethoxa-zoletrimethoprimThis research provides further incentivesto develop additives for the food cosmetic and pharmaceu-tical sectors seeking natural compounds with antimicrobialactivity Further studies are needed to determine the specificcomponent responsible for the antimicrobial activity in cac-tus pear seeds oil and determine the optimum levels of oilextract and the antimicrobial effectiveness in the foodmatrix

Additional Points

Practical Application Our results suggest that the oilsextracted from cactus pear seeds have the potential to be usedas a natural antioxidant and antimicrobial agents by the foodcosmetic and pharmaceutical sectors

Conflicts of Interest

The authors have declared that no conflicts of interest exist

Acknowledgments

This study was possible thanks to the financial supportfrom the Programa Integral de Fortalecimiento Institucional(PIFI 2013ndash2015) Mexico This research project was partiallysupported by the Food Hygiene Department Faculty ofVeterinary from the Autonomous University of BarcelonaSpain The authors acknowledge the Mexican associationCoMeNTuna (Consejo Mexicano del Nopal y la TunaHidalgo Mexico) for providing the plant materials

References

[1] B S Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Acids in Foods and Their Health Implications pp 263ndash301 CRC Press 3rd edition 2007

[2] D J Murphy I Hernandez-Pinzon and K Patel ldquoRole oflipid bodies and lipid-body proteins in seeds and other tissuesrdquoJournal of Plant Physiology vol 158 no 4 pp 471ndash478 2001

[3] A Kedia B Prakash P KMishra andN K Dubey ldquoAntifungaland antiaflatoxigenic properties of Cuminum cyminum (L)seed essential oil and its efficacy as a preservative in storedcommoditiesrdquo International Journal of Food Microbiology vol168-169 pp 1ndash7 2014

[4] S Singh S S Das G Singh C SchuffM P de Lampasona andC A Catalan ldquoComposition in vitro antioxidant and antimi-crobial activities of essential oil and oleoresins obtained fromblack cumin seeds (Nigella sativa L)rdquo BioMed Research Inter-national vol 2014 Article ID 918209 10 pages 2014

[5] M H H Roby M A Sarhan K A-H Selim and K I KhalelldquoAntioxidant and antimicrobial activities of essential oil andextracts of fennel (Foeniculum vulgare L) and chamomile(Matricaria chamomilla L)rdquo Industrial Crops and Products vol44 pp 437ndash445 2013

[6] G Kavoosi A Tafsiry A A Ebdam and V Rowshan ldquoEvalua-tion of antioxidant and antimicrobial activities of essential oilsfrom carum copticum seed and ferula assafoetida latexrdquo Journalof Food Science vol 78 no 2 pp T356ndashT361 2013

[7] S Lalas O Gortzi V Athanasiadis J Tsaknis and I ChinouldquoDetermination of antimicrobial activity and resistance tooxidation of Moringa peregrina seed oilrdquoMolecules vol 17 no3 pp 2330ndash2334 2012

[8] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extract of Laurus nobilis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

[9] R S Bhat and S Al-daihan ldquoAntimicrobial activity of Litchichinensis and Nephelium lappaceum aqueous seed extractsagainst some pathogenic bacterial strainsrdquo Journal of King SaudUniversitymdashScience vol 26 no 1 pp 79ndash82 2014

[10] J M Silvan E Mingo M Hidalgo S de Pascual-Teresa A VCarrascosa and A J Martinez-Rodriguez ldquoAntibacterial activ-ity of a grape seed extract and its fractions against Campylobac-ter spprdquo Food Control vol 29 no 1 pp 25ndash31 2013

[11] K Rakholiya M Kaneria D Desai and S Chanda ldquoAntimi-crobial activity of decoction extracts of residual parts (seedand peels) ofMangifera indica L var Kesar against pathogenicand food spoilage microorganismrdquo in Microbial pathogens andstrategies for combating them science technology and educationA Mendez-Vilas Ed vol 2 pp 850ndash856 2013

[12] N A Hasan M Z Nawahwi and H Ab Malek ldquoAntimicrobialactivity ofNigella sativa seed extractrdquo Sains Malaysiana vol 42no 2 pp 143ndash147 2013

[13] Z I Sajid F Anwar G Shabir G Rasul KM Alkharfy and A-H Gilani ldquoAntioxidant antimicrobial properties and phenolicsof different solvent extracts from bark leaves and seeds ofPongamia pinnata (L) pierrerdquoMolecules vol 17 no 4 pp 3917ndash3932 2012

[14] M Khoobchandani B K Ojeswi N Ganesh et al ldquoAntimicro-bial properties and analytical profile of traditional Eruca sativaseed oil comparisonwith various aerial and root plant extractsrdquoFood Chemistry vol 120 no 1 pp 217ndash224 2010

[15] V Kesari A Das and L Rangan ldquoPhysico-chemical charac-terization and antimicrobial activity from seed oil of Pongamiapinnata a potential biofuel croprdquo Biomass and Bioenergy vol34 no 1 pp 108ndash115 2010

[16] K Carovic-Stanko S Orlic O Politeo et al ldquoComposition andantibacterial activities of essential oils of seven Ocimum taxardquoFood Chemistry vol 119 no 1 pp 196ndash201 2010

[17] MM Tajkarimi S A Ibrahim andDO Cliver ldquoAntimicrobialherb and spice compounds in foodrdquo Food Control vol 21 no 9pp 1199ndash1218 2010

[18] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

Journal of Food Quality 7

[19] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[20] W Liu Y-J Fu Y-G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[21] B Matthaus and M M Ozcan ldquoHabitat effects on yield fattyacid composition and tocopherol contents of prickly pear(Opuntia ficus-indica L) seed oilsrdquo Scientia Horticulturae vol131 pp 95ndash98 2011

[22] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research vol 27 no 14 pp 1305ndash1314 2013

[23] KMobraten TMHaug C R Kleiveland and T Lea ldquoOmega-3 and omega-6 PUFAs induce the same GPR120-mediatedsignalling events but with different kinetics and intensity inCaco-2 cellsrdquo Lipids in Health and Disease vol 12 no 1 ArticleID 101 2013

[24] A BerraaouanA ZiyyatHMekhfi et al ldquoEvaluation of antidi-abetic properties of cactus pear seed oil in ratsrdquo PharmaceuticalBiology vol 52 no 10 pp 1286ndash1290 2014

[25] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[26] P R Murray E J Baron M A Pfaller F C Tenover and R HYolkeManual of Clinical Microbiology 1995 Washington DCUSA

[27] M Ennouri H Fetoui E Bourret N Zeghal and H AttialdquoEvaluation of some biological parameters of Opuntia ficusindica 1 Influence of a seed oil supplemented diet on ratsrdquoBioresource Technology vol 97 no 12 pp 1382ndash1386 2006

[28] Y Habibi L Heux M Mahrouz and M R Vignon ldquoMorpho-logical and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruitsrdquo Carbohydrate Polymers vol 72 no 1pp 102ndash112 2008

[29] MMoudenM Boujnah S Salmaoui S Zantar and A DouiraldquoEffect of two extraction methods and harvest period andperformance there statement of fatty oils of figs pear seedrdquoInternational Journal of Pure amp Applied Bioscience vol 4 no1 pp 1ndash8 2016

[30] A El Finti M Belayadi R El Boullani F Msanda and A ElMousadik ldquoAssessment of some agro-technological parametersof cactus pear fruit (Opuntia ficus-indica Mill) in Moroccocultivarsrdquo Journal of Medicinal Plants Research no 7 pp 2574ndash2583 2013

[31] S Majdi M Barzegar A Jabbari and M Agha AlikhanildquoSupercritical fluid extraction of tobacco seed oil and itscomparison with solvent extraction methodsrdquo Journal of Agri-cultural Science and Technology vol 14 no 5 pp 1043ndash10512012

[32] E M Marinova and N V Yanishlieva ldquoAntioxidative activity ofextracts from selected species of the family Lamiaceae insunflower oilrdquo Food Chemistry vol 58 no 3 pp 245ndash248 1997

[33] Y-Y Soong and P J Barlow ldquoAntioxidant activity and phenoliccontent of selected fruit seedsrdquo Food Chemistry vol 88 no 3pp 411ndash417 2004

[34] J R Soares T C P Dinis A P Cunha and L M AlmeidaldquoAntioxidant activities of some extracts of Thymus zygisrdquo FreeRadical Research vol 26 no 5 pp 469ndash478 1997

[35] I GulcinMOktay E Kirecci and O I Kufrevioglu ldquoScreeningof antioxidant and antimicrobial activities of anise (Pimpinellaanisum L) seed extractsrdquo Food Chemistry vol 83 pp 371ndash3822003

[36] J Lee H Chung P-S Chang and J Lee ldquoDevelopment of amethod predicting the oxidative stability of edible oils using 22-diphenyl-1-picrylhydrazyl (DPPH)rdquo Food Chemistry vol 103no 2 pp 662ndash669 2007

[37] A Fazio P Plastina J Meijerink R F Witkamp and BGabriele ldquoComparative analyses of seeds of wild fruits ofRubus and Sambucus species from Southern Italy fatty acidcomposition of the oil total phenolic content antioxidant andanti-inflammatory properties of the methanolic extractsrdquo FoodChemistry vol 140 no 4 pp 817ndash824 2013

[38] R L Prior X Wu and K Schaich ldquoStandardized methods forthe determination of antioxidant capacity and phenolics infoods and dietary supplementsrdquo Journal of Agricultural andFood Chemistry vol 53 no 10 pp 4290ndash4302 2005

[39] A Cardador-Martınez C Jimenez-Martınez and G SandovalldquoRevalorization of cactus pear (Opuntia spp) wastes as a sourceof antioxidantsrdquo Ciencia e Tecnologia de Alimentos vol 31 no3 pp 782ndash788 2011

[40] Z Ghazi M Ramdani M Tahri et al ldquoChemical compositionand antioxidant activity of seeds oils and fruit juicerdquo Journalof Materials and Environmental Science vol 6 no 8 pp 2338ndash2345 2015

[41] V K Bajpai K-H Baek and S C Kang ldquoControl of Salmonellain foods by using essential oils a reviewrdquo Food ResearchInternational vol 45 no 2 pp 722ndash734 2012

[42] K Ziebell R P Johnson A M Kropinski et al ldquoGenecluster conferring streptomycin sulfonamide and tetracyclineresistance in Escherichia coli O157H7 phage types 23 45 and67rdquo Applied and Environmental Microbiology vol 77 no 5 pp1900ndash1903 2011

[43] O Chandra K J Putra and I Wayan ldquoAntibiotic resistanceprofiles of Escherichia coli O157H7 in cattle at Suth-KutaBadung Regency Bali Indonesiardquo Global Veterinaria vol 15no 5 pp 480ndash484 2015

[44] E Moosazadeh M R Akhgar and A Kariminik ldquoChemicalcomposition and antimicrobial activity of Opuntia stricta Fessential oilrdquo Journal of Biodiversity and Environmental Sciencesvol 4 pp 94ndash101 2014

[45] S Burt ldquoEssential oils their antibacterial properties and poten-tial applications in foods - a reviewrdquo International Journal ofFood Microbiology vol 94 no 3 pp 223ndash253 2004

[46] D Mnayer A-S Fabiano-Tixier E Petitcolas et al ldquoChemicalcomposition antibacterial and antioxidant activities of sixessentials oils from the Alliaceae familyrdquo Molecules vol 19 no12 pp 20034ndash20053 2014

[47] A O Gill P Delaquis P Russo and R A Holley ldquoEvaluationof antilisterial action of cilantro oil on vacuum packed hamrdquoInternational Journal of FoodMicrobiology vol 73 no 1 pp 83ndash92 2002

[48] M Turgis K D Vu C Dupont and M Lacroix ldquoCombinedantimicrobial effect of essential oils and bacteriocins againstfoodborne pathogens and food spoilage bacteriardquoFoodResearchInternational vol 48 no 2 pp 696ndash702 2012

[49] H Zengin and A H Baysal ldquoAntibacterial and antioxi-dant activity of essential oil terpenes against pathogenic andspoilage-forming bacteria and cell structure-activity relation-ships evaluated by SEM microscopyrdquo Molecules vol 19 no 11pp 17773ndash17798 2014

8 Journal of Food Quality

[50] G Tegos F R Stermitz O Lomovskaya and K Lewis ldquoMul-tidrug pump inhibitors uncover remarkable activity of plantantimicrobialsrdquo Antimicrobial Agents and Chemotherapy vol46 no 10 pp 3133ndash3141 2002

[51] M Baltazar A Ngandjio K E Holt et al ldquoMultidrug-resistantSalmonella enterica serotype typhi Gulf of Guinea RegionAfricardquo Emerging Infectious Diseases vol 21 no 4 pp 655ndash6592015

[52] J Oumato S ZriraM Boujnah andB Saidi ldquoEffect ofmaturitystage onmorphological and chemical characteristics ofOpuntiaficus indica from Moroccordquo International Journal of Innovationand Applied Studies vol 20 no 1 pp 400ndash410 2017

[53] M deWit A Hugo N Shongwe and R van derMerwe ldquoEffectof cultivar season and locality on lipid content and fatty acidcomposition of cactus pear seed oilrdquo South African Journal ofPlant and Soil no 33 pp 279ndash288 2016

[54] Australian Oilseeds Federation Incorporated 2015 Section 1ldquoQuality standards technical information amp typical analysisrdquono 14 pp 31ndash40 2016 (Accessed 1 November 2015)

[55] A Awad A Adel A A M Nady and AAE ldquoWheat germ anoverview on nutritional value antioxidant potential andantibacterial characteristicsrdquo Food and Nutrition Sciences vol6 no 2 pp 265ndash277 2015

[56] P Pumrojana S Terapuntuwat and P Pakdee ldquoInfluence offatty acid composition of soybean oil vs beef tallow on egg yolkfatty acid profiles of laying hensrdquo Pakistan Journal of Nutritionvol 14 no 7 pp 383ndash387 2015

[57] A F Ceron M O Osorio and B A Hurtado ldquoIdentificacionde acidos grasos contenidos en los aceites extraıdos a partir desemillas de tres diferentes especies de frutasrdquo Acta Agronomicavol 61 no 2 pp 126ndash132 2012

[58] J Orsavova L Misurcova J Vavra Ambrozova R Vicha andJ Mlcek ldquoFatty acids composition of vegetable oils and itscontribution to dietary energy intake and dependence of car-diovascular mortality on dietary intake of fatty acidsrdquo Interna-tional Journal of Molecular Sciences vol 16 no 6 pp 12871ndash12890 2015

[59] M Derbali A Elaissi I Cheraief and M Aouni ldquoFatty acidcomposition and antimicrobial activity against sensitive andmulti-drug resistant bacteria of Tunisian Allium cepa seedextractrdquo Research amp Reviews Journal of Hospital and ClinicalPharmacy vol 2 no 2 pp 30ndash34 2016

[60] M B Suliman A H Nour M M Yusoff P Kuppusamy A RYuvaraj and S A Mazza ldquoFatty acid composition and antibac-terial activity of Swietenia macrophylla king seed oilrdquo AfricanJournal of Plant Science vol 7 no 7 pp 300ndash303 2013

Page 3: Natural Preservatives to Improve Food Quality and Safety

Journal of Food Quality

Natural Preservatives to ImproveFood Quality and Safety

Lead Guest Editor Moreno BondiGuest Editors Simona de NiederhausernChrissanthy Papadopoulou Andrea Laukova and Patrizia Messi

Copyright copy 2017 Hindawi All rights reserved

This is a special issue published in ldquoJournal of Food Qualityrdquo All articles are open access articles distributed under the Creative Com-mons Attribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Editorial Board

Encarna Aguayo SpainRiccarda Antiochia ItalyJorge Barros-Velaacutezquez SpainJoseacute A Beltraacuten SpainAacute A Carbonell-Barrachina SpainMarina Carcea ItalyMaria Rosaria Corbo ItalyEgidio De Benedetto ItalyAlessandra Del Caro ItalyAntimo Di Maro Italy

Rossella Di Monaco ItalyHuumlseyin Erten TurkeySusana Fiszman SpainAndrea Galimberti ItalyEfstathios Giaouris GreeceVicente M Goacutemez-Loacutepez SpainElena Gonzaacutelez-Fandos SpainAlejandro Hernaacutendez SpainJesuacutes Lozano SpainSara Panseri Italy

Mariacutea B Peacuterez-Gago SpainWitoon Prinyawiwatkul USAEduardo Pueacutertolas SpainJuan E Rivera MexicoFlora V Romeo ItalyJordi Rovira SpainAmy Simonne USAGiuseppe Zeppa Italy

Contents

Natural Preservatives to Improve Food Quality and SafetyMoreno Bondi Andrea Laukovaacute Simona de Niederhausern Patrizia Messi and Chrissanthy PapadopoulouVolume 2017 Article ID 1090932 3 pages

Natural Food Additives and Preservatives for Fish-Paste Products A Review of the Past Present andFuture States of ResearchKhawaja Muhammad Imran Bashir Jin-Soo Kim Jeong Hyeon An Jae Hak Sohn and Jae-Suk ChoiVolume 2017 Article ID 9675469 31 pages

Development of a Chemically Defined Medium for Better Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31Wenli Liu Lanwei Zhang and Huaxi YiVolume 2017 Article ID 9017452 8 pages

Lipid Oxidation Color Changes and Microbiological Quality of Frozen Beef Burgers Incorporatedwith ShiraziThyme Cinnamon and Rosemary ExtractsHadi Hashemi Gahruie Seyed Mohammad Hashem HosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan ShadVolume 2017 Article ID 6350156 9 pages

Optimization of Ultrasound Extraction of Cactus Pear (Opuntia ficus indica) Seed Oil Based onAntioxidant Activity and Evaluation of Its Antimicrobial ActivityMariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-Cansino Ernesto Alaniacutes-GarciacuteaLuis Delgado-Olivares Joseacute Alberto Ariza-Ortega Esther Ramiacuterez-Morenoand Joseacute de Jesuacutes Manriacutequez-TorresVolume 2017 Article ID 9315360 9 pages

Antioxidant and Antimicrobial Properties of Cactus Pear (Opuntia) Seed OilsEsther Ramiacuterez-Moreno Raquel Carintildeo-Corteacutes Nelly del Socorro Cruz-Cansino Luis Delgado-OlivaresJoseacute Alberto Ariza-Ortega Vanessa Yelina Montantildeez-Izquierdo Mariacutea Manuela Hernaacutendez-Herreroand Tomaacutes Filardo-KerstuppVolume 2017 Article ID 3075907 8 pages

EditorialNatural Preservatives to Improve Food Quality and Safety

Moreno Bondi1 Andrea Laukovaacute2 Simona de Niederhausern1

Patrizia Messi1 and Chrissanthy Papadopoulou3

1Department of Life Sciences University of Modena and Reggio Emilia Via G Campi 287 Modena Italy2Institute of Animal Physiology Slovak Academy of Sciences Soltesovej 4-6 040 01 Kosice Slovakia3Microbiology Department Faculty of Medicine School of Health Sciences University of Ioannina Ioannina Greece

Correspondence should be addressed to Moreno Bondi morenobondiunimoreit

Received 12 October 2017 Accepted 12 October 2017 Published 12 December 2017

Copyright copy 2017 Moreno Bondi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Food products can be contaminated by a variety of path-ogenic and spoilage microbiota the former causing food-borne diseases and the latter causing significant economiclosses for the food industry due to undesirable effects onthe food properties According to the Centers for DiseaseControl and Prevention (CDC) each year in the UnitedStates 48 million people get sick 128000 are hospitalizedand 3000 die because of foodborne infections Howeveralthough foodborne outbreaks are well recorded sporadiccases are not because not all patients visit the doctor orenter the hospital and the causative agent is not alwaysidentified A considerable number of foodborne pathogens ofgreat public health importance (eg VTEC E coli serotypesCampylobacter jejuni Listeria monocytogenes and Yersiniaenterocolitica) have emerged during the recent two decadescausing severe illness and foodborne outbreaks worldwide

Microbial food spoilage is also an area of immenseconcern for the food industry It is estimated that as much as25 of all food produced is lost after harvest due to microbialactivity While the growth of spoilage microbiota in foodsis not harmful for the human health it has negative impacton the shelf-life textural characteristics and overall qualityof the finished products affects the consumer choices andresults in significant commercial losses Thus prevention orinhibition of microbial growth in foods is of outmost impor-tance for the current globalized food production Hencethere is still the need for new processing methods to be usedeither alone or in combination with the already existing onesable to reduce or eliminate foodborne pathogens and spoilagebacteria

Chemical additives have been extensively used to preventthe survival and proliferation of microorganisms but their

safety and impact on human health are under discussionSince the reduction or elimination of pathogens and spoilagemicroorganisms in food is the foremost priority the currenttrends in food processing are focusing on the use of naturalcompounds which are considered as safe alternatives andsatisfy the consumer preferences for more ldquogreen foodsrdquoHence the increased awareness on the safety of food additivesand preservatives and the consumerrsquos trend to avoid foodscontaining chemicals which in the long-term may haveadverse impact on their health have generated a significantnumber of studies and publications on the potential useof various natural substances recognized as GRAS (Gener-ally Recognized as Safe) to be used as food preservativesChemical compounds added to foods as antioxidant agentsare also of concern particularly when important proteinsources (eg burgers steaks) are involved in the daily diet ofwesternized consumer living in the developed countries [1 2]Synthetic antioxidants such as BHT TBHQ and BHA havedemonstrated various adverse effects on the human healthincluding allergy headache asthma and dermatitis Recentstudies on the utilization of natural antioxidants (eg herbalessential oils and extracts) indicate their capacity and safety[3 4] Also the antimicrobial properties of natural substancessuch as plant essential oils and extracts have been extensivelystudied with promising results [5] The proper recycling anduse of fruit-processing plants by-products like fruit seedsor skins discarded and piling up in huge amounts everyyear are of great interest for the food industry particularlytheir potential to be a useful source of oil and meal [6]Additionally the oil from plant seeds can be used by thefood industry for manufacturing more ldquonaturalrdquo or ldquogreenrdquofoods and also can sufficiently extend the shelf-life of the

HindawiJournal of Food QualityVolume 2017 Article ID 1090932 3 pageshttpsdoiorg10115520171090932

2 Journal of Food Quality

food product [7] The oils derived from fruit seeds oils mayalso have some more useful properties beyond being justldquoediblerdquoThe oil derived from the seed extract of twoMexicanvarieties of cactus pear (Opuntia albicarpa and Opuntia ficusindica) has been found to have sufficient antioxidant andantimicrobial properties [8] Furthermore some biologicalactive compounds produced by microorganisms are widelyused in the food industry as well A good alternative toconventional chemically synthesized food preservatives is theuse of natural antimicrobials such as bacteriocins producedby lactic acid bacteria (LAB) with Nisin being officiallyemployed by the food industry and thus the most widelyused Bacteriocins are peptides actually microbial toxinsproduced from various microorganisms and so far someof them (eg enterocins produced mostly by enterococci)have shown remarkable antimicrobial potential and theirapplication as a natural barrier against pathogens and foodspoilage has been proven to be very efficient when used inthe form of purified or semipurified extracts or as protectivecultures [9 10] Therefore as the developments in foodpreservation are focusing on the implementation of naturalantimicrobials and antioxidants this special issue exploresthe potential of alternatives to currently used preserva-tives through the publication of five high-quality articleswhich aim to address recent advancements in the field ofnatural food preservatives and antioxidants The prospectto replace synthetic preservatives with natural substanceshas been demonstrated by comparing the effects of Shirazithyme cinnamon and rosemary extracts (denoted as naturalantioxidants) with those of the synthetic antioxidant BHT onprotein and lipid oxidations physicochemical microbial andsensory characteristics of frozen beef burgers during storageSpecifically the oxidative stability of the beef burgers contain-ing Shirazi thyme cinnamon and rosemary extracts was welldemonstrated and the antibacterial activitywas documentedas the total microbial counts of the tested burgers were wellbelow the maximum allowed limit Besides the evaluationof the antimicrobial and antioxidant properties of naturalsubstances it is important to optimize their recovery Withregard to bacteriocins to enhance Enterocin Y31 productionand simplify the steps of separation and purification a propersimplified and defined medium (SDM) has been developedfor the Enterococcus faecium Y31 growth and enhancementof the Enterocin Y31 production The bacterial growth didnot result in Enterocin Y31 production in MRS medium andtherefore both the growth rate and the EnterocinY31 produc-tion were set as the goal for the investigation Single omissionexperiments revealed that 5 gL NaCl five vitamins twonucleic acid bases MgSO4sdot7H2O MnSO4sdot4H2O KH2PO4K2HPO4 CH3COONa fourteen amino acids and glucosewere essential for the adequate strain growth and EnterocinY31 production As a result a novel simplified and definedmedium (SDM) was formulated containing 30 ingredientsin which the Enterocin Y31 production yield was higherwhen compared to either MRS or CDM The developmentof the SDM improved the Enterocin Y31 production andsimplified the steps of purification (only two steps) whichis very promising and increases its potential applicationsReferring to seedsrsquo oils the optimization of the extraction

conditions of cactus pear seed oil has been obtained usingultrasound in a closed system based on the antioxidantactivity and using response surface methodology The yieldextraction and antioxidant and antimicrobial activity werecompared with those obtained using both conventional andunconventional methods such as Soxhlet and macerationusing heat agitation or long extraction times microwavesupercritical fluids and ultrasound-assisted extraction inan open and in a closed system The results have shownthat ultrasound exhibited lower oil yield and antioxidantactivity but had the potential to achieve comparable resultsif multiple ultrasound extractions are performed in the timeneeded by conventional methods Seed oils showed similarantimicrobial activity despite the extraction method and canbe an alternative extraction method of seed oils from fruitssuch as cactus pear Lastly the replacement of chemicaladditives with natural compounds has been addressed for fishfoods as well Fish-paste products also known as fish cakes orsurimi-based products are worldwide favorites Surimi a wetprotein concentrate of fish muscle is used as an intermediateraw material to produce surimi seafood The flavor texturetaste shelf-life and market value of surimi-based productsdepend on several factors including the additives used toprepare the surimi While preparing surimi with chemicaladditives several problems have been observed such as alack of unique characteristics inferior acceptability and poorfunctionality In this context a systematic review of fish-paste products prepared using natural food additives (eganimal seafood and plant source additives herbs and orientalmedicines grains and roots and functional food materials)has been performed which summarizes the existing relevantknowledge in the production of new value-added foodstuffsof interest for the surimi industry

In conclusion this special issue offers to the readers thechance to be informed on the recent advancements relatedto the antimicrobial and antioxidant properties of naturalsubstances that are of interest for the contemporary foodindustry Their prospective use in the food production hasthe potential to lead towards the production of safer andhealthier foods not excluding their contribution to a moreefficient preservation of the environment when chemicalswill be replaced with natural substances

Moreno BondiAndrea Laukova

Simona de NiederhausernPatrizia Messi

Chrissanthy Papadopoulou

References

[1] G Comi E Tirloni D AndyantoMManzano and L IacuminldquoUse of bio-protective cultures to improve the shelf-life andthe sensorial characteristics of commercial hamburgersrdquo LWT -Food Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[2] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWT - FoodScience and Technology vol 68 pp 385ndash390 2016

Journal of Food Quality 3

[3] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[4] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[5] H Sakkas P Gousia V Economou V Sakkas S Petsios and CPapadopoulou ldquoIn vitro antimicrobial activity of five essentialoils on multidrug resistant Gram-negative clinical isolatesrdquoJournal of Intercultural Ethnopharmacology vol 5 no 3 pp212ndash218 2016

[6] B Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Fatty Acids in Foods and their Health ImplicationsThirdEdition vol 20073230 of Food Science and Technology pp 263ndash301 CRC Press 3rd Edition edition 2007

[7] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

[8] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research (Formerly Natural Product Letters)vol 27 no 14 pp 1305ndash1314 2013

[9] R Iseppi F Pilati M Marini et al ldquoAnti-listerial activity of apolymeric film coated with hybrid coatings doped with Ente-rocin 416K1 for use as bioactive food packagingrdquo InternationalJournal of Food Microbiology vol 123 no 3 pp 281ndash287 2008

[10] A Laukova and P Turek ldquoEffect of enterocin 4231 in Slovak fer-mented salami puchov after its experimental inoculation withListeria Innocua Lirdquo ACTA Scientiarum Polonorum TechnologiaAlimentaria vol 10 no 4 pp 423ndash431 2011

Review ArticleNatural Food Additives and Preservatives forFish-Paste Products A Review of the Past Present andFuture States of Research

Khawaja Muhammad Imran Bashir1 Jin-Soo Kim2 Jeong Hyeon An1

Jae Hak Sohn13 and Jae-Suk Choi13

1Seafood Research Center IACF Silla University 606 Advanced Seafood Processing Complex Wonyang-roAmnam-dong Seo-gu Busan 49277 Republic of Korea2Department of Seafood and Aquaculture Science Gyeongsang National University 38 Cheondaegukchi-gilTongyeong-si Gyeongsangnam-do 53064 Republic of Korea3Food Biotechnology Division of Bioindustry College of Medical and Life Sciences Silla University 140 Baegyang-daero700 beon-gil Sasang-gu Busan 46958 Republic of Korea

Correspondence should be addressed to Jae-Suk Choi jsc1008sillaackr

Received 9 June 2017 Revised 15 August 2017 Accepted 17 September 2017 Published 27 November 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Khawaja Muhammad Imran Bashir et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Fish-paste products also known as fish cakes or surimi-based products are worldwide favorites Surimi a wet protein concentrateof fish muscle is used as an intermediate raw material to produce surimi seafood The flavor texture taste shelf-life and marketvalue of surimi-based products depend on the source of the fish meat type of applied heat treatment and additives used toprepare the surimi While preparing surimi with chemical additives several problems have been observed such as a lack of uniquecharacteristics inferior acceptability and poor functionality Various types of fish-paste products have been developed by usingdifferent ingredients (eg vegetables seafood herbs and oriental medicines grains and roots including carrots and functionalfood materials) However a systematic review of fish-paste products prepared using natural food additives has not yet beenperformedTherefore the quality characteristics of fish-paste products and their functionalities were elucidated in this study Withthe increasing demand for surimi seafood products the functional properties physiochemical properties and shelf-life of surimi-based products need to be improved This review will aid the preparation of new value-added products in the surimi industry

1 Introduction

Fish-paste products popularly known as fish cakes areproduced from frozen surimi (ie they are a kind of surimi-based product) and are popular in Korea and Japan [1] Inthe Korean Food Standards Codex fish cakes are known asa processed marine product comprising salt-soluble proteinsisolated from fish meat [2] Fish muscle is mechanicallydeboned washed with water and blended with cryoprotec-tants to prepare a wet concentrate of proteins called surimiSurimi is a Japanese term that is also known as washed fishmince It is a refined fish myofibrillar protein manufacturedthrough numerous step-by-step processes including headinggutting filleting deboning (mincing) washing dewatering

refining mixing with cryoprotectants freezing and metaldetection for HACCP [3] The myofibrillar proteins make itan excellent ingredient for developing food products It hasexcellent gelling properties and forms strong and elastic gelsupon heating [4]

The setting and deformation are important to preparesurimi and surimi-based products Setting also known asldquosuwarirdquo in Japanese is a very important process which hasa significant influence on the physiological and rheologicalproperties of surimi-based products Setting is a vital processin the quality estimation of surimi because it helps to improvethe water-holding capacity as well as the gel texture of surimi-based productsWhen fishmince paste (sol) is heated at a lowtemperature (up to 50∘C) a loose network (suwari) is formed

HindawiJournal of Food QualityVolume 2017 Article ID 9675469 31 pageshttpsdoiorg10115520179675469

2 Journal of Food Quality

from myosin and actomyosin molecules this process isreferred to as setting Setting is species dependent and occursover a range of temperatures (up to 50∘C) and to a varyingextent As the temperature is increased to around 70∘Csuwari is partially disrupted to form a broken net structure(modori) a phenomenon attributed to the dissociation ofmyosin from actin and the possible fragmentation of the actinfilament [5ndash7]

Most of the surimi-based products are different types offish-paste products while less than 10 include fish burgersfish ham and fish sausages [3] Surimi-based products areprepared by mixing the raw or frozen surimi with saltsand other ingredients molded and heated to form the finalproduct in the specified shape and texture and pasteurizedbefore packaging The kind of heat treatment depends on theflavor texture and appearance of the desired final productand may include broiling steaming deep-fat frying andboiling [8] while fish-paste products in South Korea aremostly prepared by frying [9] Textural characteristics suchas gel strength are the major determinant of surimi priceand quality [10] Several studies have attempted to enhancethe textural quality of surimi or surimi-based products usingvarious protein additives [11ndash14]

Surimi quality and gelling property are mainly affectedby both intrinsic factors (effect of fish species seasonalitysexual maturity and freshness or rigor) and extrinsic fac-tors (harvesting handling water characteristics processingtime and temperature solubilization of myofibrillar proteinsduring processing the activity of the endogenous or addedprotein oxidants and proteolytic enzymes washing cyclessalinity and pH) [3 134] Surimi forms thermoirreversiblegels upon heating which do not deform with further changein the temperature This phenomenon of surimi and surimi-based products is similar to that observed in other proteinssuch as egg white milk-lactoglobulin and wheat glutenAdditionally surimi produces gels of very high deformabilityand strength This heat-induced gelation property of surimimakes it a very valuable food ingredient [134]

The gel-forming ability and capacity of surimi areadversely affected by the proteolytic degradation of myofib-rillar proteinsThe presence of indigenous proteinases causedgel softening in surimi made from fish species for examplethreadfin bream [135] arrow tooth flounder [136] Pacificwhiting [137] and lizard fish and bigeye snapper [20 59]Various active proteinases in fish muscle are responsible forsoftening of the surimi gels Nakamura and Ogawa and Anet al testified that cathepsins L and B were the most activecysteine proteinases in Pacific whiting surimi and fish filletsrespectively [7 138] The myofibril-associated proteinasesobserved in lizardfish surimi were serine proteinases andcysteine while a serine proteinase was reported in the bigeyesnapper surimi [20 59]

Seasonal analysis of the compositional properties ofAlaska pollock and Pacific whiting showed higher proteincontents in winter while the moisture contents were higherin summer [139 140] Surimi prepared from cold-water fishspecies with low thermostability of myofibrillar proteinsmakes setting easier Normally a myofibrillar protein withlow thermostability is optimum to do setting because its

reactivity is increased due to the loose internal structure bysodium chloride addition and heat denaturation In contrastthe myofibrillar protein of tropical fish species with high heatstability is difficult to denature and form the myofibrillarprotein network structure in surimi [3]

Several research groups have studied ways to enhance thequality of surimi-based products by investigating the changesin microbial content enzyme activity nutrient content andacceptability characteristics the use of raw materials thestandardization of the manufacturing process storage andmarketing Natural and chemical food-grade additives suchas konjac flour proteinase inhibitors egg white and hydro-colloids have been used to enhance the gelling properties ofsurimi [12 17 20 23 34 141ndash143] The trypsin inhibitor inegg white plays a major role in improving the gel strengthof surimi The addition of egg white inhibits the proteolyticactivity of the modori-inducing enzyme in fish meat andsuppresses the decrease of elasticity in surimi Serum pro-teins have strong inhibiting abilities against the action ofvarious proteases with different active centers such as SHgroups and serine groups In addition they also containtransglutaminases that accelerate the setting Egg white andserum proteins also play an important role in inhibiting theenzymatic activity of the parasites Apart from the use ofadditives gel strengthening can be achieved by treating thegels at low temperatures (0ndash40∘C) before cooking [144 145]Furthermore the gel quality of surimi and surimi-basedproducts can also be enhanced by using alternate fish speciesor by acid and alkali washing to increase the myofibrillarprotein concentrations [7 146 147]

Surimi production worldwide reached around800000MT by 2011-2012 [3] while South Korea alonecontributed approx 156000MT in 2013 Over the yearsthe size of the market for Korean fish-paste products hasgradually increased reaching sim350 million US dollars in2013 (based on the amount produced) [148] Howevermanufacturers have had several problems in producingsurimi-based products such as a lack of unique character-istics and inferior acceptability and functionality Thereforethere have been several attempts to develop new fish-pasteproducts with excellent acceptability and functionalityTo this end numerous types of fish-paste products havebeen developed using various natural ingredients such asvegetables seafood animals plants herbs and orientalmedicines seaweed and functional food materials It is ofworldwide interest to use these natural food preservativesinstead of chemical or synthetic ones However to date nosystematic review of fish-paste products supplemented withvarious food raw materials has been performed Thereforethe quality characteristics of fish-paste products and theirfunctionalities were elucidated in this study

2 Improvement of the Gel Properties ofFish-Paste Products

Various food additives derived from animals (eg beefswine and chicken) seafood (eg fish invertebrates) plants(eg legumes cereals) sugars polyols and functional mate-rials used in fish-paste products to improve their gelling

Journal of Food Quality 3

capabilities and strength are listed in Table 1 and describedbelow

21 Animal Source Additives Various food-grade proteaseinhibitors from animal sources are used to enhance thephysical properties of surimi-based products as well to pre-vent the protein degradation The ability of beef plasma andother food-grade additives in surimi and fishmince preparedfrom Pacific whiting (Merluccius productus) was studied byMorrissey et al [12] The strongest proteolytic inhibitionwas observed with beef plasma protein at a concentrationas low as 1 Reppond and Babbitt reported the increase ingel strength of gels prepared by arrow tooth flounder at aconcentration of 2 with a yellow hue color [16] Weeras-inghe et al characterized the inhibitory activity of these food-grade inhibitors and reported that the inhibitory activity wasmainly because of specific serine proteinase inhibitors [17]The addition of 2 dried bovine plasma to steamed fish-pasteslightly increased the chewiness and hardness but it showeda negative effect on the gel strength [18] Duangmal andTaluengphol reported that the higher levels of beef plasmaprotein unfavorably affected gel characteristics of red tilapiasurimi gels [19]

The effect of porcine plasmaprotein on the bigeye snapper(Priacanthus tayenus) surimi gel characteristics was investi-gated by Benjakul et al [14]The gels supplemented with 05porcine plasma protein had the highest level of deformationand breaking force Benjakul and colleagues later reportedthe effect of porcine plasma protein on the gel characteristicsof surimi from bigeye croaker (Pennahia macrophthalmus)bigeye snapper (P tayenus) barracuda (Sphyraena jello)and threadfin bream (Nemipterus bleekeri) [20] The porcineplasma protein was effective in increasing the deformationand breaking force of kamaboko gels Higher breaking forcesand levels of deformation occurred when chicken plasmaprotein was supplemented to sardine kamaboko gels at levelsup to 2 [21] The inhibitory activities of cysteine proteinaseinhibitor fraction from chicken plasma on Pacific whitingand arrow tooth flounder mince were reported by Rawdkuenet al [22] Furthermore similar results were observed intheir extended study onPacificwhiting surimi where chickenplasma at a level of 2 inhibited the degradation of myosinheavy chain proteins [23]

Ovomucoid is a mucoprotein obtained from egg whitethat has been tested for its potential as a gel-degradationinhibitor [24 25] The addition of 2 ovomucoid couldincrease the breaking strength and gel deformation [28]The autolytic activities of lizardfish (Saurida tumbil) surimiand mince under the application of protease inhibitors wereinvestigated by Yongsawatdigul and Piyadhammaviboon[26] At all preincubation conditions egg white enhancedthe gel-forming capability of S tumbil surimi to a greaterextent than did whey protein concentrateThe addition of 1egg white and preincubation at 25∘C increased the breakingforce by twofold Campo-Deano and Tovar [27] reportedthat the addition of egg albumen at 15 and 2 for Alaskapollock and Pacific whiting surimi respectively enhancedthe gel strength of crab sticks According to Hunt et al theincorporation of 2-3 special dried egg white improved

the gel textural characteristics of Alaska pollock and Pacificwhiting surimi [28]

Whey is the complete set of proteins isolated fromthe watery portion of milk Whey protein is comprisedof 20 milk protein and 80 casein [149] Whey proteinconcentrates have generally been used as an emulsifierfiller water binder protein supplement foam stabilizer andthickener as well as gelling agent [150] Rawdkuen andBenjakul investigated the effect of whey protein concentrateon the gelling characteristics of surimi prepared fromgoatfish(Mulloidichthys vanicolensis) bigeye snapper (P tayenus)lizardfish (S tumbil) and threadfin bream (N bleekeri) [29]All the tested surimi supplemented with 3 whey proteinconcentrate displayed inhibitory activity against autolysis andsignificantly reduced gel whiteness However better water-holding capacity was obtained by increasing concentrationsof whey protein concentrate

Plasma proteins produced from pig cow and chickenbyproducts are relatively affordable and easily collectiblesources [143 151 152] However outbreaks of foot-and-mouthdisease avian influenza andmad cow disease as well as a banonproteins frompig bone and skin in some states for religiouscauses have made it essential to search alternative sources[153 154] Various fish plasma proteins have been testedincluding those from rainbow trout and salmon [31 35 36]

22 Seafood Additives The effects of shrimp head proteinhydrolysate fromdifferent shrimp namely black tiger shrimp(Penaeus monodon) northern pink shrimp (Pandalus eous)and endeavour shrimp (Metapenaeus endeavouri) on thegelling properties of lizardfish (Saurida spp) surimi wereinvestigated by Ruttanapornvareesakul et al [30] It wasreported that the freeze-induced denaturation of lizardfishmuscle protein could be reduced by the supplementation ofshrimp head protein hydrolysate at a concentration of 5resulting in higher Ca-ATPase activity and gel strength Theeffects of rainbow trout plasma proteins on the gelling prop-erties of surimi prepared by Alaska pollock were investigatedby Li et al [31] Gel degradation deformation the breakingforce water-holding capacity and whiteness enhanced withincreasing amounts of rainbow trout plasma protein anddecreased at higher concentrationsThe rainbow trout plasmaprotein at a concentration of 075mgg could be used asa potential protease inhibitor to inhibit gel weakening inAlaska pollock surimi Li et al reported the higher inhibitoryactivities of the recombinant chum salmon cystatin againstautolysis of Alaska pollock surimi [155]

Fish gelatin is extracted from the collagen of fish skinand it is used as a food additive Hernandez-Briones et alstudied the functional and mechanical properties of Alaskapollock surimi gels while using fish gelatin as an additive[32] The increasing concentration of gelatin affected thewhiteness but the sensory panelists were unable to detect itThese results showed that fish gelatin was not effective as afunctional additive in Alaska pollock surimi Nevertheless itcould be added at up to 10 gkg without negatively affectingthe mechanical properties of surimi Yin et al reported asignificant improvement in the endogenous transglutaminaseactivity of Alaska pollock surimi prepared with nanoscaled

4 Journal of Food Quality

Table1Naturalfood

additiv

esused

toim

provethe

gelpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Animalsource

additiv

es

Beefplasma

hydrolysate

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Atlanticmenhaden

(Brevoortia

tyrann

us)

Alaskap

ollock

(Theragra

chalcogram

ma)

Moistu

recontentproteincontent

cook

inglossw

ater-holding

capacitytexturetorsio

ntest

05

ndash15

[15]

Bovine

plasma

Bostaurus

Heatedin

awater

bath

Powder

Arrow

toothflo

under

(Atheresthessto

mias)

Walleye

pollo

ck

Moistu

recontentpu

nchtorsion

colortest

2[16]

Beefplasma

protein

Bostaurus

mdashPo

wder

Pacific

whitin

g(M

erlucciusp

rodu

ctus)

Proteincontentinhibitory

assay

4[17]

Drie

dbo

vine

plasma

Bostaurus

Steaming

Powder

Alaskap

ollock

(Tchalco

gram

ma)

Nutrie

ntcontentpH

water-holding

capacitytexture

and

sensoryevaluatio

n2

[18]

Beefplasma

protein

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Redtilapia

(Oniloticus

xO

placidus)

Colortextureexpressiblewater

protein

totalsulfhydrylcon

tent

2gkg

[19]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Bigeye

snapper

(Pria

canthu

stayenus)

Expressib

ledrip

amou

ntcolor

texturesetting

cond

ition

s05

[14]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Threadfin

bream

(Nem

ipterus

bleekeri)Bigeyes

napp

er(Ptayenus)

Baracuda

(Sphyraena

jello)and

Bigeye

croaker

(Penna

hiamacrophthalmus)

Trichloroacetic

acid-solub

lepeptidescolortextureprotein

content

05

[20]

Chickenplasma

protein

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Sardine

(Sardinella

gibbosa)

Colortextureexpressiblemoistu

re

proteincontentautolysis

activ

ity2

[21]

Cyste

inep

roteinase

inhibitorfrom

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Arrow

toothflo

under

(Astomias)Pacific

whitin

g(M

produ

ctus)

Autolysis

andinhibitory

activ

ity

pHprotein

content

3[22]

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Pacific

whitin

g(M

produ

ctus)

Torsionandfracture

test

dynamic

rheologicalattribute

2[23]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[24]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[25]

Eggwhite(EW)

Gallusgallusd

omesticus

Heatedin

awater

bath

Powder

Lizardfish(Saurid

atumbil)

mince

andsurim

iAu

tolytic

activ

itytexturalattributes

EW1

[26]

Eggalbu

min

Gallusgallusd

omesticus

Heatedin

thec

ooking

roller

Eggwhite

itself

Surim

i-based

crab

sticksfrom

Alaskap

ollock

(AP)

Pacific

whitin

g(PW)

(Mprodu

ctus)

Transie

nttest

streng

thtest

texture

dynamicrheologicaland

physical

attributes

AP

15

PW2

[27]

Journal of Food Quality 5

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Regu

lard

riedegg

white(REW

)speciald

riedegg

white(SEW

)liq

uideggwhite

(LEW

)

Gallusgallusd

omesticus

Heatedin

awater

bath

Spray-dried

powder

Pacific

whitin

g(M

produ

ctus)

Totalsulfhydrylgroup

sfracture

test

dynamicrheologicalattribute

SEW2-3

[28]

Wheyprotein

concentrate

Bostaurus

Heatedin

awater

bath

Wheyprotein

concentrate

Bigeye

snapper(Ptayenu

s)Goatfish

(Mulloidich

thys

vanicolen

sis)

Threadfin

bream

(Nblee

keri)

and

Lizardfish(Stum

bil)

Water-holding

capacitycolor

autolytic

activ

ity3

[29]

Seafoo

dadditiv

esSh

rimphead

proteinhydrolysate

from

northern

pink

shrim

pendeavou

rshrim

pand

blacktig

ershrim

p

Pand

alus

eous

Metapenaeus

endeavouri

Pena

eusm

onodon

Heatedin

awater

bath

Drie

dmatter

Lizardfish

(Saurid

aspp)

Gelstr

engthcolorgel-forming

abilityC

a-AT

Pase

activ

ity5

[30]

Rainbo

wtro

utplasmap

rotein

Oncorhynchu

smykiss

Heatedin

awater

bath

Freeze-drie

dplasma

Alaskap

ollock

Proxim

atea

nalysisw

ater-holding

capacitycolortextureprotein

content

075

mgg

[31]

Fish

gelatin

Com

mercialfishgelatin

(Gelatin

Rousselot)

Heatedin

awater

bath

Powder

Alaskap

ollock

Colorm

echanicalfunctio

nal

sensoryattributes

10gkg

[32]

Nanoscaled

fish-bo

neof

Pacific

whitin

gMprodu

ctus

Heatedin

awater

bath

Powder

Alaskap

ollock

Texturescanning

electron

microscop

y1g10

0g[33]

Nanoscaled

fish-bo

ne(N

FB)+

driedeggwhite

(DEW

)

Mprodu

ctusGallus

gallu

sdom

esticus

Heatedin

awater

bath

Powder

Pacific

whitin

g(M

produ

ctus)

Rheologicaland

texturalattributes

DEW

1+

10mgNFB

Cag

surim

ipaste

[34]

Salm

onbloo

dplasma

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)

Scanning

electronmicroscop

yproteincontentdynamic

rheologicalattributes

1g10

0g[35]

6 Journal of Food QualityTa

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Freeze-drie

dchinoo

ksalm

onplasma(

FSP)

and

concentrate

salm

onplasma

(CSP

)

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)surim

iand

Salm

onmince

Proteolytic

inhibitio

nautolysis

proteincontent

Salm

onminceC

SPgt

FSP

Pacific

whitin

gsurim

iFSP

[36]

Partially

purifi

edtrypsin

inhibitor

from

ther

oeof

yello

wfin

tuna

fish

Thun

nusa

lbacares

Heatedin

awater

bath

Freeze-drie

dBigeye

snapper

(Pria

canthu

smacracanthu

s)Proteolysis

colorw

ater-holding

capacitygellin

gprop

ertie

s3g

100g

[37]

Squidink

tyrosin

ase(SIT)

+tann

icacid

(TA)

Todarodesp

acificus

Heatedin

awater

bath

Mixture

Sardine

(Sardinella

albella)

Tyrosin

asea

ctivityinvitro

oxidationassaycolortexturaland

sensoryattributes

SIT

500U

gprotein+

TA1

[38]

Plantsou

rcea

dditives

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soybean

protein

Wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[39]

Soyprotein

eggwhite(EW)

wheyprotein

concentrate

(WPC

)La

ctalbumin

(LA)

milk

proteiniso

late

(MPI)

Glycinem

ax

Gallusgallusd

omesticus

Bostaurus

Coo

kedin

aste

amcooker

Powder

AlaskaP

ollock

(Tchalco

gram

ma)

Textureexpressib

lemoistu

recontentwater

retentionprop

ertie

sEW

andMPI

[4041]

Legu

mes

eed

extractfrom

blackcowpea

whitecowpea

soybeanseeds

Mun

gbean

peanut

Vignaun

guicu

lata

Glycinem

axVignaradiata

Arachish

ypogaea

mdash

Freeze-drie

dproteinase

inhibitor

extracts

Threadfin

bream

(Nem

ipterid

ae)

ThermalstabilitypHprotein

contentproteinase

inhibitory

assay

Blackcowpea

soybeanseeds

30mgg

[42]

Legu

mes

eed

extractfrom

Cow

pea

pigeon

pea

bambara

grou

ndnu

ts

Vignaun

guicu

lata

Cajanu

scajan

Vo

andzeia

subterranea

mdashPartially

purifi

edTrypsin

Threadfin

bream

(Nem

ipterid

ae)

Sarcop

lasm

icmod

ori-ind

ucing

proteinase

activ

itycolor

30ku

nits

g[43]

bambara

grou

ndnu

tprotein

isolate

Vignasubterranea

Heatedin

awater

bath

Powder

Threadfin

bream

(Nblee

keri)

Colorautolysis

025

g100g

[44]

Soyproteiniso

late

Glycinem

axHeatedin

awater

bath

Com

mercial

soyprotein

isolate

(JinQ

ui1200)

Alaskap

ollock

(Tchalco

gram

ma)

Com

mon

carp

(Cyprin

uscarpio)

Totaln

itrogen

andmoistu

recontentgelstre

ngthcolor

10

[45]

Journal of Food Quality 7Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soyprotein

wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[46]

Dietary

fiber

(DF)

from

peaa

ndchicory+

microbial

transglutaminase

(MTG

ase)

Cichorium

intybu

sPisum

sativ

umHeatedin

awater

bath

Powder

Hake(Mcapensis)

Gilthead

seabream

(Sparusa

urata)

Seab

ass(Dice

ntrarchu

slabrax)

Meagre(Argyrosomus

regius)

Dyn

amicrheologicalattributes

MTG

ase100U

g[47]

Proteiniso

lates

from

Mun

gbean

(MBP

I)black

bean

(BBP

I)bam

bara

grou

ndnu

t(BG

PI)

Phaseolusa

ureus

Phaseolusv

ulgarisV

igna

subterranea

mdashFreeze-drie

dpo

wder

mdash

Scanning

electronmicroscop

yproteolytic

autolyticandtrypsin

inhibitory

activ

ityassaycolor

texturetrichloroacetic

acid-solub

lepeptidec

ontent

1g10

0g[48]

Partially

purifi

edtrypsin

inhibitor

from

adzukibean

Vignaangularis

Heatedin

awater

bath

Freeze-drie

dpo

wder

Threadfin

bream

(Nblee

keri)

Proteincontenttexturecolor

trypsin

inhibitory

activ

ityautolytic

activ

ityassay

3g10

0g[49]

Amylose(A)a

ndam

ylop

ectin

(AP)

mdashHeatedin

awater

bath

Powder

Walleye

pollo

ck(T

chalcogram

ma)

Gelationandbreaking

strength

Amylose70+

Amylop

ectin

4

[50]

Wheatsta

rch

Triticum

aestivum

Heatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Com

pressio

ntest

dynamic

viscoelasticityscann

ingele

ctron

microscop

y

Starch10g

+Surim

i10g

[51]

Natives

weetp

otato

starch(N

SPS)

and

Mod

ified

sweet

potato

starch

(MSP

S)

Ipom

oeabatatas

Heatedon

acontrolled

stress

rheometer

Powder

Alaskap

ollock

(T

chalcogram

ma)

Dyn

amicrheologicalattributes

5[52]

Potato

starch

Solanu

mtuberosum

Heatedin

the

Krehalon

ecasin

gfilm

Powder

Pacific

sand

lance(Am

modytes

personatus

Gira

rd)

Proxim

atea

nalysis

protein

compo

sition

colorfoldingtext

texturalandsensoryattributes

8[53]

Rice

flour

Oryza

sativa

Fried

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorrheologicaland

sensoryattributes

10ndash15

[54]

Rice

flour

Oryza

sativa

Fried

Powder

Threadfin

bream

(Nem

ipterid

ae)

Moistu

recontentpH

color

texturalandsensoryattributes

50

[55]

Rice

flour

Oryza

sativa

Fried

Powder

Goldenthreadfin

bream

(Nem

ipterusv

irgatus)

Gelstr

engthsensoryattributes

14

[56]

Cryoprotectantsa

ndhu

mectants

Xanthan(X)

locustbean

(LB)

gumsa

loneX

LB

ratio

Ceratoniasiliqua

Heatedin

awater

bath

Powder

Silver

carp

(Hypophthalm

ichthys

molitrix)

Torsiontest

gel-formingability

mechanicalattributes

XLB

025075

[57]

Pectin

gum

(HM

LM)+

CaCl2

mdashHeatedin

awater

bath

Gum

and

powder

Silver

carp

(Hm

olitrix)

Water-holding

capacitym

echanical

andtexturalattributes

Pectin

gum1+

CaCl202

[58]

8 Journal of Food Quality

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Chito

san7B

from

praw

nshell

Not

mentio

ned

Heatedin

awater

bath

Not

mentio

ned

Barred

garfish

(Hem

iramphus

far)

ProteincontentSE

Mtextural

attributes

1[59]

Konjac

glucom

annan

aqueou

sdisp

ersio

nAm

orphophallu

skonjac

Heatedin

awater

bath

Aqueou

sdispersio

n

Giant

squid(D

osidicu

sgigas)

Alaskap

ollock

(T

chalcogram

ma)

ProteinsolubilitypH

texturaland

viscoelasticrheologicalattributes

1[60]

Carrageenan+

NaC

lorK

Clmdash

Heatedin

awater

bath

Hydrocollo

idAlaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorcompressio

ntest

Carrageenan1+

KCl15

[61]

Amorphophallu

skonjac

flour

(AKF

)Am

orphophallu

skonjac

Heatedin

awater

bath

Flou

rGiant

squid(D

gigas)

Water

retentionabilitycolor

texturalandsensoryattributes

10

[62]

NaC

l+high

hydrostatic

pressure

(HHP)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Proxim

atea

nalysis

FTIR

SEM

colormechanicalrheologicaland

sensoryattributes

HHP

300MPa

+NaC

l03

[63]

Sodium

chlorid

esugarspolyols

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Larim

ichthys

polya

ctis)

Water

activ

ityV

BNcolor

moistu

recontent

Sodium

chlorid

e4

Glucose10

Glycerin

10

[64]

Starchglycine

sodium

lactate

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Lpolya

ctis)

Water

activ

ityV

BNcolorm

oistu

recontent

Sodium

lactate75

[65]

Glycerol

mdashSteamed

Liqu

idMackerel(Scom

berjaponicu

s)andBrazilian

sand

perch

(Pseud

opercis

semifa

sciata)

Water

activ

itytexturaland

sensory

attributes

20

[66]

Naa

ndCa

salts

ofpo

lyuron

ides

and

carboxym

ethyl

cellu

lose

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gel-

streng

theningeffects

2ndash6

[67]

L-ascorbicacid

(AsA

)and

dehydro-L-

ascorbicacid

(DAs

A)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthanalysis

DAsA

10120583

gg

[68]

Sodium

-L-

ascorbate

(SA)

mdash

Steamed

inNojax

cellu

lose

casin

g

Powder

Alaskap

ollock

(T

chalcogram

ma)

pHtexturaland

sensoryattributes

02

[69]

120596-3

fatty

acids

from

algae

Not

mentio

ned

Heatedin

awater

bath

Oil

Cod

(Gadus

morhu

a)TB

ARS

fattyacid

contentcolor

500m

g85

g[70]

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)

Microscop

icob

servation

viscosity

gel-formingability

10

[71]

Journal of Food Quality 9Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)Th

readfin

bream

(Nem

ipterid

ae)White

croaker(Ge

nyonem

uslin

eatus)

andJapanese

jack

mackerel(Trachu

rus

japonicus)

Proxim

atea

nalysis

color

water-holding

capacityphysic

alattributes

5ndash30

[72]

120596-3

PUFA

s-ric

hoils

Flaxseedalgae

menhaden

krillblend

(flaxseed

algae

krill

811)

Heatedin

awater

bath

Oil

Alaskap

ollock

(T

chalcogram

ma)

Torsiontest

andrheological

attributes

9g10

0g[73]

Ethano

licKiam

woo

dextract

(EKW

E)+

commercialtann

in(C

T)

Hopea

sp

Heatedin

awater

bath

Overdrie

dpo

wder

Strip

edcatfish

(Pangasiu

shypophthalmus)

pHV

BNT

BARS

color

TCA-

solublep

eptid

emoistu

re

proteincontents

texturalattributes

EKWE

008

CT002

ndash004

[74]

Cocon

uthu

skextractw

ithethano

l60(C

HE-E6

0)

80(C

HE-E8

0)

Cocosn

ucifera

Heatedin

awater

bath

Freeze-drie

dpo

wder

Sardine

(Salbella)

Totalpheno

licexpressible

moistu

reT

CA-solub

lepeptideand

proteincontents

colortextual

rheologicalandsensoryattributes

CHE-E6

00125

[75]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Solutio

nMackerel

(Rastre

lligerk

anagurta)

SEMexpressiblemoistu

reprotein

contentcolortexturalandsensory

attributes

OFA

040

OTA

050

OCF

050

OCT

010

[76]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Bigeye

snapper

(Ptayenus)

SEMexpressiblemoistu

reprotein

andfre

eaminoacid

contentcolor

texturalandsensoryattributes

OFA

020

OTA

005

OCF

015

OCT

005

[77]

Eggwhitepo

wder

(EW)whey

protein

concentrate(WPC

)

Gallusgallusd

omesticus

Triticum

aestivum

Heatedin

awater

bath

Powdera

ndconcentrate

Lizardfish

(Stum

bil)mince

andsurim

i

Autolytic

activ

ityT

CA-solub

leoligop

eptid

esprotein

content

texturalattributes

EW4

WPC

4

[26]

Zinc

sulfate

(ZnS

O4)sodium

tripolypho

sphate

(STP

P)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Yello

wstr

ipetrevally

(Sela

roideslep

tolep

is)

Expressib

lemoistu

relipid

phosph

olipidand

proteincontent

Ca-ATP

asea

ctivitycolortextural

attributes

ZnSO460120583

molkg+

STPP

05

[78]

SEMscann

ingelectro

nmicroscop

yFT

IRFou

rier-transfo

rminfrared

spectro

scop

yVBN

volatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stancesT

CAtric

hloroacetic

acid

10 Journal of Food Quality

fish bones [33] Furthermore a study on the rheologicaland textural attributes of Pacific whiting surimi showedthat slow heating and the addition of nanoscaled fish bonessignificantly enhanced gel strength [34]

Fowler and Park reported an enhanced gelling strengthand effectively inhibited proteinase activity in Pacific whitingsurimi gels heated ohmically [35] Fowler and Park laterstudied the effects of salmon plasma from Chinook salmonon proteolytic inhibition of surimi [36] Salmon plasmaeffectively inhibited both serine and cysteine proteases as wellas proteases isolated from Pacific whiting Salmon plasmaconcentrated by ultrafiltration performed slightly better thanfreeze-dried salmon plasma at inhibiting autolysis in salmonmince

Klomklao et al reported inhibitory activity of a par-tially purified trypsin inhibitor (TIYTR) from yellowfintuna (Thunnus albacores) on the gelling characteristics ofbigeye snapper (Priacanthus macracanthus) surimi [37] Theincorporation of TIYTR with a level of 30 g100 g resultedin the enhanced deformation and breaking force of surimigels suggesting that the TIYTR could be employed as anaffordable and alternative proteinase inhibitor to enhance thegel strength of surimi prepared by bigeye snapper

Vate and Benjakul investigated the effects of squid inktyrosinase mixtures of tannic acid and protein on the gellingcharacteristics of sardine surimi [38] The highest deforma-tion and breaking force were obtained when surimi gels wereallowed to react for 90min while being supplemented with1 tannic acid and 500Ug squid ink tyrosinase proteinHowever gels with an added squid ink tyrosinasetannicacid mixture were whiter than the control The surimi gelssupplemented with squid ink tyrosinasetannic acid mixtureshowed the maximum overall acceptance scores suggestingthat it could be used as an additive to increase the surimi gelproperties

23 Plant Source Additives The chicken plasma proteinegg white and beef plasma protein are considered as themost effective protease inhibitors for surimi [17 22 23156] However the use of chicken plasma and beef plasmaprotein has been forbidden because of the occurrence of avianinfluenza and mad cow disease respectively In additionhigher concentrations of beef plasma proteins have also beenassociated with off-flavors while egg white is expensive andhas an unwanted egg-like odor [29 156] Additionally veg-etarians would not want to consume surimi-based productsprepared with additives from animal or even seafood sourcesTherefore alternate food-grade additives are still desired toenhance the gel strength of surimi without affecting thecustomer demandVarious natural additives derived from theplant sources have been briefly described below

231 Legumes Theeffects of vegetable protein contentmois-ture heating and setting conditions on the physical attributesof kamaboko were examined by Yamashita [39] A firm gelwas obtained at 60∘C for kamaboko with soybean proteinand at 80∘C with wheat gluten When the kamaboko gelswere supplemented with 5 vegetable protein the changes injelly strength softness and expressiblewater of the kamaboko

with wheat gluten were somewhat greater than those of thekamaboko with soybean protein According to the results ofChung and Lee the addition of plant proteins including soyprotein isolate lactoalbumin and wheat gluten remarkablylessened the strength of non-animal protein-incorporatedsurimi gels [40] The textural and sensory attributes offiberized surimi gel products were categorized as an increasein overall textural desirability and an increase in gel strengthIn another study egg white and milk protein isolate showedhigher water retention ability than whey protein concentratesoy protein isolate and lactoalbumin [41]

Protein isolates from legume seeds can be used as alter-nate protein additives for the quality improvement of surimigels Legume seed isolates comprise trypsin inhibitors andhave been used as the protease inhibitor in the prepara-tion of surimi and surimi-based products [42 43] Ben-jakul et al reported higher protease inhibitory activities ofinhibitor extracts from soybean and black cowpea seeds[42] A reduced gel-degradation activity (modori) and ahigh thermal stability were reported In another study theyreported inhibitory effects of proteinase inhibitor extractsfrom Bambara groundnuts (Voandzeia subterranea) pigeonpea (Cajanus cajan) and cowpea (Vigna unguiculata) onautolysis and gel-degradation activity (modori) of threadfinbream surimi [43] The whiteness of surimi gels reducedslightly with the addition of proteinase inhibitor Similarresults were obtained by Oujifard and colleagues [44] TheBambara groundnut protein extracts at a level of 025 g100 gshowed improved autolytic inhibition deformation andbreaking force in surimi prepared by threadfin bream (Nbleekeri) [44] However a slight reduction in whiteness wasobserved at increasing levels of Bambara groundnut proteinisolates These studies show that the addition of Bambaragroundnut protein extracts at a suitable level could serve asan alternative food inhibitor to enhance the gelling propertiesof surimi

Plant protein isolates mainly soy protein isolates havebeen used in the surimi industry because of their safety andrational price [45] Luo et al indicated the legumin andvicilin two main legume seed storage proteins as bindersand cogelling agents in surimi gels [45] Protease inhibitorsisolated from legume seeds not only can help to reduce thegel-degradation process in surimi but can also improve thesurimi gel properties by acting as filler or binder Luo etal reported higher breaking force and quality characteristicsof silver carp surimi when supplemented at a ratio of 10soy protein isolate [46] Cardoso et al studied the effects ofdietary fiber and microbial transglutaminase from chicoryand pea on the rheological properties of protein paste fromgilthead sea bream hake meagre and seabass [47] It wasfound that a high degree of protein denaturation boosted gelhardness while a low degree of protein denaturation createdgels with high deformability It shows that the addition ofmicrobial transglutaminase could serve as a possible additivefor gels of those species having lesser protein unfoldingability

Kudre et al studied the effects of black bean (Phaseolusvulgaris) and mung bean (Phaseolus aureus) protein isolateson gelling properties and proteolysis of sardines (Sardinella

Journal of Food Quality 11

albella) surimi [48] An increase in deformation breakingforce and water-holding capacity as well as a lower levelof degradation was observed while the whiteness of kam-aboko gels reduced slightly Therefore mung bean or blackbean protein isolates could be effectively used to retardthe proteolysis in sardine surimi leading to improved gelstrength Klomklao and Benjakul studied the effects of thepartially purified trypsin inhibitor from adzuki bean on thegelling properties and proteolysis of threadfin bream (Nbleekeri) surimi [49] An increase in autolysis and inhibitoryactivity against sarcoplasmic proteinases aswell as an increasein deformation and breaking force of kamaboko gel wasobserved at increasing levels of trypsin inhibitor while gelwhiteness decreased slightly

232 Starch Starch is widely used to make fish-paste prod-ucts as it enhances elasticity and increases the weight ofthe products In attempts to control thermal stability stick-iness andor wetness under different serving and storageconditions the functional characteristics of surimi seafoodproducts have been widely studied using modified starchesStarch is the second most abundantly used ingredient in themanufacturing of fish-paste products because of its higherwater-holding ability and capacity to replace fish proteinspartially while preserving the desired gel features at a reducedcost [69 157ndash161]

Kim et al reported a positive correlation between theamount of added starch and the quality of the food products[162] Konoo et al studied the effects of adding starch andamylose to amylopectin contents of starch on the gela-tion properties of frozen walleye pollack surimi [50] Thebreaking strength of gel was not affected by the changein amylose amylopectin ratio However it increased as thecontent of amylose increased in pregelatinized starch [51]A lower packing effect was observed at 90∘C which hypoth-esized that the gelatinization of starch in fish meat can beprevented at this temperature A strong correlation betweenthe amylose to amylopectin contents and the textural andrheological properties of starch-containing surimi gels wasalso reported by Lanier et al [134]

The addition of normal and modified potato or sweetpotato starch resulted in reductions in the characteristicstorage modulus of surimi sols during heating [52] Surimigels supplemented with potato starch showed the highestfirmness and cohesiveness Yoo reported the best texturalproperties of the sand lance (Ammodytes personatus) fish-paste products at a level of 8 potato starch [53] Thesestudies show that potato or sweet potato starch can also beused as a potent food additive for the production of surimi

233 RiceRice Flour Fish meat and wheat flour are themajor ingredients used for the production of surimi-basedproducts Rice flour however can be an important ingredientto enhance the rheological properties of surimi-based prod-ucts Several attempts have been made to evaluate the poten-tial of rice flour as an alternate of wheat flour in the prepara-tion of surimi products [41] The effect of rice flour additionmethods and milling types on the sensory and rheologicalattributes of surimi products were studied by Cho et al [54]

Roll-mil rice at a concentration of 10ndash15 displayed highergel strength and sensory properties which show that roll-millrice had strong potential for replacing wheat flourThe surimiproducts containing rice flour showed similar rheological andsensory characteristics to those of a finest commercial surimiproduct Hence rice flour might be an effective alternative towheat flour for high-quality surimi products

To replace wheat flour Kwon and Lee examined thequality characteristics of fried fish cakes containing rice flour[55] The total content of corn starch and rice flour was2883 of the total content of fish cake doughThere were nonoteworthy differences in the pHmoisture level appearancecolor flavor taste and overall acceptance as compared tothe control group The addition of 50 rice flour to surimi-based products could be an effective way to increase thecontent of rice flour without decreasing texture acceptabilityYoon et al optimized the content of water and rice flourin surimi-based products [56] The surimi-based productsmanufactured under optimal environment were comparablein gel strength to the commercial products However highersensory evaluation scores were observed compared to thoseof the commercial products These studies advocate that therice flour not only can be employed as an alternative to wheatflour but can also be used to enhance the quality of surimiand surimi-based products

234 Potato Powder The food additives extracted frompotato and potato protease inhibitors used in the preparationof fish-paste products are discussed in Sections 21 232 and244

24 Cryoprotectants and Humectants To inhibit denatura-tion and to lessen the damage of gel quality during coldstorage cryoprotectants are usually added to surimi productsPolyunsaturated fatty acids protein additives polyols sugarsamino acids salts and plant extracts are frequently usedas cryoprotectants and humectants to avoid fluctuationsin myofibrillar proteins promoted by freezing storage orthawing [163] Mechanical properties of surimi gels can beimproved by the addition of numerous hydrocolloids such askonjac carrageenan locust bean xanthan gum and differentmicrobial transglutaminases during the preparation of surimiproducts [57 164ndash166] In contrast the addition of alginateshas been reported to weaken surimi gels [69]

241 Saccharides Xanthan is a nongelling polysaccharideproduced by the aerobic fermentation of Xanthomonascampestris [167] The property of xanthan to form highlyviscous and stable solution at low levels makes it acceptablein the food industry [168] Xanthan displays quite remarkablesynergistic interactions with other nongelling polysaccha-rides of the galactomannan family leading to increases in gelformation and viscosity [168 169] The three commerciallyavailable galactomannans are tara gum locust bean gum andguar gum

The impact of low methoxyl pectin on the mechanicalproperties of silver carp surimi gels was studied by Barreraet al [58] An increase in hardness shear stress and water-holding capacity of the surimi gel was observed while no

12 Journal of Food Quality

significant improvement in the mechanical properties wasobserved as compared to the control Benjakul et al reportedthe effects of prawn-shell chitosan on surimi prepared bybarred garfish (Hemiramphus far) [59] Prawn-shell chitosanat a level of 1 of the surimi gel showed an increase in gel-enhancing effect on the heat-induced gelation of myofib-rillar proteins The addition of microbial transglutaminasegenerally increases the deformation and breaking force ofsurimi gel However this effect was significantly retardedin the presence of prawn-shell chitosan resulting in lowermagnitudes of deformation and breaking force

The viscoelastic properties and the thermal stability oflow-grade squid (Dosidicus gigas) surimi were investigated byIglesias-Otero et al [60] The konjac glucomannan aqueousdispersion at a level of 1 expressed the best rheologicalproperties suggesting that the konjac glucomannan aqueousdispersion may be used to enhance the quality characteristicsof low-grade squid surimi gel Ramırez et al evaluated theeffect of protein-hydrochlorides on the gel-forming ability ofmyofibrillar proteins [142] The xanthanlocust bean gum ata ratio of 025075 showed a positive improvement in themechanical attributes of surimi gels Eom et al investigatedthe impact of carrageenan on the gelation property of salt-based Alaska pollock surimi [61] The addition of 15KCl rather than 2 NaCl significantly enhanced the gellingproperty of 120581-carrageenan-induced surimi gel and showedincreased gel strength breaking force and whiteness values

242 Salts Salts help in protein-protein interaction and theaddition of salt is critical during the processing of fish-pasteproducts However the high levels of sodium in foods andconsequently human consumption of sodium have becomea global issue The prime harmful effects of excess sodiumintake are hypertension and increased blood pressure Sub-sequently these conditions lead to cardiovascular diseasesincluding instances of stroke heart attack and relateddiseases as well as gastric cancer and osteoporosis [170ndash172] Therefore to reduce sodium intake levels in fish-pasteproducts Hwang et al prepared the sodium-reduced friedfish cakes containing potassium as a substitute for sodium [1]The quality characteristics of 30 sodium-reduced fried fishcakes were not notably different from those of full-sodiumfried fish cakes however the addition of potassium changedthe color and reduced consumer acceptance To increase theconsumer preference for sodium-reduced fried fish cakes theuse of different food additives might be advantageous

The weak gel-forming ability and the strong fishy smellof the giant squid (D gigas) make it undesirable for themanufacturing of surimi-based products To overcome theseproblems Choi and Kim used Amorphophallus konjac flourto enhance the quality characteristics of giant-squid surimiproducts [62]The increasing levels ofA konjac flour showedincreases in gel texture and water retention ability while areduction in color and taste was observed as compared tothe commercial surimi products The incorporation of theseasoning ingredients such as sweeteners might be helpfulin removing the fishy smell of D gigas ultimately improvingthe gel properties of giant-squid surimi Cando et al reportedthat the sensory and mechanical properties of surimi gels

with reduced-NaCl contents can be improved by the appli-cation of 300Mpa high hydrostatic pressures [63] The gelsmade with lower-NaCl contents revealed stronger and stablenetworks as showed by the ones with higher-NaCl contents

243 Water Activity It has been reported that humectantshad the greatest effect on lowering water activity (119886

119908) with

the efficiency of the reduction in 119886119908value decreasing in the

order of NaCl sodium lactate glycerin propylene glycoland sorbitol when each of them was combined with otherhumectants [173] Kim and Park reported the impact ofhumectants such as sodium chloride sugars and polyols tolower the water activity (119886

119908) of various model kamaboko gels

[64]The effect of sodium chloride on lowering water activity(119886119908) was the highest among all of the examined treatments

while glucose caused browning reaction on the surface ofkamaboko In another study they examined the effect ofstarch glycine and sodium lactate in lowering the wateractivity (119886

119908) of model kamaboko gels [65] Sanchez Pascua et

al reported that glycerol (15ndash50) was effective in reducingthe water activity (119886

119908) in Brazilian sand perch (Pseudopercis

semifasciata) and mackerel (Scomber japonicus marplatensis)[66] Among the tested humectants the efficiency of thereduction in water activity (119886

119908) was observed decreasing in

the order of sodium lactate glycine and starch

244 Polyuronides The effect of sodium and calcium salts ofcarboxymethyl and polyuronides cellulose on the strength-ening of kamaboko gels was investigated by Niwa et al [67]It was reported that the calcium salts of pectinic acid pecticacid alginic acid and carboxymethyl cellulose enhancedthe breaking force of Alaska pollock surimi whereas theirsodium salts except Na-pectinate failed to increase the break-ing force The increase in the breaking force induced by cal-cium carboxymethyl cellulose vanished upon increasing thedegree of substitution of hydroxyl groups to carboxymethylgroups Furthermore fine cellulose particles enhanced thebreaking strain and breaking force and reduced the amount ofexpressible water but were unsuccessful in the case of coarserparticlesThe addition of potato starch can increase the effec-tiveness even in the presence of coarse particles of cellulose

245 Ascorbic Acid The addition of dehydro-L-ascorbicacid and L-ascorbic acid to Alaska pollock surimi increasedthe gel strength [68] It was suggested that the positiveeffect of L-ascorbic acid on gel formation might be due tothe oxidation of sulfhydryl groups in fish proteins Lee etal studied the effects of sodium-L-ascorbate on the gel-forming abilities of surimi prepared by Alaska pollock [69]Sodium-L-ascorbate remarkably enhanced the gel firmnesscohesiveness strength and sensory properties of the fiber-ized products at a level of 02 It directly influenced thesurimi quality regardless of vacuum treatment indicatingthat airborne oxygen was not important Freeze-syneresisstimulated by ascorbate during frozen storage was lessenedby the application of hydroxypropylated-modified starch

246 Unsaturated Fatty Acids The addition of nutritionallybeneficial 120596-3 fatty acids during surimi preparation could

Journal of Food Quality 13

enhance the gel strength and stability [70] For the effectiveuse of highly unsaturated fatty acids such as docosahexaenoicacid (DHA) and eicosapentaenoic acid (EPA) in surimi-basedproducts Okazaki et al studied the gel-forming properties offrozen walleye pollock surimi containing DHA and EPA [71]They reported that to achieve a good quality product thevigorous agitation of surimi with fish oil is essential to allowthe heat-induced gelation of its emulsified product throughthe formation of fine oil droplets

Fukushima et al investigated changes in the physi-cal properties of heat-treated surimi gels prepared fromthreadfin breamwalleye pollock Japanese jackmackerel andwhite croaker [72] The breaking strain breaking strengthand water-holding capacity of the heat-treated gels becamegreater as the amount of fish oil increased Furthermoresurimi seafood was nutritionally enhanced with 120596-3 polyun-saturated fatty acid- (PUFA-) rich oils isolated from natu-ral sources such as algae flaxseed menhaden blend andkrill [73] The Alaska pollock surimi supplemented with120596-3 PUFA-rich oils showed improved protein fundamentaltextural properties heat-induced gelation and endothermaltransitions These studies show that the interaction of unsat-urated fatty acids and surimi proteins could contribute to theimprovement in gel properties without altering the texturalattributes

247 Plant Ethanol Extracts The effect of commercial tan-nin and ethanolic Kiam wood extract on the gelling char-acteristics of ice stored mackerel (Rastrelliger kanagurta)surimi was investigated by Balange et al [74] During12 d of iced storage pH TBARS TCA-soluble peptide andtrimethylamine (TMA) contents as well as total volatilebase (TVB) of mackerel mince increased while gel-formingability myosin heavy chain band intensity and whitenessdecreased consistently Deterioration lipid oxidation andprotein degradation proceeded as storage time increasedAn increase in deformation and breaking force of surimigel was observed with the addition of 030 commercialtannin or 015 ethanolic Kiam wood extract during the first6 d of storage Therefore commercial tannin and ethanolicKiam wood extract had not shown a gel-enhancing effecton mackerel surimi Furthermore Buamard and Benjakulinvestigated the effects of coconut husk ethanolic isolateson the gel-forming ability of sardine (S albella) surimi [75]Breaking force increasedwith the increasing levels of coconuthusk ethanolic isolates while a decrease in whiteness and nodetrimental effect on the sensory attributes of surimi gel wasobserved It was concluded that the addition of coconut huskextracts at a suitable concentration could enhance the gelstrength of sardine surimi with increased acceptability

25 Compound Additives The effect of different oxidizedphenolic compounds such as tannic acid OTA ferulic acidOFA caffeic acid OCF and catechin OCT on the gellingattributes of mackerel (R kanagurta) surimi was studied byBalange and Benjakul [76] Gels supplemented with 050OTA 040 OFA 010 OCT or 050 OCF showedincreases in deformation and breaking forces while a decreasein the expressible moisture content and myosin heavy chain

band intensity was observed In another study they inves-tigated the effects of oxidized phenolic compounds on thegel-forming abilities of bigeye snapper (P tayenus) surimi[77] An increase in breaking force and deformation witha decrease in expressible moisture contents was observedGels supplemented with the oxidized phenolic compoundshad a finer matrix with smaller strandsThe physicochemicalcharacteristics of natural actomyosin advocate that oxidizedphenolics could trigger the induction of disulfide bondformation or the conformational changes and cross-linkingthrough amino groups Therefore the addition of oxidizedphenolic compounds at an optimum concentration couldenhance the strength of surimi gel

Yongsawatdigul and Piyadhammaviboon reported aninhibition in autolysis of surimi and mince preparedby lizardfish (S tumbil) caused by p-tosyl-L-phenylalanylchloromethyl ketone and phenylmethanesulfonyl fluorideindicating the involvement of myofibrillar-associated serineproteinase Tropomyosin and myosin heavy chain proteinswere mainly hydrolyzed resulting in poor textural prop-erties [26] Arfat and Benjakul investigated the effect ofzinc chloride (ZnCl

2) and zinc sulfate (ZnSO

4) on the gel-

forming abilities of surimi produced by yellow stripe trevally(Selaroides leptolepis) [78] The kamaboko gels with ZnSO

4

added up to levels of 60120583molkg showed increased deforma-tion whiteness and breaking force as well as highly denserand interconnected gels Therefore ZnSO

4at a suitable

concentration could enhance gel strength and whiteness ofdark-fleshed fish surimi

3 Improvement in Quality andFunctionality of Fish-Paste Products

Various food additives from seafood (eg fish invertebratesand seaweed) plants (eg vegetables fruits and herbalmedicines) mushrooms animal sources and functionalmaterials used to improve the quality and functionality offish-paste products are listed in (Table 2) and describedbelow

31 Seafood Additives It has been reported that various typesof seafood namely fish including dried anchovy (Engraulisjaponicus) powder [79 80] pufferfish (Lagocephalus lunaris)powder [88] and skate (Raja kenojei) powder [81 82] andinvertebrates including warty sea squirt (Styela clava) groundflesh [83] its freeze-dried tunic powder [84] omandungi(Styela plicata) ground flesh [85] shrimp (Acetes japonicus)powder [86] and seaweed such as green laver (Ulva spp) [87]have been used to enhance the quality and functionality offish-paste

The boiled and dried Japanese anchovy (E japonicus)is a popular fisheries product in Korea and Japan As theflesh can be eaten together with bone boiled and driedanchovy products are regarded as good sources of calcium[174] Bae and Lee evaluated the properties of fried fish-paste with added anchovy (E japonicus) powder containinga high amount of calcium [79]The fish-paste containing 10anchovy powder displayed the highest values of adhesivenesshardness and strength In the overall acceptance of sensory

14 Journal of Food QualityTa

ble2Naturalfood

additiv

esused

toim

provethe

functio

nalpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Seafoo

dadditiv

es

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

1-2

[79]

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

5[80]

Skate

Rajakenojei

Fried

Hot

wind-dried

skin

and

cartilage

(64)p

owder

Seab

ream

Moistu

recontentcolortextural

andsensoryattributes

3[81]

Skate

Rajakenojei

Steamed

Ferm

ented

flesh

Nemipterusv

irgatus

Aminoacidand

moistu

recontentcolortexturaland

sensoryattributes

20

[82]

Wartyseas

quirt

Styelacla

vaFried

Groun

dflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

5[83]

Wartyseas

quirt

Styelacla

vaFried

Freeze-drie

dtunicp

owder

Frozen

Itoyori

Colortexturaland

sensory

attributes

1[84]

Pleatedseas

quirt

Styelaplica

taFried

Grin

dedflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

15

[85]

Shrim

pAc

etesjaponicus

Fried

Powder

Frozen

seab

ream

surim

iMoistu

recontentcolortextural

andsensoryattributes

5[86]

Green

laver

Ulva

spp

Fried

Powder

Frozen

seab

ream

surim

iColorsensory

attributes

5[87]

Pufferfish

Lagocephalus

luna

risFried

Powder

Nemipterusspp

Moistu

recrude

protein

lipid

colortexturalandsensory

attributes

5[88]

Maesaengi

Capsosiphon

fulve

scens

Fried

Freeze-drie

dpo

wder

Frozen

seab

ream

surim

iColortexturaland

sensory

attributes

5[89]

Redsnow

crab

Chionoecetes

japonicus

Fried

Leg-meat

powder

Frozen

Alaskap

ollock

(Tchalco

gram

ma)

Physiochem

icalandsensory

attributes

6[90]

Plantsou

rcea

dditives

Mulberryleaf

Morus

alba

Fried

Powder

Seab

ream

Colortexturesensory

attributes

05

[91]

Onion

Alliu

mcepa

Fried

Ethano

lextract

Cutla

ssfishpaste

Moistu

recontentTB

CVBN

colorsensoryattributes

3[70]

Lotusleaf

Nelumbo

nucifera

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

05

[92]

Beetroot

andSpinach

Beta

vulga

risand

Spinaciaoleracea

Microwave

inkamaboko

shape

mold

Freshbeet

rootspinach

dish

Not

mentio

ned

Moistu

retexture

analysis

Beetroot10

Spinach15

[93]

Citrus

fruits

Citru

slim

onC

junosC

unshiu

Fortun

ellajaponica

varmargarita

Steamed

Groun

dflesh

pulpwith

out

seeds

Min

Daegu

flesh

Colortexturaland

sensory

attributes

Cumqu

at[94]

Journal of Food Quality 15

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Oatbran

+SiO2

Avenasativa

Boiled

Powder

Frozen

Alaskap

ollock

surim

iColortexturaland

physiochem

icalattributes

6gOatbran10

0gSiO2

[95]

Yam

Dioscorea

japonica

Fried

Powder

Pollo

cksqu

idshrim

pFo

ldingtest

colortexturaland

sensoryattributes

2[96]

WolfberryC

hinese

Goji

Fructuslycii

Fried

Powder

Seab

ream

Texturalandsensoryattributes

3[97]

Redginseng

Pana

xginsengCA

Meyer

Fried

Powder

Not

describ

edColorlipid

oxidation

sensory

attributes

1[98]

Korean

angelicar

oot

Angelicae

gigantis

Radix

Fried

Powder

Seab

ream

Texturalandsensoryattributes

05

[99]

Turm

eric

Curcum

alongaL

Fried

Powder

Pollo

cksqu

idshrim

pColorrheologicalandsensory

attributes

3[100]

Wasabi

Wasabiajaponica

Fried

Freeze-drie

dpo

wder

Silver

pomfre

t(Pam

pusa

rgenteus)

ColorT

BCviablec

ellcou

nt

texturalandsensoryattributes

18

[101]

Wolfip

oriaextensa

Poria

cocos

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

3[102]

Mushroo

madditiv

es

Butto

nmushroo

mAg

aricu

sbisp

orus

Fried

Chop

ped

fresh

Argyrosomus

argentatus

Texturalandsensoryattributes

10

[103]

Enok

imushroo

mFlam

mulina

velutip

esFried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

5[104]

Shiitakem

ushroo

mLentinus

edodes

Fried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

10

[105]

King

oyste

rmushroo

mPleurotuseryngii

Fried

Paste

Silver

whitecroaker(Penn

ahiaargentata)

Texturalandsensoryattributes

10

[106]

King

oyste

rmushroo

mPleurotuseryngii

Steamed

Paste

Cuttlefish

(Sepiaesculen

ta)

Texturalphysio

chem

ical

sensoryattributes

40

[107]

Animalsource

additiv

es

Poultrychicken

Gallusgallus

domesticus

Fried

Breastmeat

batte

r

Itoyori

Japanese

threadfin

bream(Ne

mipterus

japonicus)

Chem

icalcompo

sition

color

fatty

acid

compo

sition

TBARS

sensoryattributes

746

or1493

[108]

Functio

nalfoo

dadditiv

es

Long

-chain

cellu

lose

mdashBo

iled

Powdered

cellu

lose

Alaskap

ollock

surim

iTexturalandrheological

attributes

6[109]

Dietary

fiber

from

ascidian

tunic

Halocynthiaroretzi

Boiled

Refin

eddietaryfib

erAlaskap

ollock

surim

iColortexturalph

ysiological

andsensoryattributes

5[110]

16 Journal of Food Quality

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Fibera

nd120596-3

oil

mdashHeatedin

awater

bath

Powdered

fiber120596

-3oil

Alaskap

ollock

surim

iTexturalandrheological

attributes

Fiber6ndash

10g

and120596-3100

g[111]

Flaxseed

orsalm

onoil

Not

describ

edCoo

kedin

awater

bath

Oil

Frozen

Alaskap

ollock

surim

i(Tchalco

gram

ma)

TBARS

colortexturaland

sensoryattributes

2g10

0gfranks

[112]

Soybeanoil

Glycinem

axHeatedin

awater

bath

Oil

Frozen

silverc

arpsurim

iColortexturalattributes

Soybeanoilgt3

[113]

Calcium

powdero

fcuttlefish

bone

treated

with

aceticacid

Sepiaesculen

taHeatin

gin

awater

bath

Calcium

powder

Alaskap

ollock

surim

iMoistu

recontentcolortextural

andsensoryattributes

009

[114]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Alaskap

ollock

meatp

aste

Colortexturaland

sensory

attributes

017

[115]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Sand

lance

(Hypoptychus

dybowskii)

Acid

andperoxide

valueVBN

sensoryattributes

02

[116]

Cheong

gukjang

Ferm

entedGlycine

max

byBa

cillussp

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

2[117]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 17

evaluation small and large size fish-paste with 1 and 2respectively of added anchovy powder was preferred Thesimilar increasing trend of calcium intensity was observedby Bae et al [80] However the fried fish-paste productscontaining 20 anchovy powder displayed the highest valuesof adhesiveness hardness and strength Regarding overallacceptance in the sensory evaluation the fried fish-pastecontaining 5 anchovy was preferred The optimal amountsof added anchovy in the results from Bae and Lee and Bae etal were different which might have been due to the differentdrying methods and sizes of the anchovies used in each study[79 80] Despite the differences in the two studies the resultssuggest that anchovy powder could be applied to fried fish-paste products to achieve high calcium contents

Skate contains many essential fatty acids includinglinolenic acid linoleic acid arachidonic acid DHA andEPA [175] Skate skin contains high percentages of collagenprotein and calcium [176] while its cartilage is rich inchondroitin sulfate [177] To improve quality and nutrientlevels Cho and Kim prepared fried fish-paste with skate (Rkenojei) powder (hot wind-dried skin and cartilage powder[6 4]) [81] According to Park et al preference testingusing steamed fish-paste product with different levels ofadded 14-day-fermented flesh of skate showed significantincreases in brownness smoothness and skate flavor scores[82] The amino acid contents of fish cake samples with20 skate added had the highest overall preference scoresConsequently the addition of 20 skate powder was optimalfor the steamed fish cake to improve its quality characteristicswith higher protein contents

Warty sea squirt (S clava) aquaculture in the Masanarea of Korearsquos south coast contains abundant unsaturatedfatty acids and essential amino acids in its flesh [178] andglycosaminoglycan in its tunic [179] Warty sea squirt has aunique taste and distinct antioxidant and anticancer activities[180] Fried fish-paste supplemented with 20 warty seasquirt (Korean name miduduk) displayed improved qualityand functionality [83] Choi et al reported a fried fish-paste containing freeze-dried byproduct of warty sea squirt(S clava tunic) [84] The hardness and strength of fish-paste increased with increasing amounts of tunic powderFor overall acceptance in sensory evaluation a fish-pastesupplemented with 1 S clava tunic obtained a relativelyhigher score The results suggested that S clava flesh andtunic could be used for fish-paste products to improve theirquality and functionality Park et al reported improvementin the functional properties of fish-paste by adding S plicata(Korean name omandungi) [85] Fried fish-paste containing20 S plicata indicated the highest values of adhesivenesshardness and strength For overall acceptance in sensoryevaluation a fish-paste containing 15 S plicata obtained thehighest score

Seo and Cho reported the preparation of fish-paste withadded shrimp (A japonicus) powder [86] The hardnessspringiness and cohesiveness increased with the increasingconcentration of shrimp powder However the brittlenessand gumminess reduced In the sensory evaluation the fish-paste prepared with 5 shrimp powder was most preferredCho and Kim reported the preparation of fish-paste with

added green laver (Ulva spp) powder [87] The hardnessspringiness and cohesiveness increased with the increasingconcentration of green laver powder However the brittlenessand gumminess decreased upon the addition of green laverpowder In the sensory evaluation a fish-paste prepared with5 green laver powder was preferred over other fish-pastesThese results suggest that green laver powder could be appliedto fish-paste to improve its quality and functionality

Pufferfish containing taurine hydroxyproline lysine andglycine impart a characteristic taste to food [181] To improvethe taste of fish-paste products Park prepared a fish-pasteby adding green rough-backed pufferfish (L lunaris) pow-der [88] The hardness strength gumminess springinessand chewiness of the fish-paste increased depending onpufferfish powder contentThe preparation of fish-paste withadded Capsosiphon fulvescens powder was reported by Park[89] The hardness springiness strength and cohesivenessincreased with the increasing concentrations of C fulvescenspowder However the brittleness and gumminess reducedwith the addition of C fulvescens powder In the sensoryevaluation overall the fish-pastes prepared with 5 Cfulvescens powderwere preferred over other fish-pastesThusthe results show that C fulvescens powder could be used tocreate fish-paste products with high quality and functionality

Kim et al reported the changes in the sensory and physic-ochemical properties of a fish-paste containing red snow crab(Chionoecetes japonicus) leg-meat powder [90] Hardnessgumminess springiness and cohesiveness increased withincreasing levels of red snow crab leg-meat powder Based onthe sensory evaluation it was concluded that the addition ofred snow crab leg-meat powder at a level of 6 could improvethe quality characteristics of fish-paste products

32 Plant Source Additives It has been reported that variousplant sources namely vegetables (eg mulberry beetrootand spinach) fruits (eg citrus) and herbal medicines (egChinese matrimony vine Korean Angelica root) have asignificant effect in improving the quality and functionalityof fish-paste products

Mulberry (Morus alba) leaf has been used traditionallyto treat a disease symptomized by thirst and stroke [182]Ever since mulberry leaf was included as a food material inthe Food Codex in 1988 by the Ministry of Food and DrugSafety (MFDS Osong Chungju South Korea) Mulberry leafpowder has been used in various processed food productsand health functional foods Shin and Park reported theuse of mulberry leaf powder in the preparation of fish-pasteproducts [91] In a texture meter test the hardness increasedbut the cohesiveness springiness gumminess and brittlenessdecreased with increasing levels of mulberry leaf powder Insensory evaluation the fish-paste with 05 mulberry leafpowder revealed the highest acceptance scores in terms offlavor texture and overall quality

Garden onion (bulb onion Allium cepa) is a perennialplant belonging to Liliaceae and is widely used as a spice andseasoning vegetable in both the East and the West Park etal investigated the quality characteristics of fried fish-pastesupplemented with flavonol-rich ethanol extract of onion[183] In the sensory evaluation as the amount of ethanol

18 Journal of Food Quality

extract of onion increased so did the favorability in termsof flavor and taste Notably 3 ethanol extract of onion hadthe best score in overall acceptance The results indicate thatethanol extract of onion can be used to prepare fried fish-paste products with high quality and functionality

Shin reported the production of fish-paste with addedlotus (Nelumbo nucifera) leaf powder [92] The flavor adhe-siveness and hardness increased with the increasing levels oflotus leaf powder The fish-paste with 05 lotus leaf powderdisplayed the highest acceptance scores in terms of springi-ness pleasant taste appearance texture flavor and overallquality Thorat et al prepared kamaboko containing greenchili coriander ginger garlic spice mixture and groundbeetroot or a spinach dish and then subjected the preparationto microwave cooking [93] Kamaboko prepared with 10beetroot and a 15 spinach dish was found to be superior tothe others

Yang and Cho developed a steamed fish cake with added5 ground citrus fruits with skin [94] The addition of citrusfruits did not disturb the flexibility of surimi The pH ofsurimi samples increased in the following order lemon (Cit-rus limon) citron (Citrus junos) tangerine (Citrus unshiu)kumquat (Fortunella japonica var margarita) and controlThe hardness of surimi was highest for lemon followed bycitron tangerine kumquat and control surimi In the sensoryevaluation surimi containing kumquat demonstrated higherscores in terms of color taste and textural properties Theseresults suggest that surimi could be prepared by adding citrusfruits to improve the quality and functionality

Oat bran is a gluten-free dietary fiber that may decreasethe risk of diabetes and heart diseases The physicochemicalproperties of surimi gels supplemented with oat bran werestudied by Alakhrash et al [95] The oat bran and SiO

2

incorporation (6 g100 g) greatly improved water-holdingcapacity and gel texture while a reduction in whiteness wasobserved Kim and Byun conducted tests on the sensoryand physicochemical characteristics of fish-paste with addedyam (Dioscorea japonica) powder [96] The addition of yampowder increased gumminess strength springiness andcohesiveness In the sensory evaluation the addition of 2yam powder had the best scores in terms of taste color andoverall preference

Fructus lycii is a fruit produced by Lycium barbarumL that has been used for nourishment tonicity and nour-ishment of the blood it has antibacterial anticancer andantioxidant properties [182ndash186] Shin et al prepared friedfish-paste containing dried F lycii powder [97] In the texturalanalysis cohesiveness increased while brittleness and gum-miness decreased with increasing levels of F lycii powderThe 3 F lycii powder sample had the highest acceptancescores in terms of appearance texture taste flavor andoverall acceptability

Red ginseng-based fried fish-pastes containing differentsizes and amounts of red ginseng powder were preparedand their biological properties including lipid oxidation toimprove fish-paste quality were investigated [98] The fish-paste products containing red ginseng powder showed asignificant increase in hardness and chewiness Furthermorean inhibitory effect on lipid oxidation and reduced number

of total microbes during storage were observedThese resultssuggest that high-quality fish-pastes could be achieved withthe addition of 1 red ginseng powder which effectivelyimproved both sensory evaluation and physicochemicalproperties

Angelicae Gigantis Radix (the dried root ofAngelica gigasNikai) more popularly known as Korean Angelica is one ofthe widely used herbal medications [187] It has been usedin Korean medicine as an important medication for anemiaand blood circulatory disorders It has also been used formenstrual pains and postmenopausal syndromes Shin et alreported the development of fish-paste with A gigas powder[99] In a texture test hardness chewiness and brittlenessincreasedwith increasing concentrations of AngelicaeGigan-tis powderHowever cohesiveness and springiness decreasedIn the sensory evaluation the fish-paste with 05 AngelicaeGigantis powder showed the highest acceptance scores forappearance flavor taste texture and overall quality

Turmeric (Curcuma longa) has been used in Ayurvedicmedicine from ancient times as a treatment for inflammatoryconditions It has been reportedly used for its various bio-logical activities including antibacterial antiviral antifungalantioxidative and antiatherogenic effects [188] Turmeric hasbeen grown as a special crop in the central and southern areasaround Jindo in South Korea [189] Choi et al investigatedthe sensory and rheological properties of fish-paste preparedwith turmeric powder [84] In terms of textural attributesthe addition of C longa powder decreased springiness andimproved strength In the sensory evaluation the addition of3 C longa powder was associated with the best scores fortaste and overall preference

Wasabi (Wasabia japonica) has various beneficialhealth properties including antioxidative antimicrobialand antimutagenic activities [190 191] Jang et al reporteda high-quality fried fish-paste product made with silverpomfret (Pampus argenteus) which is one of the savorysoft and delicious types of fish prepared by adding wasabipowder [101] Notably hardness gumminess and chewinessincreased significantly with the addition of wasabi powderIn the sensory evaluation 18 wasabi powder showed thebest score in overall acceptability These results show thatwasabi could be used as a food additive or preservative infish-paste products

White Poria cocos wolf is the inner white part of P cocosa parasite found on Pinus densiflora It is used to treat edemachronic gastritis gastric atony nephrosis acute gastroentericcatarrh emesis dizziness and vomiting [192 193] Shin et alprepared a fried fish cake with added white P cocos powderand studied the textural and sensory characteristics [102]In texture tests brittleness was observed to increase whilespringiness decreased with increasing concentrations of Pcocos powder The fish-paste product containing 3 whitePoria cocos powder showed the highest acceptance scores forflavor appearance texture taste and overall quality

Milk-vetch root is one of the most produced herbalmedicines in Korea It is a peeled and dried root of the herba-ceous perennial herb known as Astragalus membranaceuswhich belongs to the Fabaceae family [194] It has been

Journal of Food Quality 19

reported that milk-vetch root exerts diuretic tonic anti-hypertensive hypoglycemic immune-enhancing antitumorand antiviral effects [195] Kim investigated the sensoryand physicochemical properties of fish-paste prepared withmilk-vetch root powder [196] The strength cohesivenessbrittleness and gumminess of the fish-paste increased whileits springiness decreased with an increasing amount of milk-vetch root powder In the sensory evaluation the addition of10 milk-vetch root powder indicated best scores for tastetexture color and overall preference

33 Mushroom Additives Mushroom is a nutritional andfunctional food as well as a vital source of physiologicallybeneficial medicines Mushrooms have been used as tradi-tional medicines in Korea Japan China and other Asiancountries for curing various diseases including lymphaticdisease gastroenteric disorder oral ulcer and various can-cers [197] It has been reported that edible mushrooms inKorea number approximately 350 species [198] Several ediblemushrooms that are highly preferred have been added to fish-paste to enhance their quality and functionality

Ha et al prepared a fried fish-paste product with addedAgaricus bisporus which is a product described as having aracy flavor and taste [103]The elasticity hardness brittlenessand gumminess of fish-paste with the added mushroomincreased however no significant difference in strengthwas observed Regarding overall acceptance in a sensoryevaluation a fish-paste supplemented with 10 A bisporusmushroom showed the highest scores

Enoki mushroom (Flammulina velutipes) is well knownfor its anticarcinogenic and blood pressure-reducing prop-erties To utilize its functional properties enoki mushroomwas added to fried fish cake [104] The sample containing15 mushroom received the highest values for strengthgumminess and brittleness In the sensory evaluation thefish cakes with 5 mushroom obtained favorable scores foroverall acceptance

Shiitake mushroom (Lentinus edodes) is known for itshigh level of 120573-glucans Son et al investigated the effectsof shiitake mushroom on the textural properties of friedfish cake [105] The fish cake containing shiitake mushroomreceived the highest values for strength hardness gummi-ness and brittleness In the sensory evaluation the fish cakeswith 10 shiitake mushroom sample obtained the best scorefor overall acceptance

Kim et al prepared a fried fish cake using cultured kingoyster mushroom (Pleurotus eryngii) and silver white croaker(Pennahia argentata) surimi to enhance its physiologicaleffects [106] In assessing its quality properties fish cake towhich 10 mushroom was added received the highest valuesfor strength hardness gumminess and brittlenessThe effectof king oyster mushroom on the textural and physicochem-ical properties of steamed cuttlefish (Sepia esculenta) fishcake was investigated by Chung et al [107] The fish-pastewith added king oyster mushroom paste revealed significantdecreases in gumminess cohesiveness and hardness whilethe springiness increased with increasing concentrations ofking oystermushroompasteOn the sensory evaluation basisthe cuttlefish-paste supplemented with 30ndash50 king oyster

mushroom showed higher overall acceptability In the studiesby Kim et al and Chung et al the optimal amounts of kingoyster mushroom differed which might have been due tothe different cooking methods and surimi used in each study[106 107]

34 Animal Source Additives Jin et al investigated the effectof chicken meat on the quality characteristics of Itoyori(Japanese threadfin bream Nemipterus japonicus) surimi[108] The physicochemical properties such as fatty acidcomposition shear force and gel characteristics were affectedby substitution with spent laying hen meat batter Howeversensory characteristics were less affected by this substitutionA huge amount of waste in the processing of grass carp isdiscarded To deal with this waste Gao et al studied theprocessing technology used for fish and mushroom pastewith salted fish cubes mushroom soybean and fermentedsoybeans [199]

35 Functional Food Additives Functional food additivesincluding dietary fiber 120596-3-rich oil calcium additives andpropolis have been used in the preparation of fish-pasteproducts to increase their quality and functionality Westernpopulations have an inadequate quantity of health beneficialdietary fiber in their diets Besides fiber most Western pop-ulations also consume an insufficient amount of 120596-3 PUFAswhile their sodiumconsumption greatly surpasses the recom-mended maximum Debusca et al prepared Alaska pollocksurimi fortified with commercial long-chain cellulose as asource of dietary fiber [109] Fiber fortification up to a level of6 improved both texture and color a slight decline in thesevalues was observed at levels of 8 fiber An increase in gelelasticity and thermal gelation of the fish cake was observed

Yook et al prepared a fish-paste by adding dietaryfiber extracted from ascidian (Halocynthia roretzi) tunic toenhance its physiological properties [110] The hardnessgumminess adhesiveness shear force and chewiness of thefish-paste improved with the incorporation of the ascidiandietary fiber The fish-paste with 5 ascidian dietary fiberscored the highest and was generally preferred by sensorypanels Tolasa et al reported that the oxidative stability andthe uniform dispersion of 120596-3 unsaturated fatty acids can beattained in a highly consistent surimi gel system without theuse of antioxidants [200]

Surimi and surimi-based products are famous through-out the world In fact US consumption increased in the1980s while the rate leveled off thereafter The nutrificationof food products with 120596-3 PUFAs increases the health ben-efits of food consequently increasing their market demandPietrowski et al prepared surimi seafood products nutrition-ally enhanced with 120596-3 PUFAs [201] Although the nutrifica-tion of 120596-3 PUFAs indicated an increase in lipid oxidationit was within limits acceptable to consumers The color ofsurimi seafood nutrified with 120596-3 PUFAs generally improvedbut no effect on textural characteristics was observed

Debusca et al reported that the fortification of Alaskapollock surimi with either 120596-3 oil or dietary fiber alone orin combination improved both the textural and rheologicalproperties [111]The120596-3 oil and fiber in combination revealed

20 Journal of Food Quality

greater gelation of surimi and a slight reduction in color prop-erties indicating their interaction with myofibrillar proteinsThus it was suggested that the 120596-3 oils and fiber could beeffectively used as a fortifying agent to prepare high-qualitysurimi products with nutritional benefits Sell et al preparedsurimi franks fortified with salmon oil or flaxseed [112]The textural properties showed differences between franktypes with the flaxseed franks being cohesive less gummysofter and chewy while the sensory evaluation showed nosignificant differences

Chang et al determined the effects of soybean oil andmoisture contents on the physical properties of surimi gels[113] The increasing levels of soybean oil and moisturecontents resulted in an increase in whiteness and reductionin the chewiness hardness and breaking force Setting incombination with soybean oil improved the textural andcolor parameters of surimi gels indicating that soybean oilcould be used to improve the color and textural properties ofsurimi seafood products

Kim et al prepared boiled fish cake using acetic acid-treated cuttlefish bone as a calcium additive agent [114] Theresults of sensory evaluation of texture and whiteness weresimilar to those without this supplementation In the mineralcontent analysis of heat-induced surimi gel calcium contentincreased depending on the increasing concentration ofacetic acid-treated cuttlefish bone powder while phosphoruscontent did not change The optimal concentration of aceticacid-treated cuttlefish bone powder for the preparation ofhigh-quality heat-induced surimi gel was 009

Kim et al prepared Alaska pollock fried fish-pastesupplemented with propolis [115] The addition of propolisenhanced the antispoiling and antioxidative ability as well asgel strength of fried fish-paste In the sensory evaluation theaddition of 017 propolis showed the best score in overallacceptability In another study Kim et al later studied sand-lance (Hypoptychus dybowskii) meat paste prepared withpropolis [116] Similar to the previous report the addition ofpropolis on the fried fish-paste showed higher antioxidativeand antispoiling activities The fried sand-lance meat pasteprepared with 02 added propolis was the most acceptableFurthermore the bitter taste of the sand-lancemeat paste wasreduced by adding 2 sweet amber powder

Cheonggukjang is an ancient Korean food prepared byfermented soybean It contains high levels of dietary fiberoligosaccharides isoflavones saponin lecithin phytic acidand phenolic compounds among others Its many benefi-cial properties have been reported such as thrombolyticanticancer antimicrobial hepatoprotective antioxidant andcholesterol-lowering effects [202] Park et al reported theuse of fish-paste containing cheonggukjang powder [117]Theincreasing concentrations of cheonggukjang resulted in anincreased value of springiness cohesiveness and hardnesshowever a reduction in brittleness and gumminess values offish-paste was observed

4 Shelf-Life Extension of Fish-Paste Products

Fish-paste products may easily spoil due to residualmicrobes that are not removed by sterilization during the

manufacturing process or by contamination in packagingor the distribution process For such reasons even vacuum-packed fried fish-paste products have a shelf-life of fewerthan 10 days during cold storage which is relatively short[121 122] Various efforts have been made to develop long-term storage solutions for fish-paste products via physicaland chemical methods [118ndash122] Although these methodswere found to be very effective for the long-term storageof fish-paste products they require sensitive and complexmanipulation and are costly

The addition of appropriate food additives to fish-pasteproducts as an effective preservation protocol is anotherstrategy Potassium sorbate is a typical synthetic food preser-vative and is commonly used in processed foods includingfish-paste productsThis material is effective in inhibiting thegrowth of variousmicroorganisms as it has a slight sterilizingeffectThe use of this material is permitted to a concentrationof less than 20 gkg in processed fish meat products (FoodCode Ministry of Food and Drug Safety Republic of Korea)According to the results of Walker sorbates and sorbic acidexert a very low level of mammalian toxicity even in chronicstudies as up to 10 of the diet did not show any carcinogenicactivity [203] In addition Thakur and Patel summarizedthe application of sorbates in the shelf-life extension of fishand fish-based products [204] The physical and chemicalmethods along with natural food preservatives for the long-term storage of fish-paste products are listed in Table 3 andbriefly described below

41 Physical and Chemical Methods Various efforts havebeen focused on developing long-term storage solutions forfish-paste products via physical methods including highpressurization [118] microwave pasteurization [93] highhydrostatic pressure treatment [119] and even irradiation[118 121] In addition it has also been reported that treatmentwith chlorine dioxide solution at an appropriate concentra-tion which is harmless to humans could be used to preventspoilage and to extend the shelf-life [122]

High hydrostatic pressure technology has graduallygained popularity in the food industry over the last twodecades [205] In 2013 the worldwide market for highhydrostatic pressure equipment was estimated to be $350million and it is expected to grow Besides high hydrostaticpressure technologies several types of radiation have alsobeen tested including ultraviolet microwaves and gammairradiation treatments Radiation is generally used to controlbiological hazards in the production of fish-paste productsand to prolong the shelf-life of such products [206 207]Gamma radiation exerts potent antimicrobial effects whereasultraviolet rays are effective for the surface but not interiorsterilization of porous dried fish products (eg fish-pasteproducts) However gamma irradiation treatment demandslarge-scale facilities and higher costs [207 208]

Miyao et al reported that growth of the majority of thepathogenic microorganisms present in surimi was inhibitedat a high pressure of between 300 and 400Mpa [118] Severalpressure-resistant strains were isolated from surimi and wereidentified as Moraxella sp Acinetobacter sp Streptococcusfaecalis and Corynebacterium sp It was suggested that

Journal of Food Quality 21

Table3Naturalfood

additiv

esandph

ysicochemicalmetho

dsused

toim

provethe

shelf-life

offish-paste

prod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Physicalandchem

icalmetho

ds

Highhydrostatic

pressure

mdash

High-pressure

treatmento

rheattre

atment

insampletub

ewith

vacuum

packaging

mdashFrozen

Alaskap

ollock

Microbialactiv

ity40

0MPa

[118]

Highhydrostatic

pressure

mdashNot

cooked

mdash

Tuna

fishpaste

Mackerelp

astewith

paprika

mackerelp

astewith

garlic

mackerelp

astealon

eand

salm

onpaste

Microbialactiv

ity200M

Pa[119]

Co-60

Gam

mar

ays

mdashGrilled

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

texturalsensorym

icrobial

physiochem

icalattributes

75kG

y[120]

Co-60

Gam

mar

ays

mdashFried

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

pHtexturalmicrobial

physiochem

icalattributes

3kGy

[121]

Chlorin

edioxide

(ClO2)

mdashSteamed

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

VBN

TBA

RSpHm

icrobial

physicochemicalsensory

attributes

50pp

m[122]

Naturalfood

additiv

esRe

dpepp

erethano

lextract(RP

EE)

andchop

pedfre

shredpepp

er(C

FRP)

Capsicu

mannu

umFried

Ethano

lextract

andchop

ped

fresh

one

Frozen

Alaskap

ollock

TBC

sensoryattributes

RPEE

10

CF

RP5

[123]

Ethano

lextract(EE)

andwater

extract

(WE)

Phellodendron

amurense

Eugenia

caryophyllu

sPinu

srigida

Bletillastr

iata

andPa

eonia

albiflora

mdashmdash

mdashAntim

icrobialattributes

onpu

trefactiveisolatesfrom

fish

meatp

asteprod

ucts

EE2000

ppm

[124]

Eggwhitelysozyme

(EWL)

andor

sodium

hexametapho

sphate

(SHMP)sod

ium

pyroph

osph

ate(SP

P)

Gallusgallus

domesticus

Fried

Powder

Frozen

Alaskap

ollock

Viablecellcoun

tpH

VBN

biochemicalattributes

EWL5

+SP

P05

+SH

MP

01

[125]

Grapefruitseed

extract

Citru

sparadisi

mdashSolutio

nCom

merciallyavailablefi

shmeat

paste

prod

ucts

Proxim

atec

ompo

sition

textural

biochemicalrheologicalsensory

attributes

1000

ppm

[126]

22 Journal of Food Quality

Table3Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Cinn

amon

bark

extract

Cinn

amom

umcassia

Fried

Extracted

solutio

nFrozen

Alaskap

ollock

Antim

icrobialactiv

itySprayeddiluted

extract(11)

[127]

Alginicacid

hydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Relativev

iscositypHcolor

rheologicalattributes

03

[128]

Chito

sanhydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Viablecellcoun

tsrheological

sensoryattributes

03

[129]

Nisin(N

)and

or

sucrosefattyacid

esters(SFE

)mdash

Steamed

Powdera

ndsolutio

nFrozen

Alaskap

ollock

Viablecellcoun

tantim

icrobial

activ

ityN125120583

gg+

SFE10mg

[130]

Piscicolin

KH1

Carnobacteriu

mmaltalomaticu

mSteamed

Solutio

nCod

fish

Inhibitory

assayproteincontent

antim

icrobialactiv

ity50

AUg

[131]

Zein

andsoyprotein

isolate(SPI)fi

lms

containing

greentea

extract(GTE

)

Zeamays

Glycinem

axCa

melliasin

ensis

Fried

Ediblefilm

(GC-WPI)w

ithGTE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

TBARS

colorm

icrobial

physicalattributes

GTE

1

[132]

Gelidium

corneum

(GC)

-Wheyprotein

isolate(G

C-WPI)

blendfilm

containing

grapefruitseed

extract(GSE

)

Gelidium

corneum

Citru

sparadisiBo

staurus

Not

mentio

ned

Ediblefilm

(GC-WPI)w

ithGSE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

Water

vapo

rpermeability

microbiologicalanalysis

sensory

attributes

GSE

01

[133]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 23

damage to the cell membrane and degradation of ribonucleicacids occurred in the high-pressure-treated cells Malickiet al investigated the use of high hydrostatic pressure toprolong the shelf-life of traditionallymanufactured fish-pastestored under refrigeration (4∘C) for 6 weeks [119] Neitherbacteria nor molds or yeasts were detected in the highhydrostatic pressure-treated fish-paste samples at any timepoint analyzed irrespective of the pressurization conditionsIn conclusion these studies revealed the effectiveness of highhydrostatic pressure to prolong the shelf-life of traditionallymanufactured fish-paste stored under refrigerated conditionsfor up to 6 weeks

Kim et al reported a reduction in the total aerobicbacterial counts in the grilled fish-paste stored at 5∘C andirradiated by gamma rays at a level of 25 kGy or more[120] Additionally the treatment of gamma rays at a levelof 75 KGy at 30∘C showed a significant inhibition in aerobicbacterial growth Cho et al investigated the effect of Co-60 gamma irradiation on fried fish-paste and studied thephysicochemical properties of fish-paste products stored atlow temperature (3 plusmn 1∘C) and room temperature (10ndash20∘C)[121] There was no obvious difference between the vacuum-and air-packed groupsThe irradiation of 3 KGy extended theshelf-life of fish-paste up to 2 times at room temperature and3-4 times at low temperature In both studies the irradiationtreatment caused very little textural degradation and no effecton the sensory characteristics of the samples was observed

Shin et al investigated the effects of chlorine dioxide(ClO2) treatment on the physiochemical andmicrobial prop-

erties of fish-paste products [122] After ClO2treatment

fish-paste samples were individually packed and stored at4∘C The pH and VBN values of fish-paste decreased withincreasing ClO

2concentration ClO

2treatment significantly

reduced the populations of total bacteria yeast and moldduring storage In particular treatment with 50 ppm ClO

2

significantly decreased the total bacterial count the mostamong all ClO

2-treated fish-pastes showing that 50 ppm

chlorine dioxide was the optimum concentration to prolongthe shelf-life of fish-paste products

42 Natural FoodAdditives Theuse of natural food preserva-tives rather than chemical and synthetic food preservatives isofworldwide interest It has been reported that several naturalfood additives could extend the shelf-life of cooked fish andfish products Some examples include onion ethanol extract[183] egg white lysozyme [125] grapefruit seed extract [126]chitosan hydrolysate [129] cinnamon bark extract [127] andred pepper extract [123] as well as mixtures of lysozymessodium hexametaphosphate and sodium pyrophosphate

The shelf-life of fried fish-paste products prepared byadding red pepper ethanol extract was estimated by Yoonet al [123] The shelf-life of the fried fish-paste with added10 red pepper ethanol extract and 5 chopped fresh redpepper was 2 to 3 days longer than that of the commercialfish-paste product thus demonstrating the most effectivepreservation effects According to Ahn et al the extractsof Eugenia caryophyllus Pinus rigida Bletilla striata andPaeonia albiflora exerted strong inhibitory effects on thegrowth of microorganisms isolated from putrefied fish-paste

[124] Notably the ethanol extract was more effective thanwater extract in all tested microorganisms The inhibitionlevel of each extract was evident at 2000 ppm ethanol in thefish-paste

Kim et al investigated the inhibitory effects of lysozymesmixtures of lysozymes and other antibacterial substancessuch as sodium pyrophosphate and sodium hexametaphos-phate on bacterial growth in surimi products [125] Thelysozymes inhibited growth in most of the tested isolatesand themixture of antibacterial substances showed increasedeffects compared with those when they were used individ-ually A mixture of 05 sodium hexametaphosphate 05sodium pyrophosphate and 005 lysozyme in imitationcrab and kamaboko showed the highest inhibitory activ-ity

The stabilizing effects of grapefruit seed extract on fish-paste products were investigated by Cho et al [126] Texturalproperties decreased with increasing storage period Thetreatment of fish products with grapefruit seed extract pro-longed the deterioration of fish-paste product proteins duringstorage up to 4-5 daysThe chemical sensory and rheologicalevaluation revealed that the grapefruit seed extract could beused as an effective additive to extend the shelf-life of fish-paste products

The predominant bacterium in most of the isolatedmicroorganisms from packed and unpacked spoiled fish-paste products is Bacillus sp [127] Notably yeast andmolds are not reported in the vacuum-packed products Ahydrolysate of alginic acid has antimicrobial activity but ithas not been used at industrial scale The alginic acid ata concentration of 03 prolonged shelf-life of fish-pasteproducts by 4 days at 15∘Cand inhibited the growth ofBacillussp isolated from fish-paste products [128] According to theresults of Cho et al the chitosan hydrolysate made withchitosanase from Aspergillus oryzae ATCC 22787 revealedthe strongest antimicrobial activity and inhibited the growthof Bacillus sp isolated from fish-paste products [129] Theaddition of chitosan hydrolysate at a concentration of 03resulted in extended shelf-life of up to 6 days at 15∘C Jeonget al reported that spraying cinnamon bark extract on thesurface of the fried fish-paste products could inhibit thegrowth of spoilage bacteria and mold at room temperatureand resulted in prolonged shelf-life [127]

Yamazaki et al investigated the effects of nisin andsucrose fatty acid esters on the growth of spoilage bacteria infish-paste products [130] Nisin exerted antibacterial activityagainst Bacillus subtilis and Bacillus licheniformis in a liquidmedium at 20∘C and resulted in a longer shelf-life forfish-paste products It was concluded that the addition ofnisin could be used as a potential alternative method toprevent spoilage caused by spore-forming bacteria in fish-paste productsThe bacteriocin produced byCarnobacteriummaltalomaticum had the ability to inhibit both Enterococcussp and Leuconostoc sp which reduce the shelf-life of fish-paste products during preservation [131] The results showedthat the purified bacteriocin piscicolin KH1 andor nisin sig-nificantly inhibited the growth of Leuconostoc mesenteroidesand Enterococcus faecium and could be used as a food-gradepreservative for kamaboko gels

24 Journal of Food Quality

Sakai and Yamaguchi examined the possibility of inhibit-ing lipid oxidation in boiled fish-paste by adding yuzu skinto the surimi [209] The heat-treated control kamabokoand yuzu skin-added kamaboko (citron kamaboko) wererefrigerated at 0∘C for 2 days and after heating the surimithe malonaldehyde content in both kamabokos was reducedThese results suggest that the addition of citron skin sup-pressed lipid oxidation in fish-paste products

Various packing materials and wrapping techniques havealso been employed to keep fish-paste products fresh and freeof contaminants for a longer period of time Lee et al investi-gated the processing conditions and quality stability of retortpouched fried-mackerel fish-paste during storage [210] Themackerel fish-paste was ground with added ingredients friedin soybean oil cooled vacuum-packed in a laminated plasticfilm and finally sterilized at 120∘C for 20min in a hotwater circulating retortThe reported method showed a goodpreservation for 100 days at 25 plusmn 3∘CThe sensory evaluationshowed no significant differences between the prepared fish-paste products and that of products in the market Ha et alexamined the optimum storage conditions for maintainingthe quality of the fried fish-paste in retort pouches [211]Both hardness and gel strength increased with increasingsterilization temperature On the other hand no differenceswere observed in elasticity and water-holding capacity

Lee et al elucidated the antioxidative effects of soyandor zein protein films containing green tea extract on thephysiological properties of fish-paste products during storage[132]The soy protein films showed an increase in yellownesswhile a decrease in yellowness was observed with the zeinfilms The lipid oxidation was retarded at day 2 of storageby wrapping the fried fish-paste products with soy and zeinprotein films containing green tea extract Lim et al prepareda Gelidium corneum whey protein isolate (GC-WPI) blendfilm containing grapefruit seed extract and studied the effectof this film on pathogenic bacterial inhibition during storage[133]TheGC-WPI blend was effective in decreasing the pop-ulations of Salmonella typhimurium Listeria monocytogenesand Escherichia coli on films treated with 01 grapefruitseed extract These studies suggest that packaging fish-pasteproducts in plant-based protein films containing green tea orgrapefruit seed extract could be beneficial to prolong shelf-life

5 Conclusion

The production of surimi dates back to ancient times How-ever advancement in surimi processing technology startedin 1960 with the discovery of cryoprotectants which werehelpful in maintaining the gel quality and functionality offish-paste for relatively longer periods of frozen storage [3]As themarket share of quality-conscious consumers rises thedemand for the use of natural additives rather than chemicalingredients for surimi products will continue to increaseAccording to Park et al the worldwide production of surimi-related products reached around 800000MT by 2011-2012while the main fish sources for surimi products includePacificwhitingAlaska pollock jackmackerel Atkamackerelsouthern blue whiting northern blue whiting and hoki [3]

Surimi is subdivided into high-grade (FA SA and A) andlow-grade (KA KB and RA) types based on the quality ofthe raw fish sources Most of the high-grade surimi is soldin Japan for the production of kamaboko and other high-quality surimi products and in Korea for the production ofpremium crabsticks Low-grade surimi is sold in Europe andthe United States for the manufacturing of crab sticks andin Korea and Japan for the preparation of other fried fishproducts [3] With the technological advancements in thesurimi processing industry it has been possible to use low-grade surimi for the production of fish cakes fish balls andother surimi products

With increasing demand and new processing techniques(eg the pH-shift method) the use of other seafoodresources such as small pelagic species and giant squid forthe production of surimi and surimi products was possible[212] Notably the production of surimi products is cheaperinKorea than elsewhere but industry professionals are alwayssearching for the most inexpensive surimi seafood sourcesHence the production of surimi from aquaculture fish suchas catfish and carp is growing in demand

Food additives from animal and seafood sources suchas fish chicken beef plasma proteins and egg white areconsidered the most effective protease inhibitors for surimiHowever with the outbreak of avian influenza mad cow dis-ease undesirable resulting characteristics and some religiousconstraints there is limited use of these food additives Addi-tionally vegetarians in some parts of the world would notwish to consume surimi-based products containing additivesderived from animals or even from seafood sources Hencethere is a need to identify more effective and alternative food-grade ingredients (eg plant sources seaweed and microal-gae) to be used in the preparation of fish-paste products

Surimi is mainly used for human consumption As suchthe challenges of production cost composition nutritionalvalue and the shelf-life of surimi products can never beneglected This review has provided an overview of nat-ural and synthetic food additives and preservatives usedto enhance the quality functionality and shelf-life of fish-paste products In addition the improvements in the fish-paste product quality and functionality by various foodadditives from seafood plants mushrooms animal sourcesand functional materials were discussed

For decades surimi and surimi-based products have beenwell known in East Asian countries such as Japan and KoreaHowever with advancements in technology they are attract-ing attention in other Asian as well as European countriesWith the increasing consumption worldwide the manufac-turing and processing of fish-paste products may requirenew and improved additives to enhance their acceptability inthe market Continuous scientific innovations and improvedprocessing technology will aid in further advancements andimprovements in this area

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article and regarding thefunding received

Journal of Food Quality 25

Authorsrsquo Contributions

Khawaja Muhammad Imran Bashir and Jin-Soo Kim con-tributed equally to this work

Acknowledgments

This research was a part of the Project no PJT200885entitled ldquoDevelopment andCommercialization of TraditionalSeafood Products Based on the Korean Coastal MarineResourcesrdquo funded by the Ministry of Oceans and FisheriesSouth Korea

References

[1] H-J Hwang S-Y Choi and S-C Lee ldquoPreparation andquality analysis of sodium-reduced fried fish cakesrdquo PreventiveNutrition and Food Science vol 18 no 3 pp 222ndash225 2013

[2] KFDA Food code Article 1-5-12 Korea Food and Drug Admin-istration Seoul Korea 2012

[3] J W Park H Nozaki T Suzuki and J-L Beliveau ldquoHistoricalreview of surimi technology and market developmentsrdquo inSurimi and Surimi seafood J W Park Ed pp 3ndash24 CRC PressNew York NY USA 2013

[4] J A Ramırez R Dıaz-Sobac O G Morales and M VazquezldquoEvaluation of freeze-dried surimi from tilapia and fat sleeper asemulsifiers [Evaluacion de surimi liofilizado de tilapia y dormi-dor como emulsificantes evaluacion de surimi liofilizado detilapia e dormidor como emulsificantes]rdquo Ciencia y TechnologiaAlimentaria vol 2 no 4 pp 210ndash214 1999

[5] J M Aguilera and D W Stanley ldquoFood structuringrdquo inMicrostructural Principles of Food Processing and Engineeringvol 12 p 246 AN Aspen Publishers Gaithersburg MarylandUSA 1999

[6] A P Stone and D W Stanley ldquoMechanisms of fish muscle gela-tionrdquo Food Research International vol 25 no 5 pp 381ndash3881992

[7] S Nakamura and M Ogawa ldquoBiomolecular strategies forpreparation of high quality surimi-based productsrdquo PreventiveNutrition and Food Science vol 10 no 2 pp 191ndash197 2005

[8] M Okada ldquoHistory of surimi technology in Japanrdquo in Surimitechnology T C Lanier and C M Lee Eds pp 3ndash22 MarcelDekker Inc New York NY USA 1992

[9] MIFAFF ldquoStatistics of fisheries processingrdquo Ministry of FoodAgriculture Forestry and Fisheries Seoul Korea 2011

[10] T C Lanier ldquoMeasurement of surimi composition and junc-tional propertiesrdquo in Surimi technology T C Lanier and C MLee Eds pp 123ndash166 Marcel Dekker Inc New York NY USA1992

[11] K-H Chung and C-M Lee ldquoRelationships between physico-chemical properties of nonfish protein and textural propertiesof protein-incorporated surimi gelrdquo Journal of Food Science vol55 pp 972ndash975 1990

[12] M TMorrissey JWWuD Lin andHAn ldquoProtease inhibitoreffects on torsionmeasurements and autolysis of Pacific whitingsurimirdquo Journal of Food Science vol 58 no 5 pp 1050ndash10541993

[13] J W Park ldquoFunctional protein additives in surimi gelsrdquo Journalof Food Science vol 59 no 3 pp 525ndash527 1994

[14] S Benjakul W Visessanguan and C Srivilai ldquoGel propertiesof bigeye snapper (Priacanthus tayenus) surimi as affected by

setting and porcine plasma proteinsrdquo Journal of Food Qualityvol 24 no 5 pp 453ndash471 2001

[15] D D Hamann P M Amato M C Wu and E A FoegedingldquoInhibition of modori (gel weakening) in surimi by plasmahydrolysate and egg whiterdquo Journal of Food Science vol 55 pp665ndash669 1990

[16] K D Reppond and J K Babbitt ldquoProtease inhibitors affectphysical properties of arrowtooth flounder and walleye pollocksurimirdquo Journal of Food Science vol 58 pp 96ndash98 1993

[17] V C Weerasinghe M T Morrissey and H An ldquoCharacteriza-tion of active components in food-grade proteinase inhibitorsfor surimi manufacturerdquo Journal of Agricultural and FoodChemistry vol 44 no 9 pp 2584ndash2590 1996

[18] C-Y Yang ldquoEffect of the addition of bovine plasma on thequality properties of steamed fish pasterdquo The Korean Journal ofFood and Nutrition vol 21 pp 518ndash523 2008

[19] K Duangmal and A Taluengphol ldquoEffect of protein additivessodium ascorbate and microbial transglutaminase on the tex-ture and colour of red tilapia surimi gelrdquo International Journalof Food Science amp Technology vol 45 no 1 pp 48ndash55 2010

[20] S BenjakulW Visessanguan and C Chantarasuwan ldquoEffect ofporcine plasma protein and setting on gel properties of surimiproduced from fish caught inThailandrdquo LWT- Food Science andTechnology vol 37 no 2 pp 177ndash185 2004

[21] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoCysteine proteinase inhibitor from chicken plasma Fractiona-tion characterization and autolysis inhibition of fish myofibril-lar proteinsrdquo Food Chemistry vol 101 no 4 pp 1647ndash1657 2007

[22] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoEffect of chicken plasma protein and some protein additiveson proteolysis and gel-forming ability of sardine (SardinellaGibbosa) surimirdquo Journal of Food Processing and Preservationvol 31 no 4 pp 492ndash516 2007

[23] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoRheological and textural properties of pacific whiting surimigels as influenced by chicken plasmardquo International Journal ofFood Properties vol 11 no 4 pp 820ndash832 2008

[24] M Sugiyama T Mishiro Y Tsukamasa T Suzuki and KTakama ldquoPuncture properties of kamaboko with ovomucoidpasteurized at several temperaturesrdquo Nippon Suisan Gakkaishivol 64 no 1 pp 76ndash81 1998

[25] M Sugiyama T Mishiro Y Tsukamasa et al ldquoPhysical prop-erties of Kamaboko with ovomucoid pasteurized at severaltemperaturesrdquo Nippon Suisan Gakkaishi vol 64 no 1 pp 82ndash87 1998

[26] J Yongsawatdigul and P Piyadhammaviboon ldquoInhibition ofautolytic activity of lizardfish surimi by proteinase inhibitorsrdquoFood Chemistry vol 87 no 3 pp 447ndash455 2004

[27] L Campo-Deano and C Tovar ldquoThe effect of egg albumen onthe viscoelasticity of crab sticks made from Alaska pollock andPacific whiting surimirdquo Food Hydrocolloids vol 23 no 7 pp1641ndash1646 2009

[28] A Hunt J W Park and A Handa ldquoEffect of various types ofegg white on characteristics and gelation of fish myofibrillarproteinsrdquo Journal of Food Science vol 74 no 9 pp C683ndashC6922009

[29] S Rawdkuen and S Benjakul ldquoWhey protein concentrateAutolysis inhibition and effects on the gel properties of surimiprepared from tropical fishrdquo Food Chemistry vol 106 no 3 pp1077ndash1084 2008

26 Journal of Food Quality

[30] Y Ruttanapornvareesakul K Somjit A Otsuka et al ldquoCry-oprotective effects of shrimp head protein hydrolysate on gelforming ability and protein denaturation of lizardfish surimiduring frozen storagerdquo Fisheries Science vol 72 no 2 pp 421ndash428 2006

[31] D K Li H Lin and SM Kim ldquoEffect of rainbow trout (Oncor-hynchus mykiss) plasma protein on the gelation of Alaska pol-lock (Theragra chalcogramma) surimirdquo Journal of Food Sciencevol 73 no 4 pp C227ndashC234 2008

[32] A Hernandez-Briones G Velazquez M Vazquez and J ARamırez ldquoEffects of adding fish gelatin onAlaska pollock surimigelsrdquo Food Hydrocolloids vol 23 no 8 pp 2446ndash2449 2009

[33] T Yin Z H Reed and J W Park ldquoGelling properties of surimias affected by the particle size of fish bonerdquo LWT- Food Scienceand Technology vol 58 no 2 pp 412ndash416 2014

[34] T Yin and J W Park ldquoTextural and rheological properties ofPacific whiting surimi as affected by nano-scaled fish bone andheating ratesrdquo Food Chemistry vol 180 pp 42ndash47 2015

[35] M R Fowler and J W Park ldquoEffect of salmon plasma proteinon Pacific whiting surimi gelation under various ohmic heatingconditionsrdquo LWT- Food Science and Technology vol 61 no 2pp 309ndash315 2015

[36] M R Fowler and J W Park ldquoSalmon blood plasma Effectiveinhibitor of protease-laden Pacific whiting surimi and salmonmincerdquo Food Chemistry vol 176 pp 448ndash454 2015

[37] S Klomklao S Benjakul H Kishimura K Osako and BK Simpson ldquoTrypsin inhibitor from yellowfin tuna (Thunnusalbacores) roe Effects on gel properties of surimi from bigeyesnapper (Priacanthus macracanthus)rdquo LWT- Food Science andTechnology vol 65 pp 122ndash127 2016

[38] N K Vate and S Benjakul ldquoEffect of the mixtures of squid inktyrosinase and tannic acid on properties of sardine surimi gelrdquoJournal of Food Science and Technology vol 53 no 1 pp 411ndash420 2016

[39] T Yamashita ldquoEffects of commercial soybean protein andwheat gluten as subsidiary materials on physical properties ofkamabokordquo Nippon Shokuhin Kogyo Gakkaishi vol 38 no 12pp 883ndash890 1991

[40] K H Chung and C M Lee ldquoFunction of nonfish proteins insurimi-based gel productsrdquo Korean Journal of Society of FoodScience vol 10 pp 146ndash150 1994

[41] K-H Chung and C-M Lee ldquoEvaluation of wheat gluten andmodified starches for their texture-modifying and freeze-thawstabilizing effects on surimi based-productsrdquo Journal of FoodScience and Nutrition pp 190ndash195 1996

[42] S Benjakul S Karoon and A Suwanno ldquoInhibitory effects oflegume seed extracts on fish proteinasesrdquo Journal of the Scienceof Food and Agriculture vol 79 no 13 pp 1875ndash1881 1999

[43] S Benjakul W Visessanguan and P Thummaratwasik ldquoInhi-bition of gel weakening of threadfin bream surimi using Thailegume seed proteinase inhibitorsrdquo Journal of Food Biochem-istry vol 24 no 5 pp 363ndash380 2000

[44] A Oujifard S Benjakul M Ahmad and J Seyfabadi ldquoEffect ofbambara groundnut protein isolate on autolysis and gel prop-erties of surimi from threadfin bream (Nemipterus bleekeri)rdquoLWT- Food Science and Technology vol 47 no 2 pp 261ndash2662012

[45] Y Luo RKuwaharaMKaneniwa YMurata andMYokoyamaldquoEffect of soy protein isolate on gel properties of Alaska pollockand common carp surimi at different setting conditionsrdquoJournal of the Science of Food and Agriculture vol 84 no 7 pp663ndash671 2004

[46] Y Luo H Shen D Pan and G Bu ldquoGel properties of surimifrom silver carp (Hypophthalmichthys molitrix) as affected byheat treatment and soy protein isolaterdquo Food Hydrocolloids vol22 no 8 pp 1513ndash1519 2008

[47] C Cardoso B Ribeiro and R Mendes ldquoEffects of dietary fibreandmicrobial transglutaminase addition on the rheological andtextural properties of protein gels from different fish speciesrdquoJournal of Food Engineering vol 113 no 4 pp 520ndash526 2012

[48] T Kudre S Benjakul and H Kishimura ldquoEffects of proteinisolates from black bean and mungbean on proteolysis and gelproperties of surimi from sardine (Sardinella albella)rdquo LWT-Food Science and Technology vol 50 no 2 pp 511ndash518 2013

[49] S Klomklao and S Benjakul ldquoEffect of trypsin inhibitor inadzuki bean (Vigna angularis) on proteolysis and gel propertiesof threadfin bream (Nemipterus bleekeri)rdquo LWT- Food Scienceand Technology vol 63 no 2 pp 906ndash911 2015

[50] S Konoo H Ogawa and N Iso ldquoEffects of addition of amyloseand amylopectin on the breaking strength of fish meat gelrdquoNippon Suisan Gakkaishi vol 64 no 1 pp 69ndash75 1998

[51] C-S Kong H Ogawa and N Iso ldquoRheological analysis of theeffect of gelatinization of starch added to fish-meat gel based onvolume changesrdquo Fisheries Science vol 65 no 6 pp 930ndash9361999

[52] B-Y Kim W-W Kim and B Yoo ldquoEffect of native and acety-lated sweet potato starch on rheological properties of compositesurimi solrdquo Journal of Food Science and Nutrition vol 13 no 3pp 245ndash248 2008

[53] B-J Yoo ldquoThe effects of alkaline treatment and potato-starchcontent on the quality of fishmeat paste products prepared fromPacific sandlance Ammodytes personatus Girardrdquo Fisheries andAquatic Sciences vol 14 no 3 pp 161ndash167 2011

[54] S M Cho M S Yoon and S-B Kim ldquoEffects of rice flourmilling types and addition methods on rheological and sensoryproperties of surimi productsrdquo Korean Journal of Fisheries andAquatic Sciences vol 46 no 2 pp 139ndash146 2013

[55] Y-M Kwon and J-S Lee ldquoA study on the quality characteristicsof fish cakes containing rice flourrdquo Korean Journal of HumanEcology vol 22 no 1 pp 189ndash200 2013

[56] M Yoon J-S Kim D Kim J Jo and S Cho ldquoOptimization ofthe processing conditions for the preparation of surimi productscontaining rice flourrdquo Fisheries and Aquatic Sciences vol 17 no2 pp 167ndash173 2014

[57] J A Ramırez M Barrera O G Morales and M VazquezldquoEffect of xanthan and locust bean gums on the gelling prop-erties of myofibrillar proteinrdquo Food Hydrocolloids vol 16 no 1pp 11ndash16 2002

[58] A M Barrera J A Ramırez J J Gonzalez-Cabriales and MVazquez ldquoEffect of pectins on the gelling properties of surimifrom silver carprdquo Food Hydrocolloids vol 16 no 5 pp 441ndash4472002

[59] S Benjakul W Visessanguan S Phatchrat and M TanakaldquoChitosan affects transglutaminase-induced surimi gelationrdquoJournal of Food Biochemistry vol 27 no 1 pp 53ndash66 2003

[60] M A Iglesias-Otero J Borderıas and C A Tovar ldquoUse ofKonjac glucomannan as additive to reinforce the gels from low-quality squid surimirdquo Journal of Food Engineering vol 101 no3 pp 281ndash288 2010

[61] S-H Eom J-A Kim B-Y Son et al ldquoEffects of carrageenanon the gelatinization of salt-based surimi gelsrdquo Fisheries andAquatic Sciences vol 16 no 3 pp 143ndash147 2013

Journal of Food Quality 27

[62] S H Choi and S M Kim ldquoQuality properties of giant squid(Dosidicus gigas) surimi-based product manufactured withAmorphophallus konjac flourrdquo Korean Journal of Food Scienceand Technology vol 44 no 4 pp 422ndash427 2012

[63] D Cando B Herranz A J Borderıas and H M MorenoldquoEffect of high pressure on reduced sodium chloride surimigelsrdquo Food Hydrocolloids vol 51 pp 176ndash187 2015

[64] D-S Kim and Y-H Park ldquoEffect of food humectants onlowering water activity of casing kamaboko 1 Effect of loweringwater activity of sodium chloride sugars and polyolsrdquo Bulletinof the Korean Fisheries Society vol 14 pp 139ndash147 1981

[65] D-S Kim and Y-H Park ldquoEffect of food humectant on lower-ingwater activity of casing kamaboko 2 Effect of loweringwateractivity of starch glycine and sodium lactate and prediction ofthe water activity lowing ability of humectantsrdquo Bulletin of theKorean Fisheries Society vol 15 pp 74ndash82 1982

[66] G L Sanchez Pascua M R Casales and M I Yeannes ldquoInflu-ence of water and glycerol contents on the aw of fish pastesrdquoJournal of Aquatic Food Product Technology vol 10 no 1 pp89ndash100 2001

[67] E Niwa K Tsujimoto and S Kanoh ldquoKamaboko gel-strength-ening effect of polyuronides and other polysaccharidesrdquoNipponSuisan Gakkaishi vol 58 pp 85ndash88 1992

[68] R Yoshinaka M Shiraishi and S Ikeda ldquoEffect of AscorbicAcid on theGel Formation of FishMeatrdquoBulletin of the JapaneseSociety for the Science of Fish vol 38 no 5 pp 511ndash515 1972

[69] H G Lee C M Lee K H Chung and S A Lavey ldquoSodiumascorbate affects surimi gel-forming propertiesrdquo Journal of FoodScience vol 57 pp 1343ndash1347 1992

[70] Y Park S D Kelleher D J McClements and E A DeckerldquoIncorporation and stabilization of omega-3 fatty acids insurimi made from cod Gadus morhuardquo Journal of Agriculturaland Food Chemistry vol 52 no 3 pp 597ndash601 2004

[71] E Okazaki Y Yamashita and Y Omura ldquoEmulsification of fishoil in surimi by high-speed mixing and improvement of gel-forming abilityrdquo Nippon Suisan Gakkaishi vol 68 no 4 pp547ndash553 2002

[72] H Fukushima E Okazaki S Noda and Y Fukuda ldquoChangesin physical properties water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oilrdquoNippon Shokuhin Kagaku Kogaku Kaishi vol 54 no 1 pp 39ndash44 2007

[73] B N Pietrowski R Tahergorabi and J Jaczynski ldquoDynamicrheology and thermal transitions of surimi seafood enhancedwith 120596-3-rich oilsrdquo Food Hydrocolloids vol 27 no 2 pp 384ndash389 2012

[74] A K Balange S Benjakul and S Maqsood ldquoGel strengtheningeffect of wood extract on surimi produced frommackerel storedin icerdquo Journal of Food Science vol 74 no 8 pp C619ndashC6272009

[75] N Buamard and S Benjakul ldquoImprovement of gel properties ofsardine (Sardinella albella) surimi using coconut husk extractsrdquoFood Hydrocolloids vol 51 pp 146ndash155 2015

[76] A K Balange and S Benjakul ldquoEffect of oxidised phenolic com-pounds on the gel property of mackerel (Rastrelliger kanagurta)surimirdquo LWT- Food Science and Technology vol 42 no 6 pp1059ndash1064 2009

[77] A Balange and S Benjakul ldquoEnhancement of gel strength ofbigeye snapper (Priacanthus tayenus) surimi using oxidisedphenolic compoundsrdquo Food Chemistry vol 113 no 1 pp 61ndash702009

[78] Y A Arfat and S Benjakul ldquoEffect of zinc sulphate on gellingproperties of phosphorylated protein isolate from yellow stripetrevallyrdquo Food Chemistry vol 141 no 3 pp 2848ndash2857 2013

[79] M-S Bae and S-C Lee ldquoQuality characteristics of fried fishpaste containing anchovy powderrdquo Journal of the Korean Societyof Food Science and Nutrition vol 36 no 9 pp 1188ndash1192 2007

[80] M-S Bae J-U Ha and S-C Lee ldquoQuality properties of highcalcium fish paste containing anchovyrdquo Korean Journal of Foodand Cookery Science vol 23 pp 561ndash566 2007

[81] H-S Cho and K-H Kim ldquoQuality characteristics of fish pastecontaining skate (Raja kenojei) powderrdquo Journal of the EastAsian Society of Dietary Life vol 21 pp 808ndash813 2011

[82] Y H Park E Y Bum E R Jeon and LH Jung ldquoEffect of addedskate (Raja kenojei) on the quality characteristics of steamedfishmeat pasterdquo Food Science and Biotechnology vol 23 no 5 pp1453ndash1458 2014

[83] S-M Park B-B Lee Y-M Hwang and S-C Lee ldquoQualityproperties of fish paste containing Styela clavardquo Journal of theKorean Society of Food Science and Nutrition vol 35 pp 908ndash911 2006

[84] S-Y Choi E-Y Choi K-E Lee A-S Song S-H Park and S-C Lee ldquoPreparation and quality analysis of fish paste containingStyela clava tunicrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 41 no 11 pp 1591ndash1595 2012

[85] S-M Park H-K Seo and S-C Lee ldquoPreparation and qualityproperties of fish paste containing Styela plicatardquo Journal of theKorean Society of Food and Nutrition vol 35 pp 1256ndash12592006

[86] J-S Seo and H-S Cho ldquoQuality characteristics of fish pastewith shrimp powderrdquo Korean Journal of Food Preservation vol19 pp 519ndash524 2012

[87] H-S Cho and K-H Kim ldquoQuality properties of fish pastecontaining green laver powderrdquo Journal of the Korean Societyof Food Culture vol 29 pp 421ndash427 2014

[88] I-D Park ldquoQuality characteristics of fish paste containingLagocephalus lunaris powderrdquo Journal of the Korean Society ofFood Culture vol 28 pp 657ndash663 2013

[89] I Park ldquoQuality properties of fish paste containingCapsosiphonfulvescens powderrdquo Journal of The Korean Society of FoodCulture vol 31 no 4 pp 357ndash363 2016

[90] B-M Kim J-H Jung M-J Jung D-S Kim J-Y Jun and I-H Jeong ldquoThe quality characteristics and processing of fishpaste containing red snow crabChionoecetes japonicus leg-meatpowderrdquo Korean Journal of Fisheries and Aquatic Sciences vol49 pp 1ndash6 2016

[91] Y-J Shin and G-S Park ldquoQuality characteristics of fish-pastecontaining mulberry leaf powderrdquo Journal of the East AsianSociety of Dietary Life vol 15 pp 738ndash745 2005

[92] Y-J Shin ldquoQuality characteristics of fish paste containing lotus(Nelumbo nucifera) leaf powderrdquo Korean Journal of Food andCookery Science vol 23 pp 947ndash953 2007

[93] A D Thorat V R Joshi A U Pagarkar and A K BalangeldquoMicrowave pasteursation of fish paste product-Kamabokowith Beetroot and Spinachrdquo Ecology Environment and Conser-vation vol 13 no 1 pp 113ndash118 2007

[94] M-O Yang and E-J Cho ldquoQuality properties of surimi withadded citrus fruitsrdquo Journal of East Asian Society of Dietary Lifevol 17 pp 58ndash63 2007

[95] F Alakhrash U Anyanwu and R Tahergorabi ldquoPhysicochemi-cal properties of Alaska pollock (Theragra chalcograma) surimigels with oat branrdquo LWT- Food Science and Technology vol 66pp 41ndash47 2016

28 Journal of Food Quality

[96] J-S Kim and G-I Byun ldquoMaking fish paste with yam (Dios-corea japonica Thumb) powder and its characteristicsrdquo KoreanJournal of Culinary Research vol 15 pp 57ndash69 2009

[97] Y-J Shin J A Lee and G-S Park ldquoa Quality characteristics offish pastes containing Lycii fructus powderrdquo Journal of the EastAsian Society of Dietary Life vol 18 pp 22ndash28 2008

[98] D-W Shim J Jiang J-H Kim et al ldquoEffects of size adjustedwith red ginseng powders on quality of fish pastesrdquo Journal ofthe Korean Society of Food Science and Nutrition vol 41 no 10pp 1448ndash1453 2012

[99] Y-J Shin J A Lee and G-S Park ldquoQuality characteristics offish paste containing Angelicae gigantis Radix powderrdquo KoreanJournal of Food and Cookery Science vol 24 pp 699ndash705 2008

[100] S Choi ldquoQuality characteristics of fish paste containing Cur-cuma longa L powderrdquo The Korean Journal of Food and Nutri-tion vol 25 no 4 pp 833ndash841 2012

[101] J-A Jang H-A Kim and S-K Choi ldquoQuality characteristicsof fish cake made with silver pomfret (Pampus argenteus) withadded wasabi powderrdquo Journal of the East Asian Society ofDietary Life vol 20 pp 103ndash112 2010

[102] Y-J Shin K-S Kim and G-S Park ldquoTexture and sensorycharacteristics of fish paste containing white Poria cocos wolfpowderrdquo Korean J Food Cookery Sci vol 25 pp 119ndash125 2009

[103] J-U Ha S-G Koo H-Y Lee Y-M Hwang and S-C LeeldquoPhysical properties of fish paste containing Agaricus bisporusrdquoKorean Journal of Food Science and Technology vol 33 pp 451ndash454 2001

[104] S-G Koo Y-K Ryu Y-M Hwang J-U Ha and S-C LeeldquoQuality properties of fish-paste containing enoki mushroom(Flammuilna velutipes)rdquo Journal of the Korean Society of FoodScience and Nutrition vol 30 pp 288ndash291 2001

[105] M-H Son S-Y Kim J-U Ha and S-C Lee ldquoTexture prop-erties of surimi gel containing shiitake mushroom (Lentinusedodes)rdquo Journal of the Korean Society of Food Science andNutrition vol 32 pp 859-853 2003

[106] S-Y Kim M-H Son J-U Ha and S-C Lee ldquoPreparationand characterization of fried surimi gel containing king oystermushroom (Pleurotus eryngii)rdquo Journal of the Korean Society ofFood Science and Nutrition vol 32 pp 855ndash858 2003

[107] S I Chung S Y Kim Y J Nam andM Y Kang ldquoDevelopmentof surimi gel from king oyster mushroom and cuttlefish meatpasterdquo Food Science and Biotechnology vol 19 no 1 pp 51ndash562010

[108] S K Jin J H Park and S J Hur ldquoEffect of substituting surimiwith spent laying hen meat on the physicochemical character-istics of fried fish pasterdquo Food and Bioprocess Technology vol 7no 3 pp 901ndash908 2014

[109] A Debusca R Tahergorabi S K Beamer K E Matak and JJaczynski ldquoPhysicochemical properties of surimi gels fortifiedwith dietary fiberrdquo Food Chemistry vol 148 pp 70ndash76 2014

[110] H-S Yook J-W Lee H-J Lee B-S Cha S-Y Lee and M-W Byun ldquoQuality properties of fish paste prepared with refineddietary fiber from ascidian (Halocynthia roretzi) tunicrdquo Journalof the Korean Society of Food Science and Nutrition vol 29 pp642ndash646 2000

[111] A Debusca R Tahergorabi S K Beamer S Partington andJ Jaczynski ldquoInteractions of dietary fibre and omega-3-rich oilwith protein in surimi gels developed with salt substituterdquo FoodChemistry vol 141 no 1 pp 201ndash208 2013

[112] C Sell S Beamer J Jaczynski and K E Matak ldquoSensorycharacteristics and storage quality indicators of surimi franks

nutritionally enhanced with omega-3 rich flaxseed oil andsalmon oilrdquo International Journal of Food Science amp Technologyvol 50 no 1 pp 210ndash217 2015

[113] T Chang C Wang X Wang L Shi H Yang and M CuildquoEffects of soybean oil moisture and setting on the textural andcolor properties of surimi gelsrdquo Journal of Food Quality vol 38no 1 pp 53ndash59 2015

[114] J-S Kim M-L Cho and M-S Heu ldquoQuality improvement ofheat-induced surimi gel using calcium powder of cuttle Sepiaesculenta bone treated with acetic acidrdquo Journal of the KoreanFisheries Society vol 36 pp 198ndash203 2003

[115] G-W Kim G-H Kim J-S Kim et al ldquoQuality characteristicsof fried fish paste of Alaska pollack meat paste added withpropolisrdquo Journal of the Korean Society of Food Science andNutrition vol 37 no 4 pp 485ndash489 2008

[116] G-W Kim G-H Kim J-S Kim et al ldquoQuality of fried fishpaste prepared with sand-lance (Hypoptychus dybowskii) meatand propolis additiverdquo Journal of the Korean Fisheries Societyvol 41 pp 170ndash175 2008

[117] B Park H Cho and S Park ldquoStudy on quality characteristicsof fish paste containing cheonggukjang powderrdquo Journal of TheKorean Society of Food Culture vol 30 no 2 pp 213ndash219 2015

[118] SMiyao T Shindoh KMiyamori and T Arita ldquoEffects of highpressurization on the growth of bacteria derived from surimi(fish paste)rdquo Nippon Shokuhin Kogyo Gakkaishi vol 40 pp478ndash484 1993

[119] A Malicki Z Sysak S Bruzewicz J Zrodłowska-Danek andM Szpak ldquoApplication of high hydrostatic pressure to extendthe shelf-life of traditionally produced fish pasterdquo MedycynaWeterynaryjna vol 66 pp 695ndash698 2010

[120] J-H Kim J-Y Jeon S-R Ryu et al ldquoMicrobial quality andphysiochemical changes of grilled fish paste in a group-mealservice affected by gamma-irradiationrdquo Korean Journal of FoodPreservation vol 11 pp 522ndash529 2004

[121] H-O Cho J-H Kwon M-W Byun and M-K Lee ldquoPreserva-tion of fried fish-paste by Irradiationrdquo Korean Journal of FoodScience and Technology vol 17 pp 474ndash481 1985

[122] H-Y Shin Y-J Lee I-Y Park J-Y Kim S-J Oh and K BSong ldquoEffect of chlorine dioxide treatment onmicrobial growthand qualities of fish paste during storagerdquo Journal of the KoreanSociety for Applied Biological Chemistry vol 50 pp 42ndash47 2007

[123] S S YoonH Kim YM Lee E J Jeong andY J Cha ldquoShelf-lifeextension effects of fish paste product by adding pepper extractrdquoin Proceedings of the Korean Nutrition Society Conference p 216Seoul Korea 2001

[124] E-S Ahn M-S Kim and D-H Shin ldquoScreening of natu-ral antimicrobial edible plant extract for dooboo fish pastemakkoli spoilage microorganismrdquo Korean Journal of FoodScience and Technology vol 26 pp 733ndash739 1994

[125] Y-M Kim B-H Lee S-H Lee I-S Shin and T-S LeeldquoThe preservative effect of egg white lysozyme added surimiproductsrdquo Bulletin of the Korean Fisheries Society vol 21 pp269ndash275 1988

[126] S-H Cho I-S Joo I-W Seo and Z-W Kim ldquoPreservativeeffect of grapefruit seed extract on fish meat productrdquo Journalof Food Hygiene and Safety vol 6 pp 67ndash72 1991

[127] E-T Jeong M-Y Park E-W Lee U-T Park and D-S ChangldquoAntimicrobial characteristics against spoilage microorganismsand food preservative effect of cinnamon (Cinnamomum cassiaBlume) bark extractrdquo Korean Journal of Life Science vol 8 pp648ndash653 1998

Journal of Food Quality 29

[128] D-S Chang H-R Cho H-S Lee M-Y Park and S-M LimldquoDevelopment of alginic acid hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 823ndash826 1998

[129] H-R Cho D-S Chang W-D Lee E-T Jeong and E-WLee ldquoUtilization of chitosan hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 817ndash822 1998

[130] K Yamazaki T Tashiro S Shirahama J-Y Jun and Y KawaildquoGrowth inhibition of spore-forming bacteria in fish-pasteproducts by Nisinrdquo Nippon Shokuhin Kagaku Kogaku Kaishivol 61 no 2 pp 70ndash76 2014

[131] K Hashimoto M L Bari Y Inatsu S Kawamoto and J ShimaldquoBiopreservation of kamaboko (steamed surimi) using pisci-colin KH1 produced by Carnobacteriummaltalomaticum KH1rdquoJapanese Journal of FoodMicrobiology vol 28 pp 193ndash200 2011

[132] S H Lee M S Lee S K Park D H Bae S D Ha and K BSong ldquoPhysical properties of protein films containing green teaextract and its antioxidant effect on fish paste productsrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1063ndash1067 2004

[133] G-O Lim Y-H Hong and K B Song ldquoIncorporating grape-fruit seed extract into Gelidium corneum-whey protein isolateblend packaging film increases the shelf life of fish paste -Research noterdquo Journal of Food Science and Nutrition vol 13no 4 pp 370ndash374 2008

[134] T C Lanier J Yongsawatdigul and P Carvajal-RondanellildquoSurimi gelation chemistryrdquo in Surimi and Surimi Seafood J WPark Ed pp 101ndash139Marcel Dekker NewYork NYUSA 2013

[135] M Kinoshita H Toyohara and Y Shimizu ldquoPurification andproperties of a novel latent proteinase showing myosin heavychain-degrading activity from threadfin-bream musclerdquo TheJournal of Biochemistry vol 107 no 4 pp 587ndash591 1990

[136] D H Wasson J K Babbitt and J S French ldquoCharacterizationof a heat stable protease from arrowtooth flounder Atheresthesstomiasrdquo Journal of Aquatic Food Product Technology vol 1 no3-4 pp 167ndash182 1993

[137] T A Seymour M T Morrissey M Y Peters and H An ldquoPuri-fication and characterization of pacific whiting proteasesrdquoJournal of Agricultural and Food Chemistry vol 42 no 11 pp2421ndash2427 1994

[138] H An V Weerasinghe T A Seymour and M T MorrisseyldquoCathepsin degradation of Pacific whiting surimi proteinrdquoJournal of Food Science vol 59 pp 1013ndash1017 1994

[139] AFDF Ground fish quality chart Alaska fisheries departmentfoundation Anchorage Alaska 1992

[140] G Sylvia S Larkin and M T Morrissey ldquoQuality and resourcemanagement bioeconomic analysis of the Pacific whitingindustryrdquo in Recent Advances inMarine Science and TechnologyO Bellwood H Choat and N Saxena Eds James CookUniversity Townsville QS Australia 1994

[141] S H Choi and S M Kim ldquoDevelopment of giant squid(Ommastrephes bartrami) surimi-based products with gel tex-ture enhancers and the effects of setting on gel qualityrdquo Journalof the Korean Society of Food Science and Nutrition vol 41 no7 pp 975ndash981 2012

[142] J A Ramırez R M Uresti G Velazquez and M VazquezldquoFood hydrocolloids as additives to improve the mechanicaland functional properties of fish products A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1842ndash1852 2011

[143] S-K Kim H-G Byun P-J Park and F Shahidi ldquoAngiotensinI converting enzyme inhibitory peptides purified from bovine

skin gelatin hydrolysaterdquo Journal of Agricultural and FoodChemistry vol 49 no 6 pp 2992ndash2997 2001

[144] I Kimura M Sugimoto K Toyoda N Seki K-I Arai andT Fujita ldquoA study on the cross-links reaction of myosin inkamaboko rsquosuwarirsquo gelsrdquo Nippon Suisan Gakkaisi vol 57 pp1386ndash1396 1991

[145] H An M Y Peters and T A Seymour ldquoRoles of endogenousenzymes in surimi gelationrdquo Trends in Food Science amp Technol-ogy vol 7 no 10 pp 321ndash327 1996

[146] R Nopianti N Huda andN Ismail ldquoA review on the loss of thefunctional properties of proteins during frozen storage and theimprovement of gel-forming properties of Surimirdquo AmericanJournal of Food Technology vol 6 no 1 pp 19ndash30 2011

[147] A M Martın-Sanchez C Navarro J A Perez-Alvarez and VKuri ldquoAlternatives for efficient and sustainable production ofsurimi A reviewrdquo Comprehensive Reviews in Food Science andFood Safety vol 8 no 4 pp 359ndash374 2009

[148] Korea Agro-Fisheries and Food Trade Corporation Processedfood segmented market survey-fish cake market Korea Agro-Fisheries and Food Trade Corporation Seoul Korea 2014

[149] D Kraft and A DerMarderosian The A-Z guide to food asmedicine CRC Press Boca Raton Fla USA 2016

[150] C V Morr and E A Foegeding ldquoComposition and function-ality of commercial whey and milk protein concentrates andisolates a status reportrdquo Food Technology vol 44 pp 100ndash1121990

[151] A Saiga T Okumura T Makihara et al ldquoAngiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chickenbreast muscle extractrdquo Journal of Agricultural and Food Chem-istry vol 51 no 6 pp 1741ndash1745 2003

[152] B Li F Chen X Wang B Ji and Y Wu ldquoIsolation and iden-tification of antioxidative peptides from porcine collagenhydrolysate by consecutive chromatography and electrosprayionization-mass spectrometryrdquo Food Chemistry vol 102 no 4pp 1135ndash1143 2007

[153] A Trampuz R M Prabhu T F Smith and L M BaddourldquoAvian Influenza A New Pandemic Threatrdquo Mayo ClinicProceedings vol 79 no 4 pp 523ndash530 2004

[154] M C Gomez-Guillen B Gimenez M E Lopez-Caballeroand M P Montero ldquoFunctional and bioactive properties ofcollagen and gelatin from alternative sources A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1813ndash1827 2011

[155] D Li X Fu and S M Kim ldquoProduction of chum salmoncystatin from the recombinant Saccharomyces cerevisiae opti-mized using response surface methodologyrdquo Biotechnology andBioprocess Engineering vol 15 no 2 pp 314ndash323 2010

[156] H Akazawa Y Miyauchi K Sakurada H Wasson and K DReppond ldquoEvaluation of protease inhibitors in Pacific whitingsurimirdquo Journal of Aquatic Food Product Technology vol 2 no3 pp 79ndash95 1994

[157] A Hunt K J K Getty and J W Park ldquoRoles of starch in surimiseafood A reviewrdquo Food Reviews International vol 25 no 4 pp299ndash312 2009

[158] T Suzuki Fish and Krill Protein Processing Technology AppliedScience Publishers London UK 1981

[159] C M Lee ldquoSurimi process technologyrdquo Food Technology vol38 pp 69ndash80 1984

[160] M C Wu D D Hamann and T C Lanier ldquoRheological andcalorimetric investigations of starch-fish protein systems duringthermal processingrdquo Journal of Texture Studies vol 16 pp 53ndash74 1985

30 Journal of Food Quality

[161] M C Wu T C Lanier and D D Hamann ldquoRigidity and vis-cosity changes of croaker actomyosin during thermal gelationrdquoJournal of Food Science vol 50 no 1 pp 14ndash19 1985

[162] S-K Kim S-T Yang and E-H Lee ldquoThe starch content of fish-paste products onmarketrdquo Journal of the Korean Society of FoodScience and Nutrition vol 7 pp 41-42 1978

[163] G AMacDonald T C Lanier and P A Caruajal ldquoStabilizationof protein in surimirdquo in Surimi and Surimi Seafood J W ParkEd pp 91ndash125 Marcel Dekker Inc New York NY USA 2000

[164] J A Ramırez I A Santos O G Morales M T Morrisseyand M Vazquez ldquoApplication of microbial transglutaminaseto improve mechanical properties of surimi from silver carputilizacionde transglutaminasa microbiana paramellora-las-propiedades mecanicas de surimide carpaplateada utiliza-cionde transglutaminasamicrobiana paramejorarlaspropieda-des mecanicas de surimide carpaplateadardquo Ciencia y TecnologıaAlimentaria vol 3 no 1 pp 21ndash28 2000

[165] M C Gomez-Guillen A J Borderıas and P MonteroldquoSalt nonmuscle proteins and hydrocolloids affecting rigiditychanges during gelation of giant squid (Dosidicus gigas)rdquoJournal of Agricultural and Food Chemistry vol 45 no 3 pp616ndash621 1997

[166] J W Park ldquoIngredient technology and formulation develop-mentrdquo in Surimi and Surimi Seafood J W Park Ed pp 91ndash125Marcel Dekker Inc New York NY USA 2000

[167] F Garcıa-Ochoa V E Santos J A Casas and E Gomez ldquoXan-than gum production recovery and propertiesrdquo BiotechnologyAdvances vol 18 no 7 pp 549ndash579 2000

[168] A I Rodrıguez-Hernandez and A Tecante ldquoDynamic vis-coelastic behavior of gellan- 120580 -carrageenan and gellan-xanthangelsrdquo Food Hydrocolloids vol 13 no 1 pp 59ndash64 1999

[169] J A Casas and F Garcıa-Ochoa ldquoSophorolipid production byCandida bombicola Medium composition and culture meth-odsrdquo Journal of Bioscience and Bioengineering vol 88 no 5 pp488ndash494 1999

[170] H J Lim ldquoA study on the calcium and sodium intakes andurinary calcium excretion of preschool children in BusanrdquoKorean Journal of Nutrition vol 34 pp 786ndash796 2001

[171] WHO ldquoDiet nutrition and the prevention of chronic diseasesReport of a joint WHOFAO expert consultationrdquo Tech RepWHO World Health Organization Geneva Switzerland 2003

[172] L K Dahl ldquoPossible role of salt intake in the development ofessential hypertensionrdquo International Journal of Epidemiologyvol 34 no 5 pp 967ndash972 2005

[173] H-K Jeong D-S Kim S-J Chun K-S Jo and Y-H ParkldquoEffect of food humectant on lowering water activity of casingKamaboko 3rdquo Bulletin of the Korean Fisheries Society vol 16 pp88ndash96 1983

[174] J Han E Kim M Cheong S Chee and K Chee ldquoBioavailabil-ity and digestibility of organic calcium sources by bone healthindexrdquo Journal of Nutrition and Health vol 43 no 1 pp 12ndash252010

[175] M K Lee ldquoA study of the bio-functional evaluation of Rajaskates caught in Huksando areardquo Journal of the Kwangju HealthCollege vol 21 pp 253ndash265 1996

[176] S H Cho Extraction and characterization of gelatin andantimicrobial peptide from skate (Raja kenojei) skins ChonnamNational University Gwangju Korea 2003

[177] J H Choi ldquoIsolation and purification of in chondroitin sulfatefrom skate cartilagerdquo Tech Rep Pukyong National UniversityBusan Korea 2004

[178] Y G Jo ldquoThe sterol composition of Styela clavardquo Journal of theKorean Fisheries Society vol 11 pp 97ndash101 1978

[179] S H Ahn ldquoExtraction of glycosaminoglycans from Styela clavatunicrdquo Biotechnology and Bioprocess Engineering vol 18 pp180ndash185 2003

[180] J J Kim S J Kim S H Kim H R Park and S C LeeldquoAntioxidant and anticancer activities of extracts from Styelaclava according to the processing methods and solventsrdquoJournal of the Korean Society of Food Science and Nutrition vol35 pp 278ndash283 2006

[181] T Aoki K Takata and N Kunisaki ldquoComparison of nutrientcomponents of six species of wild and cultured fishesrdquo Bulletinof the Japanese Society for the Science of Fish vol 57 pp 1927ndash1934 1991

[182] Committee Donguibogam Translated Donguibogam Bubin-munwha Press Seoul Korea 1999

[183] Y-K Park H-J Kim and M-H Kim ldquoQuality characteristicsof fried fish paste added with ethanol extract of onionrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1049ndash1055 2004

[184] G L Dong J J Hyun and E-R Woo ldquoAntimicrobial prop-erty of (+)-lyoniresinol-3120572-O-120573-D- glucopyranoside isolatedfrom the root bark of Lycium chinense Miller against humanpathogenic microorganismsrdquo Archives of Pharmacal Researchvol 28 no 9 pp 1031ndash1036 2005

[185] C C Wang S C Chang B S Inbaraj and B H ChenldquoIsolation of carotenoids flavonoids and polysaccharides fromLycium barbarum L and evaluation of antioxidant activityrdquoFood Chemistry vol 120 no 1 pp 184ndash192 2010

[186] Z Zhang X Liu T Wu et al ldquoSelective suppression of cervicalcancer Hela cells by 2-O-120573-d- glucopyranosyl-l-ascorbic acidisolated from the fruit of Lycium barbarum Lrdquo Cell Biology andToxicology vol 27 no 2 pp 107ndash121 2011

[187] J S Kil M G Kim H M Choi et al ldquoInhibitory effects ofAngelicae GigantisRadix on osteoclast formationrdquo PhytotherapyResearch vol 22 no 4 pp 472ndash476 2008

[188] ANiranjan andD Prakash ldquoChemical constituents and biolog-ical activities of turmeric (Curcuma longa L) - a reviewrdquo Journalof Food Science and Technology vol 45 pp 109ndash116 2008

[189] K S Kim M G Choung and S H Park ldquoQuantitativedetermination and stability of curcuminoid pigments fromturmeric (Curcuma longaL) rootrdquo Korean Journal of CropScience vol 50 pp 211ndash215 2005

[190] I S Shin and J M Lee ldquoStudy on antimicrobial and antimuta-genic activity of horseradish (Wasabia japonica) root extractsrdquoJournal of the Korean Fisheries Society vol 31 pp 835ndash841 1998

[191] Y J ChoA study on the antioxidative and antimicrobial activitiesof wasabi (Wasabia koreana Cruciferae) extracts [PhD thesis]Sungshin Womens University Seoul Korea 2008

[192] A-S Kang T-S Kang H-R Shon et al ldquoStudies on improve-ment of artificial cultivation and antioxidative activity of Poriacocosrdquo The Korean Journal of Mycology vol 27 pp 378ndash3801999

[193] J-H Lee Y J Lee J-K Shin et al ldquoEffects of triterpenoidsfrom Poria cocos Wolf on the serotonin type 3A receptor-mediated ion current in Xenopus oocytesrdquo European Journal ofPharmacology vol 615 no 1ndash3 pp 27ndash32 2009

[194] K R Im M J Kim T K Jung and K S Yoon ldquoAnalysisof isoflavonoid contents in Astragalus membranaceus Bungecultivated in different areas and at various agesrdquo The KoreanSociety for Biotechnology and Bioengineering vol 25 pp 271ndash276 2010

Journal of Food Quality 31

[195] Y E Lee and S H Hong Oriental Medicine Food MaterialsKyomunsa Seoul Korea 2003

[196] D H Kim ldquoQuality characteristics of fish paste prepared withAstragalus membranaceus powderrdquo Food Engineering Progressvol 15 pp 362ndash369 2011

[197] S-E Kim B S Hwang J-G Song S W Lee I-K Lee andB-S Yun ldquoNew bioactive compounds from Korean nativemushroomsrdquoMycobiology vol 41 no 4 pp 171ndash176 2013

[198] National Institute of Agricultural Science The Mushrooms inKorea Dongbang Media Co Ltd Seoul Korea 2004

[199] Y-J Gao M Zhang and W-P Chen ldquoStudy on processing offish paste with waste of grass carprdquo Journal of Food Science andBiotechnology vol 31 pp 1031ndash1038 2012

[200] S Tolasa C M Lee and S Cakli ldquoPhysical and oxidativestabilization of omega-3 fatty acids in surimi gelsrdquo Journal ofFood Science vol 75 no 3 pp C305ndashC310 2010

[201] B N Pietrowski R Tahergorabi K E Matak J C Tou andJ Jaczynski ldquoChemical properties of surimi seafood nutrifiedwith 120596-3 rich oilsrdquo Food Chemistry vol 129 no 3 pp 912ndash9192011

[202] S H Kim J L Yang and Y S Song ldquoPhysiological function ofcheonggukjangrdquo Food Industry and Nutrition vol 4 pp 40ndash461999

[203] R Walker ldquoToxicology of sorbic acid and sorbatesrdquo Food Addi-tives amp Contaminants Part A vol 7 no 5 pp 671ndash676 1990

[204] B R Thakur and T R Patel ldquoSorbates in fish and fish productsmdasha reviewrdquo Food Reviews International vol 10 no 1 pp 93ndash1071994

[205] C-Y Wang H-W Huang C-P Hsu and B B Yang ldquoRecentadvances in food processing using high hydrostatic pressuretechnologyrdquo Critical Reviews in Food Science and Nutrition vol56 no 4 pp 527ndash540 2016

[206] J H Kwon M W Byun and J S Kim ldquoMicrobiological andorganoleptic qualities of boiled-dried anchovies during post-irradiation periodrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 25 pp 283ndash287 1996

[207] J Noh and J H Kwon ldquoThe quality and thermoluminescenceproperties of dried pollack during storage following irradia-tionrdquo Korean Journal of Food Science and Technology vol 36pp 711ndash716 2004

[208] I Tukenmez M S Ersen A T Bakioglu A Bicer and VPamuk ldquoDose dependent oxidation kinetics of lipids in fish dur-ing irradiation processingrdquo Radiation Physics and Chemistryvol 50 no 4 pp 407ndash414 1997

[209] T Sakai and T Yamaguchi ldquoEffects of yuzu peel addition onthe lipid oxidation in kamaboko Effects of yuzu peel additionon the lipid oxidation in kamabokordquo Bulletin of the Faculty ofAgriculture Miyazaki University vol 57 pp 101-102 2011

[210] E-H Lee K-S Oh J-G Koo H-S Park S-Y Cho and Y-J Cha ldquoStudies on processing and keeping quality of retortpouched foods (3) Preparation and keeping quality of retortpouched fried mackerel meat pasterdquo Bulletin of the KoreanFisheries Society vol 17 pp 373ndash382 1984

[211] J-H Ha E-H Lee J-S Kim S-G Ji and J-G Koo ldquoA study onthe thermal treatment conditions of retort pouched fried fish-paste 1 Influence of thermal treatment conditions on qualityrdquoBulletin of the Korean Fisheries Society vol 20 pp 573ndash581 1987

[212] P Guenneugues and J Ianelli ldquoSurimi resources and marketrdquoin Surimi and surimi seafood J W Park Ed pp 25ndash53 MarcelDekker Inc New York NY USA 2013

Research ArticleDevelopment of a Chemically Defined Medium forBetter Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31

Wenli Liu12 Lanwei Zhang23 and Huaxi Yi3

1College of Chemistry and Environmental Engineering Shenzhen University Shenzhen Guangdong 518060 China2School of Food Science amp Technology Harbin Institute of Technology 73 HuangHe Avenue Harbin Heilongjiang 150090 China3College of Food Science and Engineering Ocean University of China Yushan Road 5 Qingdao Shandong 266100 China

Correspondence should be addressed to Lanwei Zhang zhanglwhiteducn and Huaxi Yi yihxouceducn

Received 31 March 2017 Revised 17 July 2017 Accepted 2 August 2017 Published 6 September 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Wenli Liu et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The macro- and micronutrients in traditional medium such as MRS used for cultivating lactic acid bacteria especially forbacteriocin production have not been defined preventing the quantitative monitoring of metabolic flux during bacteriocinbiosynthesis To enhance Enterocin Y31 production and simplify steps of separation and purification we developed a simplifiedchemically definedmedium (SDM) for the growth of Enterococcus faeciumY31 and production of its bacteriocin Enterocin Y31Wefound that the bacterial growthwas unrelated toEnterocinY31 production inMRS therefore both the growth rate and theEnterocinY31 production were set as the index for investigation Single omission experiments revealed that 5 gL NaCl five vitamins twonucleic acid basesMgSO

4sdot7H2OMnSO

4sdot4H2OKH

2PO4 K2HPO4 CH3COONa fourteen amino acids and glucosewere essential

for the strainrsquos growth and Enterocin Y31 production Thus a novel simplified and defined medium (SDM) was formulated with30 components in total Consequently Enterocin Y31 production yield was higher in SDM as compared to either MRS or CDMSDM improved the Enterocin Y31 production and simplified the steps of purification (only two steps) which has broad potentialapplications

1 Introduction

Bacteriocins are ribosomally synthesised antimicrobial pro-teins or protein complexes that inhibit other bacteria andthey either have a narrow antimicrobial spectrum (againstthe same species) or broad antimicrobial spectrum (againstacross genera) [1 2] Bacteriocin produced by lactic acidbacteria (LAB) is generally regarded as safe (GRAS) andQualified Presumption of Safety (QPS) status [3 4] andit is a desirable trait as a food additive for extending theshelf-life of the fermented food and controlling the safetyof foods [5 6] Based on their molecular structure bac-teriocins can be divided into four groups class I bacte-riocins contain posttranslational modifications (lantibioticsand molecular weight le 5 kDa) class II bacteriocins areunmodified and include small heat-stable nonlanthionine-containing peptides [7] The third class includes large

heat-labile bacteriocins Finally the fourth class comprisescomplex bacteriocins containing a protein moiety with oneor more other lipids or carbohydrates [8] Most bacteriocinsproduced by the Enterococcus faecium group of LAB are classII bacteriocins One subgroup class IIa contains bacteriocinswith certain sequence motifs in their N-terminal halves andis active against the food pathogen Listeria monocytogenes[9] Class IIa bacteriocins have become a focus of researchowing to their low molecular weight good dispersity andhigh thermostability This is also a case of Enterocin Y31produced by E faecium Y31 in the current work [10]

Enterocin Y31 is a class IIa bacteriocin produced byE faecium Y31 [11] Previous research results showed thatEnterocin Y31 had broad spectrum inhibition activity againstBacillus subtilis ATCC 6633 Escherichia coli ATCC 25922Listeria monocytogenes ATCC 19111 Bacillus cereus CICC20463 Staphylococcus aureus and Salmonella enterica serovar

HindawiJournal of Food QualityVolume 2017 Article ID 9017452 8 pageshttpsdoiorg10115520179017452

2 Journal of Food Quality

TyphimuriumATCC 14028The isoelectric point of EnterocinY31 was 825 it was stable in both acidity and alkalescenceconditions hence Enterocin Y31 has a broad applicationprospect (not published) However two main drawbacks ofEnterocin Y31 with regard to application in foods are asfollows (1) bacteriocins are secreted in very small quan-tities in the production media and (2) the media used togrow the bacteriocin-producing strains are very complex[12] as the LAB are fastidious organisms requiring aminoacids B vitamins and various minerals for their growthThese components are normally provided by sources such assoybean meal yeast extract and meat extract All of thesesources contain proteins and peptides as sources of aminoacids which are often very closely related to the bacteriocinproduced Therefore purification of bacteriocin from sucha complex medium requires a series of steps At each stepthere is some loss and sometimes after the final purificationthe antimicrobial activity may be completely lost Complexmedia do not allow the examination of all individual mediumfactors [13 14] affecting bacteriocin production

Ricciardi reported a modified chemically defined med-ium to promote the growth of Lactobacillus casei and Lacto-bacillus plantarum groups [15] In the present study weimproved the chemically defined medium to improve theyield of Enterocin Y31 produced by E faecium Y31 Thereare four objectives of this study (1) to develop a newand improved production method for Enterocin Y31 (pro-duced by E faecium Y31) (2) to determine the macro- andmicronutrients necessary for cultivating E faecium Y31 andimproving Enterocin Y31 production (3) to develop a noveland simple separation and purificationmethod for EnterocinY31 (avoiding a series of chromatography steps and the lossof Enterocin Y31 activity) and (4) to compare Enterocin Y31production in a defined medium with that in a complexmediumThis is feasible using a completely defined mediumand a minimal medium for bacteriocin production can thusbe established

2 Materials and Methods

21 Strains and Growth Conditions The bacteriocin-pro-ducer strain E faecium Y31 isolated from Chinese traditionalfermented foods (fermented vegetable juice from Lanzhou)was previously found to produce class IIa bacteriocin [10]which wasmaintained as stock cultures inMRSmediumwith18 glycerol at minus80∘C

Escherichia coli ATCC 25922 was selected as a sensitivestrain for antimicrobial activity assays because the bacte-riocin produced by E faecium Y31 has the highest activityagainst E coli ATCC 25922 in gram-negative bacteria

22 Medium The growth of E faecium Y31 and productionof Enterocin Y31 in a defined medium in a fermenter werecompared with those in MRS (reference medium) used forthe optimisation of the growth of E faecium Y31 and theproduction of Enterocin Y31 This medium CDM consistedof 44 components described by Khan et al [12] (listed inTable 1) All chemicals used for the preparation of the definedmedium were of analytical grade and obtained from either

Sigma-Aldrich (St Louis MO USA) or BDH ChemicalsLtd (Poole UK) For all the experiments aqueous stocksolutions of the individual components were prepared inthe appropriate concentrations and sterilized by autoclav-ing with the exception of the heat-sensitive componentsThe heat-sensitive amino acids (asparagine glutamine andtryptophan) all of the B vitamins and FeSO

4were filter-

sterilized (pore size 022120583m membrane Millipore CorpBillerica MA USA) All the stock solutions were then storedat 4∘C except FeSO

4which was freshly prepared before each

experiment because it is prone to oxidation during storage Inaddition to the defined medium MRS medium was used asa reference for comparison with the defined medium beforeeach experiment

23 Determination of the Antimicrobial Activity of EnterocinY31 The antimicrobial activity of bacteriocin was monitoredusing the agar well diffusion assay (AWDA) as describedpreviously [16] with some modifications E faecium Y31 wascultured for two or three generations and then the cell-free supernatants (CFSs) of E faecium Y31 were preparedby centrifuging for 30min at 10000timesg Aliquots (80 120583L) ofthe cell-free supernatants (CFSs) of E faecium Y31 wereadded to the wells (6mm diameter) on double-layer agarplates previously inoculated with 02mL overnight cultureof the indicator strain E coli ATCC 25922 Plates were keptstatic at room temperature for 3 h to allow diffusion of theCFSs evenly in the agar and then the plates were incubatedfor 24 h at 37∘C The bacteriocin titre was determined byeliminating the effect of the organic acid eliminating theeffect of H

2O2 and protease verificationThe diameter of the

zone of inhibition (not including the wells) was measuredusing a Vernier caliper An arbitrary unit (AUmL) wasdefined as the reciprocal of the highest dilution that producedan inhibition zone Specific activity was expressed as that unitper milligram of protein

24 Protein Concentration Determination Protein concen-tration was determined by the BCA (bicinchoninic acid)microassay method (Pierce Rockford IL USA) [17]

25 Monitoring of the Growth of E faecium Y31 The ODvalue of the fermentation liquid of E faecium Y31 wasmonitored with UV spectrophotometry at 600 nm each hourSterile culture medium was used as blanks to subtract thebackground value Samples having an OD600 nm value ofmore than 07 were diluted with the sterile culture mediumand the corrected OD value was obtained by multiplying thedilution factor ODmax (600 nm) represents the maximumOD value of the growth of E faecium Y31 ODmax (600 nm)was calculated before any centrifugation

26 Determination of the Relative Growth Rate The relativegrowth rate was calculated according to Monod [18] Thefollowing equation was used to calculate the growth rate

120583 = [(lnOD2minus lnOD

1) divide (1199052minus 1199051)] divide 120583CDM (1)

where 120583 is the relative growth rate (hminus1) ln is the symbol fornatural logarithm and OD

1and OD

2are the corrected OD

Journal of Food Quality 3

Table 1 Composition of CDM and SDMmedium

Constituent ContentCDM SDM

Amino acids (g Lminus1)L-Asparagine 100 100L-Aspartic acid 100 mdashL-Glutamic acid 100 100L -Glutamine 100 mdashL-Cys 100 100L-Alanine 100 mdashL-Arginine 100 100Glycine 100 100L-Histidine 100 100L-Isoleucine 100 100L-Leucine 100 100L-Lysine 100 100L-Methionine 100 100L-Phenylalanine 100 100L-Proline 100 mdashL-Serine 100 100L-Threonine 100 100L-Tryptophan 100 100L-Tyrosine 100 mdashL-Valine 100 mdash

Nucleic acid bases (g Lminus1)AdemomeSO

4002 002

Guanine 002 mdashInosine 002 mdashXanthine 002 mdashUracil 002 002Thymine 002 mdashOrotic acid 002 mdash

B vitamins (mgsdotLminus1)Biotin 2000 2000Para-aminobenzoic acid 1000 mdashNicotinic acid 200 200Ca-pantothenic acid 2000 2000Riboflavin 200 200Folic acid 200 200Cyanocobalamin 200 mdashThiamine 1000 mdashPyridoxal 2000 mdash

Minerals (gsdotLminus1)Manganese sulfate 005 005Magnesium sulfate 01 010Ferrous sulfate7H

2O 002 mdash

CaCl2

mdash mdashSodium citrate 500 500Potassium dihydrogen phosphate 200 200Dipotassium hydrogen phosphate 700 700

Table 1 Continued

Constituent ContentCDM SDM

Carbon source (gsdotLminus1)Glucose 1500 1500

Others (gsdotLminus1)Tween 80 100 100Glycerol mdash mdashNaCl mdash 500

27 Effects of NaCl CaCl2 and Glycerol on the Growth of Efaecium Y31 and Enterocin Y31 Production To determine theeffects of these components 5 gL 10 gL 15 gL and 20 gLNaCl 10 gL CaCl

2 and 50 gL glycerol were individually

added to 1000mLCDM andCDMmediumwith no addtionswas used as a control wherein the inoculum size was 2fermentation temperature was 37∘C and inoculum time was24 h The culturing liquid was then centrifuged for 20minat 10000timesg and then the CFSs were used to determineEnterocin Y31 activity and ODmax (24 h)

28 Effects of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth ofE faecium Y31 and Enterocin Y31 Production According tothe Leave One Out (LOO) technique each amino acid Bvitamin mineral and nucleic acid base was sequentially andindividually omitted from 1000mLCDMmedium andCDMwithout additions was used as a control The inoculum sizewas 2 fermentation temperature was 37∘C and inoculationtime was 24 h The culture liquid was then centrifugedfor 20min at 10000timesg and then the CFSs were used todetermine Enterocin Y31 activity and ODmax (24 h)

The following terms were used to describe the rela-tionship between each medium component and growth asdetermined by the single omission technique A constituentwas considered essential if its omission resulted in less thanhalf the maximum strain growth rate and production ofbacteriocin of the positive control stimulatory when itsabsence resulted in the fact that the growth rate and thebacteriocin production was between 50 and 80 of thatobserved in complete CDM and nonessential if the growthrate and Enterocin Y31 production was 80 (or more) of thatobtained in the complete CDM

29 Purification of Enterocin Y31 E faecium Y31 was allowedto grow in the SDM (Table 1) for 24 h The cells were thenremoved by centrifugation (11800timesg 25min) The CFSswere then filtered through a 022 120583m filter (low-protein-binding HVLP filter Millipore Corp) to remove any remain-ing cells These filtered CFSs were referred to as crude bacte-riocin The crude bacteriocin was subjected to ultrafiltrationof 1 kDa and 30 kDa The retentate from the 1 kDa step wasthen subjected to Tricine-SDS-PAGE

210 Statistical Analyses All experiments were preformedseparately three times and mean plusmn standard deviation (SD)values were calculated from triplicate determinations All

4 Journal of Food Quality

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 320002

0604

081012141618202224

ODpHInhibition zone diameter (mm)

Time (h)

OD

35404550556065707580

pH

0

2

4

6

8

10

12

14

Inhi

bitio

n zo

ne (

mm

)

Figure 1 Relationship between the growth of the bacteriocinogenicstrain and Enterocin Y31 production

data were subjected to one-way analysis of variance (one-way ANOVA) Comparison of means was performed withDuncanrsquos multiple range tests Statistical significance was setat 119875 lt 005

3 Results and Discussion

31 Relationship between the Growth of the Strain andEnterocin Y31 Activity The growth of E faecium Y31 wasunrelated to EnterocinY31 activity inMRSmedium as shownin Figure 1 The result was consistent with the result ofBacterocin J23 produced by Lactobacillus paracasei J23 asdescribed by Huaxi Yi in our research group (not published)whichwas inconsistentwith the result of Salivaricin producedby L salivarius CRL 1328 [19] thus the growth rate of EfaeciumY31 and Enterocin Y31 activity were used as detectionindexes for developing a novel chemical defined mediumEnterocin Y31 activity could be detected at the exponentialphase of the producing strain (9 h) and reached its highestvalue of 1126 plusmn 036mm at stationary phase of producingstrain (24 h) ODmax remained stable at 16 h of fermentationof strain Y31 thus ODmax (16 h) was used as an index of thestrain growth status

32 Effect of NaCl Concentration on the Growth of E faeciumY31 and Enterocin Y31 Production Theeffect of NaCl at 5 gL10 gL 15 gL and 20 gL was determined in CDMwith CDMwith no additives as the control The results indicated thatthe growth of E faecium Y31 and production of EnterocinY31 were not significant difference when adding 5 gL or10 gL NaCl and 0 gL and 15 gL NaCl had no effect onthe growth of strain Y31 and production of Enterocin Y31When the concentration of NaCl was 20 the growth of Efaecium Y31 and production of Enterocin Y31 reduced whichshowed the significant difference when compared to 0 gLand 15 gL NaCl We can conclude that 20 gL NaCl have anegative effect on the growth of strain Y31 and the productionof Enterocin Y31 When the adding concentration of NaClwas 5 gL the ODmax (16 h) of E faecium Y31 was highest

150

155

160

165

170

175

180

Enterocin Y31 production (AUmg protein)

CDM

(con

trol)

bc c

bc

ab

a

b b bab

a

GR

(16B

)

ODmax (16 B)

10A

L N

aCl

15A

L N

aCl

20A

L N

aCl

5A

L N

aCl 0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 2 Effect of NaCl concentration on the growth of Enterococ-cus faecium Y31 and Enterocin Y31 production Means not sharing acommon superscript letter are significantly different fromeach other(119875 lt 005)

172 plusmn 001 and the antibacterial activity also reached themaximum value 128364 plusmn 4140AUmg protein Based thesignificant difference analysis we could conclude that 5 gLNaCl stimulated the growth of strain Y31 (119875 lt 005) andhad no effect on the production of Enterocin Y31 (Figure 2)Similar results have been reported in a study of nutritionalrequirements of L salivarius CRL 1328 producing Salivaricin[19] Considering that the condition for the growth of Efaecium Y31 was crucial 5 gL NaCl was added to the novelchemically defined medium SDM (the medium ingredientsof SDM were listed in Table 1)

33 Effect of CaCl2 and Glycerol on the Growth of E faeciumY31 and Enterocin Y31 Production The results shown inTable 2 indicated that adding 10 gL CaCl

2to CDM had no

effect on the growth of E faecium Y31 but had a negativeeffect on the production of Enterocin Y31 (119875 lt 005) whereasadding 50 gL glycerol had a slight negative effect on thegrowth of E faecium Y31 (119875 lt 005) and a negative influenceon Enterocin Y31 production (119875 lt 005)

34 Effect of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth of Efaecium Y31 and Enterocin Y31 Production According to theLeaveOneOut (LOO) technique each amino acid B vitaminmineral and nucleic acid base was sequentially omitted ina series of prepared formulations along with CDM as acontrol The results shown in Table 3 indicated that L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser and L-Cys areessential amino acids which had an effect on the growth ofE faecium Y31 and Enterocin Y31 production and the stim-ulatory amino acids mainly included L-Asn L-Glu L-Iso L-Lys and L-Try Omitting the stimulatory amino acids resultedin the slow growth of E faecium Y31 and low production

Journal of Food Quality 5

Table 2 Effects of CaCl2and glycerol on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Added components ODmax (600 nm) after 16 h Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003b 124224 plusmn 4141c

10 gL CaCl2

170 plusmn 002b 28986 plusmn 4141a

50 gL glycerol 153 plusmn 003a 56591 plusmn 4181b

Note CDM is explained in Table 1 and means in the same row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

Table 3 Effect of omitting a single amino acid on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Omitted amino acid ODmax (16 h) Relative growth rate Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003h 100 124224 plusmn 4141cd

L-Ala 150 plusmn 005g 90 122843 plusmn 6325cd

L-Arg 076 plusmn 002c ng mdasha

L-Asp 143 plusmn 004g 93 117322 plusmn 6325cd

L-Asn 091 plusmn 003d 60 122843 plusmn 8225cd

L-Cys 100 plusmn 004de 44 mdasha

L-Glu 152 plusmn 004g 72 110420 plusmn 2391c

L-Gln 171 plusmn 004h 84 124224 plusmn 5686d

L-Gly 061 plusmn 003ab ng mdasha

L-His 066 plusmn 003bc ng mdasha

L-Iso 106 plusmn 004ef 79 66252 plusmn 8251b

L-Leu 071 plusmn 003bc ng mdasha

L-Lys 116 plusmn 004f 80 62111 plusmn 4140b

L-Met 053 plusmn 002a ng mdasha

L-Phe 077 plusmn 002c ng mdasha

L-Pro 181 plusmn 003h 71 110420 plusmn 6545cd

L-Ser 049 plusmn 003a ng mdasha

L-Thr 068 plusmn 002bc ng mdasha

L-Try 112 plusmn 003ef 80 57322 plusmn 2391b

L-Tyr 170 plusmn 007h 100 120082 plusmn 3487cd

L-Val 196 plusmn 008i 98 122843 plusmn 6582cd

Note ldquongrdquo represents that the strain did not grow and ldquomdashrdquo represents that there was no inhibition activity CDM is explained in Table 1 and means in thesame row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

of Enterocin Y31 Therefore the essential amino acids andstimulatory amino acids were included in the SDM (listedin Table 1) A previous study reported the similar results asZhang et al found that six amino acids (arginine histidineisoleucine leucine methionine and valine) were necessaryfor the lactococci enterococci and streptococci [20]

Pyridoxal and pantothenic acid are essential B vitaminswhich had an effect on the growth of E faeciumY31 and Ente-rocin Y31 production and the stimulatory B vitamins mainlyincluded niacin and riboflavin Wherein the stimulatory Bvitamins could not result in the growth arrest of E faeciumY31 and the biosynthesis arrest of Enterocin Y31 they couldcause low growth rate and low biosynthesis volume There-fore the essential and stimulatory B vitamins were neededin the SDM Omitting folic acid would cause a reduction of80 in the ODmax (16 h) of E faecium Y31 therefore folicacid is also needed for the growth of E faecium Y31 and theproduction of Enterocin Y31 (Figure 3) It has been reported

that nutritional requirements of L delbrueckii ssp lactis CRL581 growthwere nicotinic acid and pyridoxal and pantothenicacid whereas the growth of L delbrueckii ssp lactis CRL654 requires niacin and pantothenic acid and riboflavinand cyanocobalamin were found to be stimulatory for bothstrains [21] Research results about S thermophilus strains(ST1 ST7 ST8 ST11 ST18 and ST21) indicated that riboflavinwas essential for the growth of all strains whereas Ca-pantothenic acid and nicotinic acid were also required [22]

In the present study MgSO4sdot7H2O was an essential min-

eral andMnSO4sdot4H2OKH

2PO4 K

2HPO4 andCH

3COONa

were stimulatory minerals which had an effect on the growthof E faecium Y31 and Enterocin Y31 production (Figure 4)The necessity of magnesium and phosphate has previouslybeen reported by other researchers for various LAB species[20 23 24]

Adenine and uracil are stimulatory nucleic acids whichhad an effect on the growth of E faecium Y31 and Enterocin

6 Journal of Food Quality

Non

e (CD

M)

Pyrid

oxal

Thia

min

e

Nia

cin

D-B

iotin

Ribo

flavi

n

Cyan

ocob

alam

in

Folic

acid

p-A

min

oben

zoic

acid

Pant

othe

nic a

cid

02040608101214161820

Omitted vitamins

f

b

f

c

f

d

e ef

a

d

b

d

b

ccd

cdcd

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 3 Effect of individually omitting each B vitamin on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Y31 production (Figure 5) No nucleic acid was essential forthe growth of E faecium Y31 and Enterocin Y31 production

35 Comparison of Enterocin Y31 Production onMRSMediumand SDM A novel chemical defined medium (SDM) wasdeveloped (Table 1 and Figures 3 4 and 5) and SDMcontainedNaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

and uracil Strain Y31 grew better on SDM than on MRSmedium (Figure 6) As shown in Figure 7 Enterocin Y31production on SDM was 16 times than that on MRS

36 Purification and Characterization of Enterocin Y31 Afterthe removal of cells from the defined medium the cell-free supernatant was subjected to ultrafiltration through a30 kDa ultrafiltration membrane The active permeate liquorwas then subjected to a second ultrafiltration step using a1 kDa NMWL The antimicrobial activity was again foundin the retentate (10240AUL) Enterocin Y31 was purified byTricine-SDS-PAGE and its molecular weight was 674 kDa(showed in Figure 8)

4 Conclusion

When culturing E faecium Y31 using novel chemical definedmedium (SDM) Enterocin Y31 production increased 16times than that on MRS The ingredients were composedof NaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-ThrL-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

Non

e (CD

M)

Am

mon

ium

citr

ate d

ibas

ic

MnS

O4 middot 4

H2O

MgS

O4 middot 7

H2O

KH2P

O4

K2H

PO4

Sodi

um ac

etat

e

0204060810121416182022

Omitted minerals

d d

b

a

b

c ce e

b

a

c

d d

Enterocin Y31 production (AUmg protein)$

GR

(16B

)$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

Figure 4 Effect of individually omitting each a mineral on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Non

e (CD

M)

Aden

ine

Gua

nine

Inos

ine

Xant

hine

Oro

tic ac

id

Ura

cil

Thym

ine

14

15

16

17

18

19

20

Omitted nucleic acid bases

d

a

c

d d d

b

d

d

abbc

d d d

a

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

Figure 5 Effect of individually omitting each a nucleic acid baseon the growth of Enterococcus faecium Y31 and Enterocin Y31production Means not sharing a common superscript letter aresignificantly different from each other (119875 lt 005)

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

uracil and glucose which were the macro- and micronu-trients needed by biosynthesis of Enterocin Y31 SDM washelpful to the growth of E faecium Y31 and EnterocinY31 production improvement In addition SDM avoided aseries of chromatography steps and the loss of Enterocin Y31

Journal of Food Quality 7

0 5 10 15 20 25 30 3500020406081012141618202224

Time (h)

SDMMRS

GR

(16B

)

Figure 6 Growth of Enterococcus faecium Y31 on MRS and SDM

0 5 10 15 20 25 30 3502468

10121416182022

Time (h)

Inhi

bitio

n zo

ne d

iam

eter

(mm

)

SDMMRS

Figure 7 Enterocin Y31 productions on MRS and SDM

Enterocin Y31

M 140 +$

30+$

20 +$

10 +$

46 +$

17 +$

Figure 8 Tricine-SDS-PAGE of Enterocin Y31 M protein marker1 Enterocin Y31

activity only two steps of ultrafiltration and Tricine-SDS-PAGE were needed to separate and purify Enterocin Y31Therefore chemically defined medium has better potentialfor improving the bacteriocin production and reducing thesteps of separation and purification Chemically definedmedia is useful for purification of not only large bacteriocinssuch as Enterocin Y31 but also small peptide bacteriocinsThe alternative use of a chemically defined medium meetsthe nutritional requirements of strains producing bacteri-ocins and therefore is an excellent alternative to reduce theload of contaminating peptides from the medium therebydecreasing the purification steps To our knowledge no suchstudies have been conducted to improve class IIa bacteriocinEnterocin Y31 production and purify Enterocin Y31

Ethical Approval

This study complies with the research ethics guidelines and itdoes not contain any studies with human or animal subjects

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article

Acknowledgments

This work was financially supported by the 60th Finan-cial Grant from China Postdoctoral Science Foundation(Grant no 2016M602534) the Youth Innovation TalentsProject of General Higher School in Guangdong Province(2016KQNCX144) and theNationalNatural Science Founda-tion of China (Grants nos 31571850 31771988 and 31701621)

References

[1] R C R Martinez M Wachsman N I Torres J G LeBlancS D Todorov and B D G D M Franco ldquoBiochemical anti-microbial and molecular characterization of a noncytotoxicbacteriocin produced by Lactobacillus plantarum ST71KSrdquo FoodMicrobiology vol 34 no 2 pp 376ndash381 2013

[2] I M Aasen T Moslashretroslash T Katla L Axelsson and I StorroslashldquoInfluence of complex nutrients temperature and pH on bacte-riocin production by Lactobacillus sakei CCUG 42687rdquo AppliedMicrobiology andBiotechnology vol 53 no 2 pp 159ndash166 2000

[3] P Alvarez-Sieiro M Montalban-Lopez D Mu and O PKuipers ldquoBacteriocins of lactic acid bacteria extending thefamilyrdquo Applied microbiology and biotechnology vol 100 no 7pp 2939ndash2951 2016

[4] F A C Martinez E M Balciunas A Converti P D Cotterand R P De Souza Oliveira ldquoBacteriocin production by Bifido-bacterium spp A reviewrdquo Biotechnology Advances vol 31 no 4pp 482ndash488 2013

[5] E F OrsquoShea P D Cotter R P Ross and C Hill ldquoStrategiesto improve the bacteriocin protection provided by lactic acidbacteriardquo Current Opinion in Biotechnology vol 24 no 2 pp130ndash134 2013

[6] A-M Zouhir E Kheadr I Tahiri J Ben Hamida and IFliss ldquoCombination with plant extracts improves the inhibitoryaction of divergicin m35 against Listeria monocytogenesrdquo Jour-nal of Food Quality vol 31 no 1 pp 13ndash33 2008

8 Journal of Food Quality

[7] J Pei Y Yuan and T Yue ldquoPrimary characterization of bacteri-ocin paracin C - A novel bacteriocin produced by Lactobacillusparacaseirdquo Food Control vol 34 no 1 pp 168ndash176 2013

[8] D Drider and S Rebuffat ldquoClassification of Bacteriocins fromGram-Positive Bacteriardquo in Prokaryotic Antimicrobial Peptidespp 29ndash53 Springer New York NY USA 2011

[9] T Aymerich H Holo L S Havarstein M Hugas M Garrigaand I F Nes ldquoBiochemical and genetic characterization of ente-rocin A from Enterococcus faecium a new antilisterial bac-teriocin in the pediocin family of bacteriocinsrdquo Applied andEnvironmental Microbiology vol 62 no 5 pp 1676ndash1682 1996

[10] W Liu L Zhang H Yi et al ldquoQualitative detection of class IIabacteriocinogenic lactic acid bacteria from traditional Chinesefermented food using a YGNGV-motif-based assayrdquo Journal ofMicrobiological Methods vol 100 no 1 pp 121ndash127 2014

[11] W Liu L Zhang J Shi et al ldquoAssessment of the safety and appli-cations of bacteriocinogenic Enterococcus faecium Y31 as anadjunct culture in North-eastern Chinese traditional fermen-tation paocairdquo Food Control vol 50 pp 637ndash644 2015

[12] H Khan S H Flint and P-L Yu ldquoDevelopment of a chemicallydefined medium for the production of enterolysin A fromEnterococcus faecalis B9510rdquo Journal of Applied Microbiologyvol 114 no 4 pp 1092ndash1102 2013

[13] M Silva d M Andrade d S A Bauermeister et al ldquoA SimpleDefined Medium for the Production of True Diketopiperazinesin Xylella Fastidiosa and Their Identification by Ultra-FastLiquidChromatography-Electrospray Ionization IonTrapMassSpectrometryrdquoMolecules vol 22 no 6 p 985 2017

[14] E Texeira J Checa A Rıal et al ldquoA New Chemically DefinedMedium for Cultivation of Streptococcus Pneumoniae SerotyperdquoJournal of Biotech Research vol 6 p 54 2015

[15] A Ricciardi R G Ianniello E Parente and T Zotta ldquoModifiedchemically definedmedium for enhanced respiratory growth ofLactobacillus casei and Lactobacillus plantarum groupsrdquo Journalof Applied Microbiology vol 119 no 3 pp 776ndash785 2015

[16] U Schillinger and K Lucke F ldquoAntibacterial activity of Lacto-bacillus sake isolated from meatrdquo Applied and EnvironmentalMicrobiology vol 55 no 8 pp 1901ndash1906 1989

[17] P K Smith R I Krohn G Hermanson et al ldquoMeasurement ofprotein using bicinchoninic acidrdquo Analytical biochemistry vol150 no 1 pp 76ndash85 1985

[18] J Monod ldquoThe Growth of Bacterial Culturesrdquo Annual Reviewsin Microbiology vol 3 no 1 pp 371ndash394 1949

[19] E V Pingitore EMHebert F Sesma andM E Nader-MacıasldquoInfluence of vitamins and osmolites on growth and bacteriocinproduction by Lactobacillus salivarius CRL 1328 in a chemicallydefinedmediumrdquoCanadian Journal of Microbiology vol 55 no3 pp 304ndash310 2009

[20] G Zhang D AMills and D E Block ldquoDevelopment of chemi-cally defined media supporting high-cell-density growth ofLactococci Enterococci and Streptococcirdquo Applied and Environ-mental Microbiology vol 75 no 4 pp 1080ndash1087 2009

[21] E M Hebert R R Raya and G S De Giori ldquoNutritionalrequirements of Lactobacillus delbrueckii subsp lactis in achemically defined mediumrdquo Current Microbiology vol 49 no5 pp 341ndash345 2004

[22] C Letort and V Juillard ldquoDevelopment of a minimal chemi-cally-defined medium for the exponential growth of Streptococ-cus thermophilusrdquo Journal of AppliedMicrobiology vol 91 no 6pp 1023ndash1029 2001

[23] N Terrade and R Mira de Orduna ldquoDetermination of theessential nutrient requirements of wine-related bacteria fromthe genera Oenococcus and Lactobacillusrdquo International Journalof Food Microbiology vol 133 no 1-2 pp 8ndash13 2009

[24] F M Saguir and M C M De Nadra ldquoImprovement of a chem-ically definedmedium for the sustained growth of Lactobacillusplantarum nutritional requirementsrdquo Current Microbiologyvol 54 no 6 pp 414ndash418 2007

Research ArticleLipid Oxidation Color Changes and MicrobiologicalQuality of Frozen Beef Burgers Incorporated with ShiraziThyme Cinnamon and Rosemary Extracts

Hadi Hashemi Gahruie Seyed Mohammad HashemHosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan Shad

Department of Food Science and Technology School of Agriculture Shiraz University Shiraz Iran

Correspondence should be addressed to Mohammad Hadi Eskandari eskandarshirazuacir

Received 3 January 2017 Revised 17 March 2017 Accepted 11 April 2017 Published 21 May 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Hadi Hashemi Gahruie et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In this study the oxidative stability of beef burgers incorporated with Shirazi thyme cinnamon and rosemary extracts wascompared with that of BHT-incorporated and antioxidant-free samples The chemical composition TBARS metmyoglobin pHcolor and microbial and sensory characteristics were evaluated during storage at minus18∘C for 2 months The results indicated thatShirazi thyme and cinnamon extracts did not change the colorimetric properties significantly (119875 lt 005) Incorporating naturalantioxidants led to a significant (119875 lt 005) reduction in TBARS (3658ndash4634) and metmyoglobin (1625ndash1847) as compared tocontrol Except for the control sample total microbial counts of burgers were lower than the maximum allowed limit Burgersformulated with Shirazi thyme revealed the lowest amount of total count Regarding the sensory characteristics the overallacceptability of different samples decreased in the order of cinnamon gt BHT gt Shirazi thyme gt rosemary gt control Finally theresults showed that these plant extracts can be utilized as an alternative to synthetic antioxidants in formulation of burgers

1 Introduction

Meat and meat products are among the most importantprotein sources in the daily diet of people living in developedcountries Beef burger is almost the most popular meatproduct consumed by millions of people from all over theworld The common processes (such as mincing cookingand salt addition) applied in the production of burgersenhance the formation of reactive oxygen species thereforethe resultant product is highly vulnerable to oxidation [1]Lipid and protein oxidations have been reported as theprincipal reason for the decreased quality of burgers duringstorage resulting in decreasing the shelf life [2ndash4]

Application of antioxidants is the best strategy to pre-vent oxidation reactions [5] Synthetic antioxidants such asBHT TBHQ and BHA have various adverse human healtheffects including allergy headache asthma and dermatitis

Therefore the application of natural antioxidants (such asherbal essential oils and extracts) is of interest and canbe observed in a growing number of research works [6ndash8](Aliakbarlu et al 2016)Moreover consumers are increasinglydemanding for green-labeled food products such as thosecontaining natural antioxidant Natural compounds can beobtained from natural sources such as plants fruits vegeta-bles oil seeds spices team honey bee pollen and cereals[9] A lot of extracts have been approved as GRAS (GenerallyRecognized as Safe) that is the addition of these chemicals orsubstances into food is considered safe by experts and theirapplication is exempted from the usual Federal Food Drugand Cosmetic Act (FFDCA) [10]

The potential of natural antioxidants in preventing thelipid oxidation in different food products has been evaluatedby many researchers around the world [11] It has beenreported that the extracts of kinnow rind pomegranate rind

HindawiJournal of Food QualityVolume 2017 Article ID 6350156 9 pageshttpsdoiorg10115520176350156

2 Journal of Food Quality

Hamburger ingredients Extracts (20 g herb + 500 ml water)

Preparation of base batter

Formula 1without additives

(control)

Formula 2with BHT(100 ppm)

Formula 3with Shirazi thyme

(22 mlkg)

Formula 4with rosemary

(28 mlkg)

Formula 5with cinnamon

(73 mlkg)

Analysis (0 15 30 45 and 60 days)

Chemical analysis

Chemical compotation(i) Moisture

(ii) Protein(iii) Fat(iv) Carbohydrate(v) Ash

Deterioration criteria(i) TBARS

(ii) pH(iii) Metmyoglobin

Microbiological analysis(i) Total aerobic bacterial count

Sensory analysis(i) Appearance

(ii) Texture(iii) Taste(iv) Odor(v) Overall acceptance

Color analysis(i) Llowast

(ii) alowast

(iii) blowast

(iv) ΔE

Production and storage at minus18∘C

Figure 1 Schematic diagram of experimental design

and seed powders were significantly able to decrease the lipidoxidation in goat meat patties [12] The effects of natural(sage and rosemary) and synthetic (BHT) antioxidants onprotein oxidation discoloration and texture of refrigeratedpatties produced from pig liver have been studied by Estevezet al [13] Authors reported that the antioxidant propertiesof natural and synthetic antioxidants were similar In treatedsamples the increase in the carbonyl content as a result ofoxidation was significantly (P lt 005) lower than controlsamples Moreover antioxidants could successfully protectheme molecules from degradation Among different naturalantioxidants it has been reported that the extracts of Shirazithyme cinnamon and rosemary reveal substantial antioxi-dant capacity [14]

The main objective of the current study was to comparethe effects of Shirazi thyme cinnamon and rosemary extracts(denoted as natural antioxidants) with those of BHT on pro-tein and lipid oxidations and physicochemicalmicrobial andsensory characteristics of frozen beef burgers during storageThe results of this study may have potential implications

in substituting the synthetic antioxidants with nature-madeones

2 Materials and Methods

A schematic representation of beef burger production isshown in Figure 1

21 Materials Beef flanks (18 fat) from freshly slaughteredanimals (24 hours post slaughter)were purchased froma localmarket (Shiraz Iran) and transported to the laboratory ininsulated polystyrene ice-boxes The meat was ground (MeatGrinder Philips HR2743 AmsterdamNetherlands) througha perforated plate with a hole diameter of 5mm Thiobar-bituric acid (Sigma-Aldrich St Louis MO USA) 1133-tetraethoxypropane (Sigma-Aldrich St Louis MO USA)and diphenyl-2-picrylhydrazyl (DPPH∙) (Sigma-Aldrich StLouisMOUSA) soy protein isolate (SPI 90 protein SonicCo India) onions salt spices and ruskwere also used in thisstudy

Journal of Food Quality 3

22 Plant Extracts Shirazi thyme (Zatariamultiflora) cinna-mon (Cinnamomum zeylanicum) and rosemary (Rosmarinusofficinalis) were purchased from a local grocery The genusand species were certified by experts from the Herbariumof Biology Department (Shiraz University Shiraz Iran)Dried plants were powdered with a mill and then kept inpolyethylene bags at room temperature before extraction

221 Extract Preparation Plant powder (20 g) was thor-oughly mixed with boiling distilled water (500mL) for5min followed by filtration through Whatman grade No 1filter papers and concentration in rotary evaporator (BuchiRotavapor R Switzerland) at 50∘C [15]

222 DPPH Radical Scavenging Activity Antioxidant activ-ity of natural extracts and BHT was calculated using DPPHfree radicalmethod described by Cam et al [16]The amountsof extracts required to replace BHT were calculated basedon the IC50 of BHTThe required amounts of natural extractsshould have equal antioxidant activity to BHT

23 Beef Burger

231 Burger Preparation and Storage The formulation ofbeef burger used in this study was composed of beef (70)onions (134) rusk (4) water (8) SPI (3) salt (1)black (03) and red (02) peppers Ground meat saltwater and minced onion were mixed together After thatSPI was added and then mixed for 15min to obtain ahomogenousmixture Rusk and spices were added in the nextstep Finally natural extracts andor BHT were incorporatedinto the homogenate and thenmixing process was continuedThe concentration of BHT was 100 ppm A burger maker(9 cm internal diameter) was used to shape the mixture intopatties of approximately 90 g and 5mm thickness Burgers(15 patties per treatment) were then packed in light-resistantpolyethylene containers and frozen at minus18∘C Analyses wereperformed during 15-day intervals for two months Beforeanalysis the samples were thawed at +4∘C and then hand-mixed for 30 s

232 Chemical Analysis Moisture protein fat and ashcontents of burgers were determined according to the AOACmethods [17] Carbohydrate content was estimated by sub-tracting the total amounts of moisture protein fat and ashfrom 100

233 pH Measurement Meat sample (10 g) was homog-enized with 50mL deionized water for 1min pH wasmeasured at room temperature using a digital pH meter(Suntex TS-1 Taiwan) equipped with a probe-type combinedelectrode (Ingold) through direct immersion of electrode intothe mixture [17]

234 Instrumental Color Evaluation Color attributes of beefburgers were measured by 119871lowast119886lowast119887lowast method described byYam and Papadakis [18] The values of 119871lowast (brightness) 119886lowast(redness-greenness) and 119887lowast (yellowness-blueness) weremea-sured on the whole outer surfaces of beef burger A wooden

box (50 times 50 times 60 cm3) equipped with a natural daylightsource (6500K) and a digital camera (CanonPowershotA540of six megapixels resolution) in a vertical position and adistance of 25 cm from the samples was used for takingphotos Adobe PhotoshopCS6 was applied to determine theaverage surface color

235 Determination of Lipid Oxidation Lipid oxidationwas monitored by measuring thiobarbituric acid reactivesubstances (TBARS) Meat sample (4 g) was homogenizedwith 20mL trichloroacetic acid solution (20 wv) and thencentrifuged at 3000119892 for 10min The supernatant (2mL) wasmixed with 2mL thiobarbituric acid solution (01 wv indouble distillated water) followed by heating in a water bathat 100∘C for 30min and then cooling to room temperatureTherefore TBARS were extracted in chilled atmosphere Theabsorbance of each extract was measured at 520 nm in aspectrophotometer (spec 1650PC Shimadzu Japan) 1133-tetraethoxypropane was used to develop the standard curvefor TBARS assay TBARS values were reported as mg ofmalonaldehyde per kg of beef burger [7]

236 Metmyoglobin Measurement A modified method ofAn et al [19] was used to measure the metmyoglobincontent in raw beef burgers The sample (4 g) was mixedin a homogenizer with 20mL of phosphate buffer (004MpH 68) and then stored at 1∘C for 1 h The mixture wasthen centrifuged at 3500119892 and 4∘C for 30min Finally thesupernatant was filtered through Whatman grade No 1filter paper The absorbance of the solution was measuredat 525 572 and 700 nm Metmyoglobin () was calculatedaccording to the following equation

Metmyoglobin () = [1395 minus [(119860572 minus 119860700)(119860525 minus 119860700)]]times 100

(1)

Total Aerobic Bacterial Count Total aerobic bacteria werequantified every 15 days using the method described byAliakbarlu et al (2016) Beef burgers (10 g) were asepti-cally transferred into individual stomaching bags containing90mL of sterile saline (09) and homogenized for 2minSerial 10-fold dilutions were prepared in saline and 100 120583Lfrom appropriate dilutions was spread on the surface of platecount agar for total aerobic count (TMC) and then incubatedat 35∘C for 24 h

237 Sensory Evaluation Sensory analyses have been per-formed by 20 trained panelists from the Department of FoodScience and Technology (Shiraz University) Panelists wereboth male and female in the age range of 23ndash28 years oldPanelists were selected based on their previous experiences inconsuming traditional beef burgers Moreover they receivea preparatory session before the sensory test to train themhow to describe all evaluated factors completely Burgers werefried at 150∘C in a forced draft oven to a core temperatureof 72∘C and kept warm in the oven for 3ndash8min until thesensory testing [20] Rectangular pieces of approximately

4 Journal of Food Quality

2 cm were cut from the center of each burger and then servedat room temperature Each panelist randomly evaluated threepieces of all formulations and asked to give a numericalvalue between 1 and 9 for the following attributes taste 1(imperceptible) to 9 (extremely intense) texture attributesand juiciness 1 (extremely dry) to 9 (extremely moist)appearance 1 (extremely soft) to 9 (extremely tough) andodor 1 (imperceptible) to 9 (extremely intense) Tap waterwas provided for panelists to rinse their mouth betweendifferent samples At the end of evaluation each panelist wasasked to give an overall score from 1 (dislike very much) to9 (like very much) for the overall acceptability of differentformulations

24 Statistical Analysis A completely randomized blockdesign with five treatments (including antioxidant-free (con-trol) treatment and those incorporated with BHT cinnamonrosemary and Shirazi thyme extracts) was used in this studyExperiments were performed during a 60-day storage periodat 15-day intervals (0 15 30 45 and 60) Independent blocks(developed from three different batches) were replicatedthree times at each sampling point A two-way analysisof variance (ANOVA) and Duncanrsquos multiple range tests(SAS 80 software SAS Institute Inc Cary NC USA) wereperformed to analyze the effect of treatments storage periodand their interaction on the physicochemical microbial andsensory characteristics of beef burgers at a confidence levelof 005 In the analysis models the treatments storage timesand their interaction were assigned as fixed effects and thereplications as random effects

The given scores of different sensory attributes werecompared between the treatments using general linear model(GLM) Duncanrsquos multiple range tests were used for compar-ison of means at a confidence level of 005 Treatments andassessors were considered as main effects and the replicationsas random effects Data was reported as mean plusmn standarderror (SE)

3 Results and Discussion

31 Antioxidant Activity of Extracts The IC50 values (definedas the concentration of an antioxidant required to reduce theinitial DPPH concentration by 50 using DPPH free radicalmethod described by Cam et al [16]) of natural extracts(including Shirazi thyme cinnamon and rosemary) andsynthetic BHT were 0022 0373 0062 and 0107mgmLrespectively Therefore the amounts of Shirazi thyme cinna-mon and rosemary concentrated extracts required to replace100 ppm BHT in formulation were 22 73 and 28mL per kgof beef burger respectively Cinnamon is a source of bioactivecompounds such as cinnamaldehyde eugenol and coumarin[21] The effect of cinnamon extract as direct scavengersof free radicals has been studied by Roussel et al [22]Carnosic acid and carnosol are the main bioactive com-pounds present in the rosemary extract [23] According toSharififar et al [24] the major chemical compounds presentin Shirazi thyme were carvacrol (3365) thymol (3759) p-cymene (772) 120574-terpinene (388) and 120573-caryophyllene(206)

40

45

50

55

60

65

70

75

80

Met

myo

glob

in (

)

15 30 45 600Storage period (days)

ControlBHTCinnamon extract

Rosemary extractShirazi thyme extract

Figure 2 Effect of incorporating Shirazi thyme cinnamon androsemary extracts on the metmyoglobin () developed in raw beefburgers during frozen storage at minus18∘C

32 Physicochemical Properties of Beef Burger The resultsindicated that the samples contained 5913 moisture 19protein 12 fat 772 carbohydrate and 2 ash

33 Color Stability When assessing meat a consumer paysa great attention to its color which as a visual impressionis induced mainly by the presence of pigments but it alsodepends on tissue composition and meat structure Hencethe color of fresh meat is an important quality parameterthat determines a consumerrsquos response and decision to buyor not to buy that product at retail Changes in 119871lowast 119886lowast and119887lowast values of beef burgers during frozen storage are shown inTable 1 No significant difference (119875 gt 005) was observedbetween the samples incorporated with natural antioxidantsand those incorporated with BHT at production time (day 0)resulting in low Δ119864 values at early stages of storage All of theformulations showed significant decrease in 119886lowast during frozenstorage Formulation incorporated with rosemary extractshowed lower amounts of 119886lowast at the end of storage timeThe significant decrease in 119886lowast values indicated the red colorreduction of products during storage this is despite the factthat BHT- and extract-incorporated treatment significantlyreduced the Met-mb development ratio in comparison tocontrol one (Figure 2) During the first 30 days of storage119871lowast values increased significantly (119875 lt 005) then remainedconstant During frozen storage changes in the amountsof 119871lowast in cinnamon- (642) or Shirazi thyme-incorporatedsamples (597) were less than those in other formulationsSamples incorporated with rosemary extract showed the leastredness (433)

A significant decrease in 119886lowast values of raw pork pat-ties containing grape seed extract and bearberry has beenreported over a 12-day storage by Carpenter et al [25]however 119887lowast values (particularly of control samples) increasedsignificantly (119875 lt 005) Similarly Nunez de Gonzalez et al[26] reported that 119886lowast value of beefs stored under refrigeration

Journal of Food Quality 5

Table 1 Effect of addition of Shirazi thyme cinnamon and rosemary extracts and BHT on 119871lowast 119886lowast 119887lowastand Δ119864 values of raw beef burgersduring frozen storage at minus18∘CParameter Sample Storage period (days)

0 15 30 45 60

119871lowastControl 6033 plusmn 088 glowastlowast 5800 plusmn 058 hi 7133 plusmn 034 abc 7167 plusmn 034 ab 7267 plusmn 067 aBHT 5867 plusmn 088 ghi 5733 plusmn 034 i 6833 plusmn 034 de 6933 plusmn 034 cd 7067 plusmn 067 abc

Cinnamon extract 6033 plusmn 067 g 5433 plusmn 034 j 5967 plusmn 067 gh 6533 plusmn 067 f 6800 plusmn 058 deRosemary extract 5733 plusmn 034 i 5433 plusmn 082 i 6967 plusmn 088 bcd 7133 plusmn 088 abc 7167 plusmn 034 ab

Shirazi thyme extract 5733 plusmn 146 i 5667 plusmn 067 i 5700 plusmn 058 i 6700 plusmn 058 ef 6833 plusmn 067 de

119886lowastControl 1133 plusmn 034 a 833 plusmn 034 de 833 plusmn 034 de 767 plusmn 034 ef 667 plusmn 034 fghBHT 1100 plusmn 058 ab 667 plusmn 034 fgh 767 plusmn 067 ef 700 plusmn 058 fg 667 plusmn 034 fgh

Cinnamon extract 933 plusmn 034 cd 733 plusmn 034 efg 667 plusmn 034 fgh 567 plusmn 034 hij 533 plusmn 034 ijkRosemary extract 1167 plusmn 034 a 533 plusmn 034 ijk 533 plusmn 034 ijk 467 plusmn 034 jk 433 plusmn 034 k

Shirazi thyme extract 1000 plusmn 058 667 plusmn 034 fgh 633 plusmn 034 ghi 567 plusmn 034 hij 533 plusmn 034 ijk

119887lowastControl 2333 plusmn 034 kl 2500 plusmn 058 ij 3233 plusmn 034 bc 3267 plusmn 067 b 3400 plusmn 058 aBHT 2233 plusmn 034 lmn 2333 plusmn 034 kl 3100 plusmn 058 cd 3133 plusmn 067 bcd 3167 plusmn 067 bcd

Cinnamon extract 2167 plusmn 034 mno 2267 plusmn 034 lm 2533 plusmn 034 ij 2600 plusmn 058 i 2767 plusmn 034 hRosemary extract 2033 plusmn 0340 2100 plusmn 058 no 2900 plusmn 058 fgh 3067 plusmn 034 de 3133 plusmn 067 bcd

Shirazi thyme extract 2300 plusmn 000 klm 2433 plusmn 034 jk 2833 plusmn 034 gh 2933 plusmn 034 efg 3033 plusmn 034 def

Δ119864lowastlowastlowastControl 000 plusmn 000 f 1700 plusmn 025 aBHT 272 plusmn 069 e 1409 plusmn 018 bc

Cinnamon extract 282 plusmn 072 e 1078 plusmn 095 dRosemary extract 442 plusmn 104 e 1559 plusmn 102 ab

Shirazi thyme extract 354 plusmn 030 e 1229 plusmn 080 cdlowastlowastData represent averages of three independent repeats plusmn standard errorslowastlowastMeans with different letters are significantly different (119875 le 005)lowastlowastlowastFor each storage time the color difference (Δ119864) was calculated by comparing the color attributes of different formulations with those of control sample

for 10 weeks decreased significantly (119875 lt 005) The resultsof the current study showed that high antioxidant activity ofnatural extracts can be potentially used to develop naturalcolor stabilizers particularly for controlling 119871lowast and 119887lowast valuesin frozen beef burger

As mentioned already samples incorporated with BHTand natural extracts did not show any significant differencein Δ119864 value at the beginning of the storage time However atthe end of storage the lowest and highest changes in Δ119864wereobserved in cinnamon-incorporated and control samplesRedmeat color is an important property of visual appearanceand could influence meat purchasing decisions more thanany other quality parametersThe color of meat products andmeat is influenced by metmyoglobin percentage in muscleInitially the myoglobin was changed into oxymyoglobin(light pink color) which could result in brighter redmeat andthen oxymyoglobin was oxidized into metmyoglobin duringstorage [7]

34 Metmyoglobin Content Assay The amount of metmyo-globin has been positively linked to the extent of proteinoxidation in meat products The heme complex of heme(in) proteins consists of iron in the ferrous state (Fe+2)which turns into the ferric state (Fe+3) via a process calledautoxidation [27] The effects of natural extracts on thechanges of metmyoglobin content are shown in Figure 2Themaximum amount of metmyoglobin (7426) was measuredin antioxidant-free samples The presence of antioxidantsresulted in a significant decrease (1625ndash1847) in the

amounts of metmyoglobin developed during storage whichwas attributed to the strong antioxidant activity An etal [19] evaluated the percent metmyoglobin of the porkjerky samples incorporated with different kimchi powderconcentrations It has been reported that the metmyoglobincontents () of the samples prepared with various kimchipowder levels (ranged from 81 to 83) were significantly(119875 lt 005) lower than that of control sample (85) [19]There was no significant difference between the amounts ofmetmyoglobin under the influence of natural extracts or BHTindicating that these natural extracts can be utilized as asubstitute for BHT to prevent discoloration

The myoglobin reactions with peroxides result in theformation of lipid oxidation promoting compounds [28]The lowest amount of metmyoglobin was measured in thesamples formulated with cinnamon extract indicating thatit was more effective than the other antioxidants (eithernatural or synthetic) in preventing metmyoglobin formationA reverse relationship between the metmyoglobin level and119886lowast value was observed in this study A decrease in 119886lowast valuescorresponding to the decreased redness of lamb meat as aresult of myoglobin oxidation (metmyoglobin formation) hasbeen reported previously [29 30]

Metmyoglobin content increased during storage Thelowest increasing rate was observed in the samples incor-porated with rosemary extract The highest amount of met-myoglobin was observed in the control sample at the endof storage Changes in the metmyoglobin content of controlsample became significant after 15 days

6 Journal of Food Quality

Table 2 Thiobarbituric acid reactive substances (TBARS) values (mg malonaldehyde per kg) of beef burger during frozen storage at minus18∘CSample Storage period (days)

0 15 30 45 60Control 012 plusmn 001lowast 015 plusmn 002 020 plusmn 002 023 plusmn 001 041 plusmn 004BHT 010 plusmn 001 013 plusmn 001 015 plusmn 002 018 plusmn 001 023 plusmn 002Cinnamon extract 011 plusmn 001 013 plusmn 001 016 plusmn 001 017 plusmn 002 024 plusmn 002Rosemary extract 011 plusmn 001 013 plusmn 002 017 plusmn 002 019 plusmn 002 022 plusmn 002Shirazi thyme extract 012 plusmn 001 014 plusmn 002 017 plusmn 002 018 plusmn 001 026 plusmn 002lowastData represent averages of three independent repeats plusmn standard errors

35 Oxidative Stability Initiation is the step in which afatty acid radical is produced Two notable initiators inoxidative stability are OH∙ and HOO∙ which combines witha hydrogen atom to make water and a fatty acid radical Thefatty acid radical is not a very stable molecule so it reactsreadily with molecular oxygen thereby creating a peroxyl-fatty acid radical This radical is also an unstable species thatreacts with another free fatty acid producing a different fattyacid radical and a lipid peroxide or a cyclic peroxide if ithad reacted with itself This cycle continues as the new fattyacid radical reacts in the same wayThe radical reaction stopswhen two radicals react and produce a nonradical speciesThe lipid oxidation leads to produce of some componentscausing off-flavors and reduced nutritional quality such asmalondialdehyde and 4-hydroxynonenal

Thiobarbituric acid test can be used to determine thesecondary products of lipid oxidation in different foods suchas meat and its products [31] Thiobarbituric acid reactivesubstances (TBARS) values of different formulations (as afunction of storage time) are shown in Table 2 Exceptfor control sample the variations in TBARS values of theother formulations revealed a similar pattern Due to theabsence of antioxidant in formulation the observed changesin TBARS values of control were significantly (119875 lt 005)higher than others (8636 higher than rosemary) Natu-ral extracts were as effective as BHT for preventing lipidoxidation in beef burgers This observation indicated thatnatural herbal extracts are suitable replacers for syntheticantioxidant It has been reported that rosemary oleoresin(7704) and a mixture of BHT and BHA (7869) wasequally efficient in inhibiting the lipid oxidation of breakfastsausage containing 25 turkey meat [32] These findings arealso in good agreement with those of Mielnik et al [33] whoreported lower TBARS values after cooking of mechanicallydeboned turkey meat already stored in dark cold and treatedwith rosemary (8834) and grape seed extracts (8383)Sanchez-Escalante et al [34] reported that incorporatingrosemary essential oil into beef patties led to a significant(119875 lt 005) decrease (6400) in TBARS values during coldstorage The essential oil of rosemary was also effective inpreventing (7243) the rancidity of heat-treated turkeymeatproducts [35] It has also been reported that rosemary extractaddition into deboned poultry meat can protect (9820) theproduct from cooking-induced oxidation [36]

Regardless of sample type examined TBARS valuesincreased significantly during the frozen storage and reached

43

45

47

49

51

53

55

57

59

Tota

l aer

obic

bac

teria

l cou

nt (l

og cf

ug)

15 30 45 600Storage period (Days)

52

53

54

55

56

57

58

59

6

61

pH

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

Figure 3 Total aerobic bacterial count (log cfug) (solid symbols)and pH value (open symbols) of different beef burger formulationsas a function of storage time

to a maximum amount of 041mg malonaldehyde per kg inantioxidant-free (control) sample after 60 days At TBARSvalues of 20 off-flavors are definitely detectable and themeatis considered to be unacceptable [37]

36 Changes in pH Values Changes in pH values of beefburgers during frozen storage are shown in Figure 3 Allformulations revealed relatively similar pH values just afterproduction ranging from 588 to 593 coinciding with theISIRI 2008 Mohamed and Mansour [38] similarly reportedthat no significant differences (119875 gt 005) were observed in thepH values of beef patties after incorporating natural herbalextracts

A downward pattern of different rates was observed in thepH values of all formulations during frozen storage As nomicrobial growth was expected during storage the decreasein the pH values could be attributed to the microbial growthduring thawing (by consuming sugar and producing organicacids) Control sample had the lowest pH (551) at the end ofstorage Emiroglu et al [39] reported that the pH values of

Journal of Food Quality 7

all fresh ground beef patty samples treated with thyme andoregano generally decreased after sixth day of storage (119875 gt005)

Also the result showed that to decrease pH amount oflipid oxidation and metmyoglobin significantly increasedLapidot et al (2005) evaluated lipid peroxidation of grilledred turkey muscle (Donor Kabab) as affected by pH In thisstudy they show indeed that lipid peroxidation and myo-globin of a real fast food (turkey Doner Kebab shawarma) issignificantly more rapidly oxidized at pH 30 than at pH 50

37 Microbial Growth As shown in Figure 3 total aerobicbacterial counts of antioxidants-incorporated formulationswere not significantly (119875 lt 005) different The highestamount of total count was observed in control sample(Figure 3) Shirazi thyme-incorporated beef burgers had thelowest microbial count which could be attributed to thehigh antimicrobial properties resulting from thymol and car-vacrol The antibacterial mechanism of thymol and carvacrolis the disruption of the cytoplasmic membrane which raisesits permeability and depolarizes its potential Total countof frozen raw beef burger should be lower than 6 log cfug[40] Except for the control sample the microbial counts ofbeef burgers were lower than the maximum allowed countA relatively good correlation was observed between the pHvalues and total aerobic counts For example control samplehad the lowest pH and the highestmicrobial count Rosemaryextract (1000 ppm) inhibitory effect on the microbial growthof surface-applied beef steaks has been reported by Djenaneet al [41] However Sanchez-Escalante et al [34] reportedthat rosemary did not affect the microbial counts of beefpatties during storage (3 logCFUg)

An increase in the microbial counts was observed duringstorage but not beyond the standard range As a rule ofthumb in good manufacturing and hygienic practices duringpreparation of beef burger and its related products rapidand proper storage is important for decreasing the microbialgrowth and enhancing the shelf life

Vieira et al [42] studied the effect of frozen storage condi-tions (temperature and length of storage) on microbiologicaland sensory quality of rustic crossbred beef at different statesof ageing The result showed that psychrotrophic bacteriaincreased (138 logCFUg) significantly during 90-day storage38 Sensory Properties Color flavor and texture are themostimportant sensory attributes which influence the acceptabil-ity of meat products by consumers [43] Sensory evaluationresults of cooked beef burgers are shown in Figure 4 Gener-ally incorporating Shirazi thyme cinnamon and rosemaryextracts into beef burger formulations had no significantinfluence on the sensory properties Although samples for-mulated with Shirazi thyme and cinnamon extracts with6944 and 7167 acceptability obtained the highest tastescores by panelists (119875 lt 005) The antioxidant prop-erties of natural extracts were the main reason for theincreased sensory scores of natural extract-incorporatedformulations through preventing the formation of oxidation-mediated off-flavors and off-odors (short-chain aldehydes

4

45

5

55

6

65

7Appearance

Taste

OdorTexture

Overall

ControlBHTRosemary extract

Shirazi thyme extractCinnamon extract

Figure 4 Sensory evaluation of different beef burger formulationsa 9-point descriptive scale (1 = extremely poor and 9 = highlyacceptable) was used during evaluation

and ketones) during storage Moreover the presence ofpleasant volatile constituents in natural extracts (particu-larly in cinnamon and Shirazi thyme) led to an increasedsensory score in comparison to the BHT-incorporatedformulation

A significant increase in the flavor scores of beef pattiesincorporated with antioxidant mechanically deboned poul-try meat during frozen storage was similarly reported byMohamed and Mansour [38]

4 Conclusion

This work aimed to study the possible replacement ofsynthetic antioxidant BHT with natural extracts (includingShirazi thyme cinnamon and rosemary extracts) in beefburger formulation Different samples were prepared thendifferent characteristics such as protein and lipid oxidationand physicochemical microbial and sensory properties wereevaluated during frozen storage Herbal extracts could inhibitthe lipid oxidation in formulated burgers Moreover it wasdemonstrated that natural herbal extracts were generallybetter than BHT in preventing the lipid and protein oxi-dations as well as improving the sensory attributes of beefburgersTherefore it can be concluded that natural extracts ofShirazi thyme (0022mgmL) cinnamon (0373mgmL) androsemary (0062mgmL) can be used as natural substitutesfor BHT (0107mgmL)This substitutionmay have potentialimplication for developing green-labeled meat product Infuture studies it would be informative to study the effect ofmixed extracts and their possible synergistic or antagonisticeffects in extending the shelf life of meat products

8 Journal of Food Quality

Additional Points

Practical Applications Beef burger containing natural antiox-idant is one of themost important functional food for humanconsumption attributable to its nutritional properties andhealth effects However the nutraceutical properties of thisfood have improved due to alternative BHT with extractsThe present investigation demonstrated the effects of addingvarious natural antioxidants to the beef burger so as tomonitor the changes that occur to the physicochemicalantimicrobial and sensorial properties of the beef burger

Conflicts of Interest

The authors declare that they have no conflicts of interest

Acknowledgments

This research project was financially supported by ScientificAffairs Shiraz University and Department of Food Scienceand Technology Shiraz University Shiraz Iran

References

[1] D Ladikos and V Lougovois ldquoLipid oxidation in muscle foodsa reviewrdquo Food Chemistry vol 35 no 4 pp 295ndash314 1990

[2] C JMussinan andM JMorello ldquoFlavor analysis developmentsin isolation and characterizationrdquo American Chemical Societypp 343ndash358 1998

[3] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWTmdashFoodScience and Technology vol 68 pp 385ndash390 2016

[4] G Comi E Tirloni D Andyanto M Manzano and LIacumin ldquoUse of bio-protective cultures to improve the shelf-life and the sensorial characteristics of commercial hamburg-ersrdquo LWTmdashFood Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[5] F Shahidi ldquoAntioxidants in food and food antioxidantsrdquoFoodNahrung vol 44 pp 158ndash163 2000

[6] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[7] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[8] H H Hashemi Gahruie M H Eskandari G Mesbahi andM A Hanifpour ldquoScientific and technical aspects of yogurtfortification a reviewrdquo Food Science and Human Wellness vol4 no 1 pp 1ndash8 2015

[9] K Yamazaki S Kawamorita H Ohmiya and M SawamuraldquoDirected ortho borylation of phenol derivatives catalyzed by asilica-supported iridium complexrdquo Organic Letters vol 12 no18 pp 3978ndash3981 2010

[10] A Roberts and L A Haighton ldquoA hard look at FDArsquos review ofGRAS noticesrdquo Regulatory Toxicology and Pharmacology vol79 pp S124-S128 2016

[11] H H Hashemi Gahruie E Ziaee M H Eskandari andS M Hosseini ldquoCharacterization of basil seed gum-basededible films incorporated with Zataria multiflora essential oilnanoemulsionrdquo Carbohydrate Polymers vol 166 pp 93ndash1032017

[12] S K Devatkal K Narsaiah and A Borah ldquoAnti-oxidant effectof extracts of kinnow rind pomegranate rind and seed powdersin cooked goatmeat pattiesrdquoMeat Science vol 85 no 1 pp 155ndash159 2010

[13] M Estevez R Ramırez S Ventanas and R Cava ldquoSage androsemary essential oils versus BHT for the inhibition of lipidoxidative reactions in liver paterdquo LWTmdashFood Science andTechnology vol 40 no 1 pp 58ndash65 2007

[14] E Abdollahzadeh M Rezaei and H Hosseini ldquoAntibacterialactivity of plant essential oils and extracts the role of thymeessential oil nisin and their combination to control listeriamonocytogenes inoculated in minced fish meatrdquo Food Controlvol 35 no 1 pp 177ndash183 2014

[15] A Alaklabi I A Arif A Ahamed R Surendra Kumar andA Idhayadhulla ldquoEvaluation of antioxidant and anticanceractivities of chemical constituents of the saururus chinensis rootextractsrdquo Saudi Journal of Biological Sciences 2017

[16] M Cam Y Hısıl and G Durmaz ldquoClassification of eightpomegranate juices based on antioxidant capacity measured byfourmethodsrdquo FoodChemistry vol 112 no 3 pp 721ndash726 2009

[17] AOAC Association of Official Agricultural Chemists ldquoOfficialmethods of analysis of AOAC Internationalrdquo in AgricultureChemicals Contaminants Drugs vol 1 AOAC InternationalArlington VA USA 16th edition 1995

[18] K L Yam and S E Papadakis ldquoA simple digital imagingmethodfor measuring and analyzing color of food surfacesrdquo Journal ofFood Engineering vol 61 no 1 pp 137ndash142 2004

[19] K-I An J-H Choi Y-S Choi et al ldquoEffects of kimchi powderon quality characteristics of semi-dried pork jerkyrdquo KoreanJournal for Food Science of Animal Resources vol 30 no 2 pp198ndash205 2010

[20] B Kodal Coskun E Calikoglu Z Karagoz Emiroglu and KCandogan ldquoAntioxidant active packaging with soy edible filmsand oregano or thyme essential oils for oxidative stability ofground beef pattiesrdquo Journal of Food Quality vol 37 no 3 pp203ndash212 2014

[21] B Shan Y Z Cai M Sun and H Corke ldquoAntioxidant capacityof 26 spice extracts and characterization of their phenolicconstituentsrdquo Journal of Agricultural and Food Chemistry vol53 no 20 pp 7749ndash7759 2005

[22] A-M Roussel I Hininger R Benaraba T N Ziegenfuss andR A Anderson ldquoAntioxidant effects of a cinnamon extract inpeople with impaired fasting glucose that are overweight orobeserdquo Journal of the American College of Nutrition vol 28 no1 pp 16ndash21 2009

[23] S Moreno T Scheyer C S Romano and A A VojnovldquoAntioxidant and antimicrobial activities of rosemary extractslinked to their polyphenol compositionrdquo Free Radical Researchvol 40 no 2 pp 223ndash231 2006

[24] F Sharififar M H Moshafi S H Mansouri M Khodashenasand M Khoshnoodi ldquoIn vitro evaluation of antibacterial andantioxidant activities of the essential oil and methanol extractof endemic Zataria multiflora Boissrdquo Food Control vol 18 no7 pp 800ndash805 2007

[25] R Carpenter M N OrsquoGrady Y C OrsquoCallaghan N M OrsquoBrienand J P Kerry ldquoEvaluation of the antioxidant potential of grape

Journal of Food Quality 9

seed and bearberry extracts in raw and cooked porkrdquo MeatScience vol 76 no 4 pp 604ndash610 2007

[26] M T Nunez de Gonzalez B S Hafley R M Boleman R KMiller K S Rhee and J T Keeton ldquoAntioxidant propertiesof plum concentrates and powder in precooked roast beef toreduce lipid oxidationrdquo Meat Science vol 80 no 4 pp 997ndash1004 2008

[27] M P Richards and M A Dettmann ldquoComparative analysisof different hemoglobins autoxidation reaction with peroxideand lipid oxidationrdquo Journal of Agricultural and FoodChemistryvol 51 no 13 pp 3886ndash3891 2003

[28] J Everse and N Hsia ldquoThe toxicities of native and modifiedhemoglobinsrdquo Free Radical Biology and Medicine vol 22 no6 pp 1075ndash1099 1997

[29] C Kennedy D J Buckley and J P Kerry ldquoInfluence of differentgas compositions on the short-term storage stability of mother-packaged retail-ready lamb packsrdquo Meat Science vol 69 no 1pp 27ndash33 2005

[30] J P Kerry M G OrsquoSullivan D J Buckley P B Lynch andP A Morrissey ldquoThe effects of dietary 120572-tocopheryl acetatesupplementation and modified atmosphere packaging (MAP)on the quality of lamb pattiesrdquo Meat Science vol 56 no 1 pp61ndash66 2000

[31] J Fernandez J A Perez-Alvarez and J A Fernandez-LopezldquoThiobarbituric acid test for monitoring lipid oxidation inmeatrdquo Food Chemistry vol 59 no 3 pp 345ndash353 1997

[32] S Barbut D B Josephson and A J Maurer ldquoAntioxidantproperties of rosemary oleoresin in Turkey sausagerdquo Journal ofFood Science vol 50 no 5 pp 1356ndash1359 1985

[33] M B Mielnik K Aaby and G Skrede ldquoCommercial antioxi-dants control lipid oxidation in mechanically deboned turkeymeatrdquoMeat Science vol 65 no 3 pp 1147ndash1155 2003

[34] A Sanchez-Escalante D Djenane G Torrescano J A Beltranand P Roncales ldquoThe effects of ascorbic acid taurine carnosineand rosemary powder on colour and lipid stability of beef pattiespackaged in modified atmosphererdquoMeat Science vol 58 no 4pp 421ndash429 2001

[35] M B Mielnik S Sem B Egelandsdal and G Skrede ldquoBy-products from herbs essential oil production as ingredient inmarinade for Turkey thighsrdquo LWTmdashFood Science and Technol-ogy vol 41 no 1 pp 93ndash100 2008

[36] J H Macneil P S Dimick and M G Mast ldquoUse of chemicalcompounds and a rosemary spice extract in quality mainte-nance of deboned poultry meatrdquo Journal of Food Science vol38 no 6 pp 1080-1081 1973

[37] E TEC ldquoMeat technology update 1-6 2009rdquo[38] H M H Mohamed and H A Mansour ldquoIncorporating

essential oils of marjoram and rosemary in the formulation ofbeef patties manufactured with mechanically deboned poultrymeat to improve the lipid stability and sensory attributesrdquoLWTmdashFood Science and Technology vol 45 no 1 pp 79ndash872012

[39] Z K Emiroglu G P Yemis B K Coskun and K CandoganldquoAntimicrobial activity of soy edible films incorporated withthyme and oregano essential oils on fresh ground beef pattiesrdquoMeat Science vol 86 no 2 pp 283ndash288 2010

[40] ISIR Raw frozen hamburgermdashSpecifications vol 2304 Instituteof standards and industrial research of Iran Karaj Iran 3rdedition 2008

[41] DDjenane A Sanchez-Escalante J A Beltran andP RoncalesldquoAbility of 120572-tocopherol taurine and rosemary in combination

with vitamin C to increase the oxidative stability of beef steakspackaged in modified atmosphererdquo Food Chemistry vol 76 no4 pp 407ndash415 2002

[42] C Vieira M T Diaz B Martınez and M D Garcıa-CachanldquoEffect of frozen storage conditions (temperature and lengthof storage) on microbiological and sensory quality of rusticcrossbred beef at different states of ageingrdquo Meat Science vol83 no 3 pp 398ndash404 2009

[43] J Aliakbarlu and S Khalili Sadaghiani ldquoEffect of avishaneshirazi (zataria multiflora) and clove (syzygium aromaticum)essential oils on microbiological chemical and sensory proper-ties of ground sheep meat during refrigerated storagerdquo Journalof Food Quality vol 38 no 4 pp 240ndash247 2015

Research ArticleOptimization of Ultrasound Extraction of Cactus Pear(Opuntia ficus indica) Seed Oil Based on AntioxidantActivity and Evaluation of Its Antimicrobial Activity

Mariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-CansinoErnesto Alaniacutes-Garciacutea Luis Delgado-Olivares Joseacute Alberto Ariza-OrtegaEsther Ramiacuterez-Moreno and Joseacute de Jesuacutes Manriacutequez-Torres

Centro de Investigacion Interdisciplinario Area Academica de Nutricion Instituto de Ciencias de la Salud Universidad Autonoma delEstado de Hidalgo Circuito Actopan-Tilcuautla SN Ex Hacienda La Concepcion 42160 San Agustın Tlaxiaca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 20 February 2017 Accepted 9 April 2017 Published 27 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Marıa de los Angeles Ortega-Ortega et alThis is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The purpose of the present study was to determine the optimal ultrasound conditions (amplitude level and time) for the extractionof cactus pear seed oil with the highest antioxidant activity using a closed system Seed oil was analyzed for yield antioxidant activityby ABTS and DPPH and antimicrobial activity Conventional extraction methods were assessed for comparison Amplitude levelsignificantly affected antioxidant activity in linear terms (p lt 00001 DPPH and p lt 0001 ABTS resp) so at lower amplitudes thehigher antioxidant activity was achieved The optimum ultrasound extraction conditions were of 78 amplitude for 10min andyielded antioxidant activity values of 6625mg AAE100 g and 289120583mol TE100 g for ABTS and DPPH respectively Comparedwith conventional extraction methods ultrasound exhibited lower oil yield and antioxidant activity but had the potential toachieve comparable results if multiple ultrasound extractions are performed in the time needed by conventional methods Seed oilsshowed similar antimicrobial activity despite the extraction method and were more effective against Escherichia coli The resultsdemonstrated that ultrasound can be an alternative extraction method of seed oils from fruits such as cactus pear

1 Introduction

Cactus pear fruit (Opuntia ficus indica) is common in aridand semiarid regions around the world [1] This fruit that ismainly consumed fresh in Mexico [2] is composed by pulppeel and seeds [3] According to several studies cactus pearfruit has bioactive compounds [4 5] with high antioxidantand antimicrobial activity [6 7] Some of these compoundsare found in the seeds [8] which comprise 3 to 15 of thecactus pear pulp [9] and are usually considered waste afterpulp processing [7] Seeds also have a high content of oil(988 gkg) [10] characterized by high levels of linoleic andoleic acids [7] and other components as phenols [11] all whichmay contribute to humanhealth [12] Currently seed oils havebeen used as natural agents for food preservation [13] andmany have exhibited antimicrobial and antioxidant activity

some of these oils are from pumpkin [14] apple [15] blackcumin [16] and basil [17] among other seeds Cactus pearseeds fromOpuntia dillenii also have a high antioxidant activ-ity derived from bioactive compounds such as polyphenolsand polyunsaturated fatty acids [18] Some polyunsaturatedfatty acids have also been identified in seeds from Opuntiaficus indica [19 20] implying that these seeds may also havehigh antioxidant activity

Seed oil is usually extracted by means of conventionalmethods such as Soxhlet and maceration using heat agita-tion or long extraction times [21] Microwave supercriticalfluids and ultrasonic assisted extraction are unconventionalmethods that exert a physical effect on the sample [22]Ultrasound has been used to extract antioxidants frommanyfood materials including seeds Ultrasound and ultrasound-assisted extractions use sound waves to produce cavitation

HindawiJournal of Food QualityVolume 2017 Article ID 9315360 9 pageshttpsdoiorg10115520179315360

2 Journal of Food Quality

microbubbles that collapse violently in the sample and facili-tate the release and extraction of several compounds [23ndash25]Some researchers had evaluated ultrasound-assisted extrac-tion in an open system using a sonicator probe directly onthe liquid sample to obtain seed oil fromflaxseed [26] Koreanpine [27] and pomegranate [28] The purpose of the presentstudy was to optimize the extraction conditions of cactuspear seed oil using ultrasound in a closed system based onantioxidant activity and using response surfacemethodologyYield extraction and antioxidant and antimicrobial activitywere compared with conventional methods

2 Materials and Methods

21 Sample Green cactus pear (Opuntia ficus indica) Reynavariety was provided by the Mexican Association CoMeN-Tuna (Consejo Mexicano del Nopal y la Tuna AC ofActopanHidalgoMexico) in spring of 2012Thegreen cactuspear seeds were obtained after several washes with water thatremoved the pulp and residues The seeds were leaved todry at ambient temperature until they reached a moisture of643 After the seeds were crushed using an industrial mill(Cyclotec 1093 Tecator Hoganas AB Sweden) the powderwas passed through a mesh sieve to obtain a particle size ofapproximate 05mm and then stored in sealed plastic bags atroom temperature and dark conditions

22 Ultrasound Extraction Ultrasound (VCX-1500 Sonic ampMaterials Inc Newtown CTUSA) at 1500Wwith a constantfrequency of 20 kHz and a probe of 25mm was used forthe extraction of green cactus pear seeds oil Extractionfrom milled and sieved seeds (20 g) was carried out at anamplitude and time ranges of 80 to 90 and 5 to 15minrespectively and a fixed outlet temperature of 25∘C A sampleof 400mL was introduced in a jacketed vessel with waterat 4∘C circulating through the secondary layer [29] Afterextraction the aqueous and solid phases were separatedby filtration using a vacuum pump (DOA-P704-AA GASTManufacturing Inc BentonHarbor MI USA) Both phasesaqueous and solid (this last was dried) (Weston 74-1001-wWeston Products LLC Strongsville OH USA) were mixedwith hexane for 30min and then separated from the solventby filtration The aqueous phase was centrifuged (Allegra25R Beckman Couler CA USA) at 10000 rpm for 30minat 4∘C and was stored in plastic containers and kept frozenuntil analysis The solid phase was stored in hermeticallysealed bags in the dark The solvent obtained from the twophaseswas evaporated (BUCHILabortechnikAG Flawil SGSwitzerland) at 40∘C to obtain the oil

23 Soxhlet Extraction Soxhlet extraction was performedaccording to the AOAC [30] Milled and sieved seeds (5 g)hexane (120mL) and a universal fat extraction system (BuchiLabortechnik AG Flawil SG Switzerland) were used

24 Maceration Extraction Milled and sieved seeds (10 g)were introduced in a previously defatted cotton bag andthen immersed in 200mL of hexane in a closed glass at atemperature of asymp25∘C After the sample was stored in a dark

place for 24 hrs the oil was obtained after solvent evaporationusing a rotary evaporator (BUCHI Labortechnik AG FlawilSG Switzerland) at 40∘C

25 Yield Oil yield was determined according to Chouguiet al [31] using the following equation

Oil () = (1198721 minus11987201198722 ) times 100 (1)

where1198720 is the weight of the empty Eppendorf tube (g)1198721is the weight of the Eppendorf tube after evaporation (g) and1198722 is the weight of the milled seeds (g)

The oil was stored in 2mL amber Eppendorf tubes atminus32∘C until analysis

26 Determination of Antioxidant Activity

261 ABTS Assay Antiradical capacity by ABTS was mea-sured according to Kuskoski et al [32] The radical cation221015840azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) diam-monium salt (ABTS∙+) was produced by reacting 7mMABTSstock solution with 245mM potassium persulfate in thedark at room temperature for 16 hrs before being used TheABTS∙+ solution was diluted with deionized water to anabsorbance of 070 plusmn 010 at 754 nm An aliquot of 20120583L ofsample was added to 980120583L of the diluted ABTS∙+ solutionand absorbance readings were taken after 7min incubationat room temperature The absorbance of the mixture wasmeasured at 754 nm in themicroplate reader (PowerWaveXSUV-Biotek software KC Junior VT USA) and antioxidantcapacity was expressed as mg ascorbic acid equivalent per100 g of oil (mg AAE100 g)

262 DPPH Assay Antiradical activity was measured using11-diphenyl-2-picrylhydrazyl (DPPH∙) radical as describedby Morales and Jimenez-Perez [33] A methanol-acetatesolution (74mg100mL) of the stable DPPH∙ radical wasprepared A sample aliquot of 100120583Lwas placed into vials and500 120583L of DPPH∙ solution was added before the mixture wasleft to sit at room temperature for 1 hr Finally absorbancewasmeasured at 520 nm in the microplate reader (Power WaveXS UV-Biotek software KC JuniorWinooski VT USA) andantioxidant activity was expressed as 120583mol of Trolox equiva-lents per 100 g of oil (120583mol TE100 g)

27 Experimental Design

271 Optimization The optimization of the ultrasoundextraction conditions was performed using the responsesurface methodology (RSM) with a central composite rotat-able design for two independent extraction variables at fivelevelsThe independent extraction variables (amplitude level80ndash90 time 5ndash15min) were determined based on prelimi-nary experiments where higher antioxidant activity by ABTSand DPPH was observed Design consisted in thirteen com-binations with five central points replicates (Table 1) Exper-imental data were subjected to multiple nonlinear regression

Journal of Food Quality 3

Table 1 Experimental design matrix

Numbera Pattern Amplitude level () Time (min)119883119894 119883119895

(1) 00 85 10(2) +minus 90 5(3) ++ 90 15(4) 00 85 10(5) A0 92 10(6) minusminus 80 5(7) 00 85 10(8) a0 78 10(9) 0A 85 17(10) minus+ 80 15(11) 00 85 10(12) 00 85 10(13) 0a 85 3aNonrandomized

analysis (JMP 702 SAS Institute Inc Cary NC USA) fittedto a second-order polynomial model

119884 = 1205730 +2

sum119894=1

120573119894119883119894 +2

sum119894=1

1205731198941198941198832119894 +sum119894

sum119895=119894+1

120573119894119895119883119894119883119895 (2)

where 119884 is the predicted response 1205730 is the constant coeffi-cient120573119894 is the lineal coefficient120573119894119894 is the quadratic coefficientand120573119894119895 is the interaction coefficients In thismodel119883119894 and119883119895are the independent extraction variables amplitude level ()and time (min) respectively

The adequacy of themathematicalmodel was determinedusing the coefficient 1198772The significance of the model regres-sion coefficients was evaluated using an analysis of varianceThree-dimensional curves from the response surface plotswere obtained to interpret the effects of the interactionbetween independent variables on the response variablesContour plots were generated to represent the extrapolationand interpret the optimization of the extraction variablesusing the Sigma Plot 123 graphing software (SYTAT softwareInc Richmond CA USA)

272 Treatment Comparison Comparison between extrac-tion methods (ultrasound-optimized Soxhlet and macera-tion) was carried out by a one-way analysis of variance(ANOVA) All determinations were performed in triplicateand significant differences between means were determinedby Duncan test (p le 005) using the SPSS program (150 SPSSInc Chicago IL USA)

28 Scanning Electron Microscopy Scanning electron micro-scopy (SEM) was used to examine the morphological alter-ations caused to the cactus pear seeds before and after theultrasound extraction Samples deposited on the siliconwaferwere coated with a thin layer of gold (Denton VacuumDesk V Moorestown NJ USA) applying 20 millitorr and

20mA during 4min Samples were observed in a scanningelectronic microcopy (JEOL JSM-6300 Peabody MA USA)at 1000 and 500 amplifications and micrographs were takento establish the structural comparison between both samples

29 Antimicrobial Activity The green cactus pear seed oilwas tested against one Gram-positive bacteria Staphylococ-cus aureus (ATCC 1654) and two Gram-negative bacteriaEscherichia coli (ATCC 25922) and Pseudomonas aeruginosa(ATCC 27853) All microorganisms were obtained from theMexicanMicrobial Culture Collection of CINVESTAV of theNational Polytechnic Institute (Mexico) For each microor-ganism bacterial suspensions were made in a soybean-casein digest medium to a concentration of approximately108 CFUmL

To evaluate the antimicrobial activity and the mini-mum inhibitory concentration (MIC) the disk diffusionmethod was used Each bacterial suspension (100 120583L fromthe 108 CFUmL) was spread on prepared agar plates (sterileStandardMethodsAgar for bacteria) Filter sterile paper discs(6mm in diameter) were impregnated with 6667 50 3333and 1667 120583L of the undiluted oil and were placed on theinoculated plates The negative control was hexane whileampicillin (10 120583g) and streptomycin (10 120583g) were used aspositive controls The plates where incubated at 37∘C (ArsaAR-130 Felisa Jalisco Mexico) for 24 hrs The diameters ofthe inhibition zones were measured in millimeters and theresults of MIC were expressed as 120583g120583L

3 Results and Discussion

31 Extraction Yield Table 2 shows the oil yields achievedby the ultrasound treatments The extraction yield variedfrom 375 to 6 and the maximum yield was obtained at thehighest amplitude level of 92 Oil yield strongly dependedon amplitude level probably because at high amplitudes thecavitation effect increases [21] and induces physical changeson the structure of the seed such as disruption of the cell wallsreduction of the particle size and increase of exposure areaThese conditions may facilitate the penetration of the solventand thus the extraction of oil [26 28 34] The maximumyield was achieved after 10min of treatment and longertimes (15min) at high amplitudes (90) did not increase oilextraction (Table 2) Albeit time is an important variable afteryield reaches a peak a longer treatment does not maximizeextraction the same was described by Zhang et al [27] forKorean pine seed who demonstrated that oil yield increasedwith time but when it reached amaximum yield equilibratedand then decreased gradually This may be attributed to aninitial complete fracture of the cell walls during the firstminutes of the cavitation effect [26 28 34]

32 Antioxidant Activity of Green Cactus Pear Seed OilExtracted by Ultrasound Due to the complexity of theoxidation processes it is advisable to performmore than onemethod to obtain the antioxidant profile of a sample [35]In order to determine the antioxidant activity of the green

4 Journal of Food Quality

Table 2 Extraction yield and antioxidant activity of green cactus pear seed oil extracted by ultrasound under different conditions

Extraction conditions Antioxidant activity

Amplitude level () Time (min) Oil yield () ABTS DPPHmg AAE100 g 120583mol TE100 g

85 10 575 plusmn 003 6615 plusmn 407 24610 plusmn 09290 5 415 plusmn 001 5598 plusmn 313 14176 plusmn 39090 15 485 plusmn 002 5993 plusmn 445 16702 plusmn 11485 10 525 plusmn 001 6812 plusmn 659 23601 plusmn 32292 10 600 plusmn 006 5584 plusmn 236 10163 plusmn 46880 5 525 plusmn 001 6607 plusmn 217 26707 plusmn 73785 10 375 plusmn 000 6837 plusmn 392 24505 plusmn 23778 10 540 plusmn 010 6599 plusmn 501 28926 plusmn 02685 17 560 plusmn 006 6578 plusmn 037 26009 plusmn 13380 15 540 plusmn 000 6691 plusmn 320 28496 plusmn 09385 10 575 plusmn 000 6773 plusmn 040 27755 plusmn 17185 10 530 plusmn 010 6744 plusmn 389 24508 plusmn 29285 3 550 plusmn 010 6763 plusmn 000 25005 plusmn 199plusmn standard deviation

Table 3 Antioxidant activity regression coefficients of the ultra-sound extraction conditions

Coefficient ABTS DPPH1205730 67562964a 24996199a

120573119894 minus3927762b minus6357459a120573119895 02724311 71702572120573119894119895 077572 18421052120573119894119894 minus3719624b minus2977102b120573119895119895 minus0826106 004258041198772adj 093 096120573119894 amplitude level 120573119895 time significance levels a119901 lt 00001 b119901 lt 0001

cactus pear seed oil two parameters were evaluated antiox-idant and scavenging capacity by ABTS and DPPH respec-tively The results and experimental design are described inTable 2 Antioxidant activity ranged from 5584 to 6837mgAAE100 g for ABTS and 10163 to 28926120583mol TE100 g forDPPH A 1198772 value closest to one or at least of 080 indicates agood fit of themodel [36]The1198772 values for ABTS andDPPHwere 093 and 096 respectively (Table 3) indicating thatthe averages obtained adjusted to the mathematical responsesurface model

33 Effect of Ultrasound Extraction Conditions on the Antiox-idant Activity of Cactus Pear Seed Oil In this study asecond-order polynomial model for predicting the antiox-idant activity of green cactus pear seed oil was obtainedby multiple linear regression analysis of the experimentaldata Table 3 shows the regression coefficients and significantprobabilities of the linear quadratic and interaction effects ofthe ultrasound conditions on the seed oil antioxidant activityBoth ABTS and DPPH values were significantly affected byamplitude level in linear term (120573119894) at 119901 lt 00001 DPPH and119901 lt 0001 ABTS respectively as well as in its quadratic term

(120573119894119894) at 119901 lt 0001 DPPH and ABTS The three-dimensionalsurface plots constructed to observe the effect of ultrasoundprocessing (Figure 1) demonstrated that antioxidant activitywas higher when the applied amplitude decreased

34 Optimization of the Ultrasound Extraction Conditions ofCactus Pear Seed Oil Optimal extraction conditions wereselected from the overlapped contour plots inwhich the effectof amplitude level and time on the antioxidant activity ofgreen cactus pear seed oil was considered

Figure 2 shows the optimal zone where the highestantioxidant activity by ABTS and DPPH was achieved Theconditions corresponded to amplitude of 78 applied for10min In this zone the values for antioxidant activity wereof 6625mg AAE100 g and 289 120583mol TE100 g for ABTS andDPPH respectively

35 Comparison between Methods

Extraction Yield and Antioxidant Activity Figure 3 comparesthe oil yields obtained by the three extraction methodsThe results revealed that the yield obtained using the opti-mized ultrasound extraction was significantly lower than theobtained with the Soxhlet and maceration procedures Thehigher oil yield obtained by Soxhlet could be attributed to theconstant and extended contact (4 to 6 hrs) of the sample withthe solvent at high temperatures in addition to the repeatedwashing cycles [37] The ultrasound yield was closer to thatof maceration method but this last one required longer time(24 hrs) as compared to 10min ultrasound treatment

The results of antioxidant activity by ABTS andDPPH areshown in Figure 4 Both parameters were significantly higherin the oil extracted by Soxhlet (5433 plusmn 084mg AAE100 gand 26660 plusmn 197 120583mol TE100 g resp) compared to theother extraction methods The ultrasound and macerationextractions exhibited similar antioxidant activity by ABTSwhile DPPH was significantly higher for the ultrasound seed

Journal of Food Quality 5

45

50

55

60

65

70

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(mg

AA

E100

g)A

ntio

xida

nt ac

tivity

(a)

50

100

150

200

250

300

350

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(120583m

ol T

E100

g)A

ntio

xida

nt ac

tivity

(b)

Figure 1 Effect of the ultrasound extraction on the antioxidant activity of green cactus pear seed oil (a) ABTS (b) DPPH

121

109

133145

157

169181

157

169

193

169

181

205

193

205

217

217

205

229

217

229

241

229

241

253

241

253

253

265

265

265

265

277

277

277

265

289

DPPH

5650

5650

557555005425

572558005875

5950

6025

6100

6175

6250

5950

6025

63256400

6175

6250

6250

6325

6475

6325

64006475

6400

6550

6475

6550

6550

6625

6625

6625

6700

6700

6700

6775

6775

6775

6700

6700

6625

6550

6475

6625

ABTS

Optimun condition

4

6

8

10

12

14

16

Tim

e (m

in)

80 82 84 86 88 90 9278Amplitude level ()

Figure 2 Optimal ultrasound extraction conditions of green cactuspear seed oil based on the highest antioxidant activity

oil Albeit the oil extracted by the Soxhlet method presentedhigher yield and antioxidant activity the ultrasound-assistedextraction may be enhanced if multiple extractions arecarried out in a time comparable to the required by theSoxhlet procedure (4ndash6 hrs)

36 Antimicrobial Activity Escherichia coli and Staphylo-coccus aureus are distributed in nature (water soil andvegetation) and are also part of the human intestinal

c

a

b

Ultrasound Soxhlet Maceration0

1

2

3

4

5

6

7

8Yi

eld

()

Figure 3 Cactus pear seed oil yield achieved by different extractionmethods abcDifferent letters mean significant differences betweenmethods (p lt 005)

b a b

b

a

c

Ultrasound Soxhlet Maceration0

255075

100125150175200225250275300

DPPH (120583mol TE100 g)ABTS (mg AAE100 g)

Figure 4 Antioxidant activity by ABTS and DPPH of cactus pearseed oil extracted by different methods abcDifferent letters meansignificant differences between methods (p lt 005)

6 Journal of Food Quality

Table 4 Antimicrobial activity of cactus pear seed oil extracted by different methods

Diameter of inhibition zone (mm)Oillowast (+) control (minus) control

Staphylococcus aureus (Gram-positive)Ultrasound 917 plusmn 029a 1889 plusmn 154 NDSoxhlet 950 plusmn 087a 1878 plusmn 164 NDMaceration 978 plusmn 069a 1811 plusmn 117 NDEscherichia coli (Gram-negative)Ultrasound 778 plusmn 019a 1556 plusmn 212 NDSoxhlet 756 plusmn 019a 1533 plusmn 265 NDMaceration 756 plusmn 038a 1400 plusmn 233 NDPseudomonas aeruginosa (Gram-negative)Ultrasound ND 1256 plusmn 038 NDSoxhlet ND 1222 plusmn 038 NDMaceration ND 1278 plusmn 038 NDlowastSeed oil 6667120583L (+) control ampicillin (disc 10 120583g Staphylococcus aureus and Escherichia coli) and streptomycin (disc 10 120583g Pseudomonas aeruginosa) (minus)control hexane ND not detected plusmn standard deviation a Same superscripts indicates that there is no significant difference (p gt 005)

microbiota [38] Pseudomonas aeruginosa besides beingpresent in the intestinalmicrobiota [39] is a bacteria found inthe soil fertilizers and water used for food production [40]and thus it can contaminate fresh or processed food whichis an indicator of inadequate sanitation or improper han-dling during food production [41] Table 4 summarizes theantimicrobial activity of green cactus pear seed oil Extractionmethod did not have a significant effect on the antimicrobialactivity against Staphylococcus aureus and Escherichia colibut the effect was lower than the positive controls Theseresults may be explained by the similar seed oil concentrationand combined action of compounds on the structure ofmicrobial cells [42 43] despite the extraction method Seedoil did not exhibit antimicrobial activity against Pseudomonasaeruginosa probably due to the oil chemical composition thetype of microorganism and the own characteristics of thebacteria [42ndash44]The antimicrobial activity of oils is generallymore effective against Gram-positive bacteria in comparisonto Gram-negative bacteria which are more resistant mainlybecause their outer membrane is less permeable [42 4345 46] The results suggest that Pseudomonas aeruginosawas more resistant than Escherichia coli probably due tothe lipopolysaccharides present in the outer membrane thatrestrict the diffusion of compounds making it less permeable[45]The resistance can also be caused by systems of exclusionpumps that eject antimicrobial compounds from the inside ofthe bacteria before they can cause damage [39 44]

37 Effect of Ultrasound on the Physical Structure Scanningelectron micrographs of the green cactus pear seeds powderbefore and after the ultrasound treatment at magnificationsfactors of 1000x and 500x are shown in Figure 5 Beforethe ultrasound treatment and despite the previous millingprocess in the control sample it was possible to identify intactstructures of the seeds cell as well as some starch granules

(Figure 5(a)) After the ultrasound treatment the cell struc-tural damage and the variations in the shape and size of theparticles were observed (Figure 5(b)) For instance starchgranules were not observed because sonication fragmentedthese particles while cavitation phenomenon disrupted thecell structures of the seeds [47 48]

4 Conclusions

This study demonstrated that response surface methodologyand a second-order polynomial model were effective tools todetermine the optimumprocessing conditions of ultrasound-assisted extraction based on the maximum values of antiox-idant activity The results demonstrated that cactus pearseed oil has good antioxidant and antimicrobial propertiesUltrasound-assisted extraction was comparable to macera-tion but a single ultrasound process yielded less oil andlower antioxidant activity than solvent extraction (Soxhlet)Ultrasound can be considered an alternative technology forthe extraction of seed oil but further research is required todetermine the uses of the seed oil and the technology withinthe food industry and the potential of several ultrasoundcycles at the optimized conditions

Conflicts of Interest

The authors declare that there are no conflicts of interest

Acknowledgments

This work was financially supported by Programa Integral deFortalecimiento Institucional (PIFI 2014-2015) The authorsacknowledge Mexican Association CoMeNTuna (HidalgoMexico) for providing the plant materials Marıa de losAngeles Ortega-Ortega participated in this research and she

Journal of Food Quality 7

(i) (ii)

A A

(a)

(i) (ii)

(b)

Figure 5 Scanning electron micrographs of green cactus pear seed powder before (a) and after (b) ultrasound treatment (i) 1000x (ii) 500xA The black circle shows a starch granule

received her Bachelorrsquos degree in nutrition in the Universi-dad Autonoma del Estado de Hidalgo Mexico (Act no 12872016)

References

[1] L Lozano ldquoEcofisiologıa de la tuna (Opuntia ficusmdashindica (L)Mill)rdquo Horticultura Argentina vol 30 no 72 pp 37ndash52 2011

[2] LMedina-Torres J A Gallegos-Infante R F Gonzalez-Laredoand N E Rocha-Guzman ldquoDrying kinetics of nopal (Opuntiaficusmdashindica) using three different methods and their effect ontheir mechanical propertiesrdquo LWTmdashFood Science and Technol-ogy vol 41 no 7 pp 1183ndash1188 2008

[3] J A Reyes-Aguero J R Aguirre-Rivera and H M HernandezldquoSystematic notes and a detailed description of Opuntia ficusindica (L)Mill (Cactaceae)rdquoAgrociencia vol 39 no 4 pp 395ndash408 2005

[4] H I Jun M N Cha E I Yang D G Choi and Y S KimldquoPhysicochemical properties and antioxidant activity of Koreancactus (Opuntia humifusa) cladodesrdquoHorticulture Environmentand Biotechnology vol 54 no 3 pp 288ndash295 2013

[5] A Rabhi H Falleh F Limam R Ksouri C Abdelly and ARaies ldquoUpshot of the ripening time on biological activitiesphenol content and fatty acid composition of Tunisian Opuntiaficus-indica fruitrdquo African Journal of Biotechnology vol 12 no40 pp 5875ndash5885 2013

[6] M Kaur A Kaur and R Sharma ldquoPharmacological actions ofOpuntia ficus indica a reviewrdquo Journal of Applied Pharmaceuti-cal Science vol 2 no 7 pp 15ndash18 2012

[7] M R Bhatt and P S Nagar ldquoEvaluation of physicochemicalproperty and fatty acid composition ofOpuntia elatior seed oilrdquoJournal of the Professional Association for Cactus Developmentvol 15 pp 13ndash19 2013

[8] M Ennouri H Fetoui E Bourret N Zeghal F Guermazi andH Attia ldquoEvaluation of some biological parameters of Opuntiaficus indica 2 Influence of seed supplemented diet on ratsrdquo Bio-resource Technology vol 97 no 16 pp 2136ndash2140 2006

[9] SAGARPA Secretarıa de Agricultura Ganaderıa DesarrolloRural Pesca y Alimentacion Pliegos de condiciones para eluso de la marca oficial Mexico calidad suprema en tuna 2005httpwwwmexicocalidadsupremaorgassetsgaleriaPC 0462005 Tunapdf

[10] M F Ramadan and J-TMorsel ldquoOil cactus pear (Opuntia ficus-indica L)rdquo Food Chemistry vol 82 no 3 pp 339ndash345 2003

[11] K El-Mostafa Y Kharrassi A Badreddine et al ldquoNopal Cactus(Opuntia ficus-indica) as a source of bioactive compounds fornutrition health and diseaserdquo Molecules vol 19 no 9 pp14879ndash14901 2014

[12] Z Ghazi M Ramdai M L Fauconnier B El Mahi and RCheikh ldquoFatty acids sterols and Vitamin E composition of seedoil of Opuntia ficus indica and Opuntia dilenii from MoroccordquoJournal of Materials and Environmental Science vol 4 no 6 pp967ndash972 2013

[13] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extrac of Laururs nobillis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

8 Journal of Food Quality

[14] A Nawirska-Olszanska A Kita A Biesiada A Sokol-Łętowska and A Z Kucharska ldquoCharacteristics of antioxidantactivity and composition of pumpkin seed oils in 12 cultivarsrdquoFood Chemistry vol 139 no 1ndash4 pp 155ndash161 2013

[15] V Cervantes-Cardoza N E Rocha-Guzman J A Gallego-Infante M Rosales-Castro L Medina-Torres and R FGonzalez-Laredo ldquoActividad antioxidante de extractos desemilla de tres variedades de manzana (Malus domestica Borkh-Rosaceae-)rdquo Boletın Latinoamericano y del Caribe de PlantasMedicinales y Aromaticas vol 9 no 6 pp 446ndash456 2010

[16] M K M Nair P Vasudevan and K Venkitanarayanan ldquoAnti-bacterial effect of black seed oil onListeriamonocytogenesrdquoFoodControl vol 16 no 5 pp 395ndash398 2005

[17] A I Hussain F Anwar S T H Sherazi and R PrzybylskildquoChemical composition antioxidant and antimicrobial activi-ties of basil (Ocimum basilicum) essential oils depends on sea-sonal variationsrdquo Food Chemistry vol 108 no 3 pp 986ndash9952008

[18] W Liu Y J Fu Y G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[19] M T Labuschagne and A Hugo ldquoOil content and fatty acidcomposition of cactus pear seed compared with cotton andgrape seedrdquo Journal of Food Biochemistry vol 34 no 1 pp 93ndash100 2010

[20] S Zine S Gharby and M El Hadek ldquoPhysicochemical char-acterization of Opuntia ficus-indica seed oil from MoroccordquoBiosciences Biotechnology Research Asia vol 10 no 1 pp 99ndash105 2013

[21] R Azuola and P Vargas ldquoExtraccion de sustancias asistida porultrasonido (EUA)rdquoTecnologıa enMarcha vol 20 no 4 pp 30ndash40 2007

[22] M Gao and C Z Liu ldquoComparison of techniques for theextraction of flavonoids fromcultured cells of SaussureamedusaMaximrdquo World Journal of Microbiology and Biotechnology vol21 no 8-9 pp 1461ndash1463 2005

[23] B Karki B P Lamsal S Jung et al ldquoEnhancing protein andsugar release from defatted soy flakes using ultrasound tech-nologyrdquo Journal of Food Engineering vol 96 no 2 pp 270ndash2782010

[24] F Adam M Abert-Vian G Peltier and F Chemat ldquolsquoSolvent-freersquo ultrasound-assisted extraction of lipids from freshmicroal-gae cells a green clean and scalable processrdquo BioresourceTechnology vol 114 pp 457ndash465 2012

[25] T Allaf V Tomao K Ruiz and F Chemat ldquoInstant controlledpressure drop technology and ultrasound assisted extraction forsequential extraction of essential oil and antioxidantsrdquo Ultra-sonics Sonochemistry vol 20 no 1 pp 239ndash246 2013

[26] Z S Zhang L J Wang D Li S S Jiao X D Chen and ZH Mao ldquoUltrasound-assisted extraction of oil from flaxseedrdquoSeparation and Purification Technology vol 62 no 1 pp 192ndash198 2008

[27] T Zhang Z Wang and X Chen ldquoUltrasound-associatedextraction of seed oil of Korean pinerdquo Journal of Forest Researchvol 16 no 2 pp 140ndash142 2005

[28] A M Goula ldquoUltrasound-assisted extraction of pomegranateseed oilmdashkinetic modelingrdquo Journal of Food Engineering vol117 no 4 pp 492ndash498 2013

[29] Q Y Zafra-Rojas N S Cruz-Cansino A Quintero-Lira etal ldquoApplication of ultrasound in a closed system optimum

condition for antioxidants extraction of blackberry (Rubusfructicosus) residuesrdquoMolecules vol 21 no 7 p 950 2016

[30] AOAC Official Methods of Analysis AOAC InternationalGaithersburg Md USA 18th edition 2005

[31] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[32] EM Kuskoski A G Asuero AM Troncoso J Mancini-Filhoand R Fett ldquoAplicacion de diversos metodos quımicos paradeterminar actividad antioxidante en pulpa de frutosrdquo Cienciae Tecnologia de Alimentos vol 25 no 4 pp 726ndash732 2005

[33] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[34] Y Tian Z Xu B Zheng and Y Martin Lo ldquoOptimization ofultrasonic-assisted extraction of pomegranate (Punica grana-tum L) seed oilrdquo Ultrasonics Sonochemistry vol 20 no 1 pp202ndash208 2013

[35] M L Agudo ldquoTecnicas para la determinacion de compuestosantioxidantes en alimentosrdquo 2010 httpwwwanpebadajozesautodidactaautodidacta archivosnumero 9 archivosl amedinapdf

[36] S K Ho C P Tan Y Y Thoo F Abas and C W HoldquoUltrasound-assisted extraction of antioxidants inMisai Kucing(Orthosiphon stamineus)rdquo Molecules vol 19 no 8 pp 12640ndash12659 2014

[37] S R Kirk R Sawyer and H Egan ldquoMetodos quımicos gen-eralesrdquo inComposicion y Analisis de Alimentos pp 25ndash29 Com-panıa editorial continental Ciudad de Mexico Mexico 2002

[38] S Vazquez S OrsquoNeill and M Legnani ldquoImportancia de loscoliformes en los alimentosrdquo 2013 httpwwwmontevideogubuysitesdefaultfilesimportancia de los coliformes en losalimentospdf

[39] C A Gomez-Alvarez A L Leal-Castro M J Perez de Gonza-lez and M L Navarrete-Jimenez ldquoMecanismos de resistenciaen Pseudomonas aeruginosa entendiendo a un peligroso ene-migordquo Revista de la Facultad de Medicina de la UniversidadNacional de Colombia vol 53 no 1 pp 27ndash34 2005

[40] S D Kominos C E Copeland B Grosiak and B Postic ldquoIntro-duction of Pseudomonas aeruginosa in to a hospital via vegeta-blesrdquo Applied Microbiology vol 24 no 4 pp 567ndash570 1972

[41] NOM Norma Oficial Mexicana NOM-210-SSA1-2014 Pro-ductos y servicios Metodos de prueba microbiologicosDeterminacion de microorganismos indicadores Determina-cion de microorganismos patogenos 2014 httpdofgobmxnota detallephpcodigo=539868ampfecha=26062015

[42] F Reyes-Jurado E Palou and A Lopez-Malo ldquoMetodos deevaluacion de la actividad antimicrobiana y de determinacionde los componentes quımicas de los aceites esencialesrdquo TemasSelectos de Ingenierıa de Alimentos vol 8 pp 68ndash78 2014

[43] D Zekaria ldquoLos aceites esenciales una alternativa a los antimi-crobianosrdquo 2015 httpwwwwpsa-aecaesaeca imgs docswpsa1182855355apdf

[44] DM Livermore ldquoMultiplemechanisms of antimicrobial resist-ance in Pseudomonas aeruginosa our worst nightmarerdquo Clini-cal Infectious Diseases vol 34 no 5 pp 634ndash640 2002

[45] M Viuda-Martos M A Mohamady J Fernandez-Lopez et alldquoIn vitro antioxidant and antibacterial activities of essentials oilsobtained from Egyptian aromatic plantsrdquo Food Control vol 22no 11 pp 1715ndash1722 2011

Journal of Food Quality 9

[46] X Feas L M Estevinho C Salinero et al ldquoTriacylglyc-eride antioxidant and antimicrobial features of virgin camelliaoleiferaC reticulata andC sasanqua oilsrdquoMolecules vol 18 no4 pp 4573ndash4587 2013

[47] R G Earnshaw ldquoUltrasound a new opportunity for foodpreservationrdquo in Ultrasound in Food Processing M J W PoveyandT JMason Eds pp 183ndash192 Editorial BlackAcademic andProfessional New York NY USA 1998

[48] M Vinatoru ldquoAn overview of the ultrasonically assisted extrac-tion of bioactive principles from herbsrdquo Ultrasonics Sonochem-istry vol 8 no 3 pp 303ndash313 2001

Research ArticleAntioxidant and Antimicrobial Properties of CactusPear (Opuntia) Seed Oils

Esther Ramiacuterez-Moreno1 Raquel Carintildeo-Corteacutes2 Nelly del Socorro Cruz-Cansino1

Luis Delgado-Olivares1 Joseacute Alberto Ariza-Ortega1 Vanessa Yelina Montantildeez-Izquierdo3

Mariacutea Manuela Hernaacutendez-Herrero3 and Tomaacutes Filardo-Kerstupp4

1Academic Area of Nutrition Health Sciences Institute Autonomous University of Hidalgo State 42160 Pachuca HGO Mexico2Academic Area of Medicine Autonomous University of Hidalgo State Eliseo Ramırez Ulloa 400 42090 Pachuca HGO Mexico3Department of Food Hygiene Faculty of Veterinary Autonomous University of Barcelona 08193 Bellaterra Spain4Academic Area of Chemistry Basic Science and Engineering Institute Autonomous University of Hidalgo StateCarretera Pachuca-Tulancingo Km 45 Mineral de la Reforma 42183 Pachuca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 23 January 2017 Accepted 5 April 2017 Published 26 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Esther Ramırez-Moreno et alThis is an open access article distributed under the Creative CommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Seed oils from two Mexican varieties of cactus pear (green Opuntia albicarpa and red Opuntia ficus indica) were extracted withdifferent solvents (hexane ethanol and ethyl acetate) to evaluate their antioxidant activity The seed oil with higher antioxidantactivitywas selected to evaluate antimicrobial activityThe fatty acid profilewas analyzed by gas chromatography-mass spectrometry(GC-MS) Oil from green cactus pear seeds obtained with ethanol and ethyl acetate exhibited higher antioxidant activity (119901 lt 005)of 323 and 316 120583mol TE20mg (p lt 005) respectively compared to red cactus pear seed oil (asymp274 and 247 120583mol TE20mgwith ethyl acetate and ethanol resp) The oil obtained with ethanol and higher antioxidant activity was used to determine theantimicrobial activity Both cactus pear oils produced a microbial inhibition zone in most of the microorganisms evaluatedparticularly Saccharomyces cerevisiae which had similar diameter (38ndash40mm) The oil fatty acids profiles of both varieties weresimilar and exhibited a high content of linoleic acid while two fatty acids (linolenic and behenic) found in red cactus pear were notobserved in the green variety

1 Introduction

A relatively untapped source of lipid and protein rawmaterialis the by-product of fruit-processing plants Millions ofpounds of fruit seeds are discarded yearly causing disposalproblems while proper utilization of these waste productscould lead to an important new source of oil and meal [1]Seeds of fruits collect at least some cytoplasmic lipid bodies asmajor storage reserve for lipid accumulation [2] Fruit seedsoils are of great interest because they are edible oils with highdegree of unsaturation antioxidant radical scavenging prop-erties [3ndash8] and a broad spectrum of antimicrobial activity[9ndash15] Therefore the oil from plants can be potentially usedby the food industry for the manufacturing of ldquonaturalrdquo orldquogreenrdquo safe foods [16] and extend shelf-life [17 18]

The oil from cactus pear seed has been found to havean appreciable amount of oil with high levels of unsaturatedfatty acids [19] with antioxidant [20 21] and antimicrobialactivity [22] as well as cardioprotective antithrombotic anti-inflammatory antiarrhythmic hypolipidemic and antihy-perglycemic effect [23 24] These properties are of interestfor the pharmaceutical and food industry However theconcentration and effectiveness of these oils may vary amongcultivars or varieties crop environmental factors (eg lighttemperature and type of soil nutrients) or methods andsolvents used for their extraction Therefore the purpose ofthis research was to determine the antioxidant and antimi-crobial activity and fatty acid profile of the oil obtained fromtwo Mexican varieties of cactus pear (Opuntia albicarpa andOpuntia ficus indica) seeds extracted with different solvents

HindawiJournal of Food QualityVolume 2017 Article ID 3075907 8 pageshttpsdoiorg10115520173075907

2 Journal of Food Quality

2 Materials and Methods

21 Plant Material Two Mexican varieties of cactus pear(Opuntia albicarpa and Opuntia ficus indica) fruit green (cvReyna) and red (cv Rojo Pelon) respectively were providedby theMexican association CoMeNTuna (ConsejoMexicanodel Nopal y la Tuna AC Actopan Hidalgo Mexico) Fruitsfree of external injuries were selected washed and manuallypeeled Cactus pear seeds were obtained after juice wasextracted stirring the pulpwith an industrial blender (38BL52LBC10 Waring Comercial USA) and passing it through aconventional strainer The seeds retained were washed in thestrainer with water until pulp residues were removed

22 Powder Seed and Oil Extraction Green cactus pear seeds(GCPS) and red cactus pear seeds (RCPS)were sun-dried andthen grounded (Cyclotec 1093 Tecator Sweden) to a 1mmdiameter mesh and stored at minus32∘C until further analysisTheseed oil was extracted as follows 25 g of powdered seeds wasmixed with 500mL of solvents with varying polarities (hex-ane ethanol and ethyl acetate) and the obtained residue wasreextracted until extraction solvents become colourless Allthe extracts were filtered through filtration paper Whatmannumber 1 and the filtered extracts were collected for furtherdrying and removal of the remaining solvent at 50∘C using arotary evaporator (BUCHI R-200 Switzerland) All extractswere placed in plastic bottles and then stored at minus20∘C untilused The oils obtained were used to further analysis

23 Free Radical Scavenging Assay The free radical scaven-ging activity was measured using 11-diphenyl-2-picrylhy-drazyl (DPPH∙) radical as described byMorales and Jimenez-Perez [25] A volume of 500 120583L of ethanolic DPPH∙ solution(74mg100mL) was added to a sample aliquot of 100 120583Lplaced in vialsThemixturewas left to sit at room temperaturefor 1 h and then was vortexed and centrifuged at 3000 rpm for10 minutesThe absorbance of the supernatant was measuredat 520 nm in amicroplate reader (PowerWave XSUV-Bioteksoftware KC Junior USA) and 120583mol of Trolox equivalentsper 20 milligram (120583mol TE20mg) of sample was obtainedOil samples with best antioxidant capacity obtained from thedifferent solvents were used for the antimicrobial analysis

24 Antimicrobial Activity Eight standard freeze-dried cul-tures of bacteria Candida albicans (ATCC 10231) Escherichiacoli O58H21 (ATCC 10536) Escherichia coli O157H7(CCUG 44857) Staphylococcus aureus (ATCC 13565) Liste-ria monocytogenes (CCUG 15526) Pseudomonas aeruginosa(ATCC 15442) Saccharomyces cerevisiae (CECT 1942) andSalmonella Typhi (CCUG 29478) were obtained in ther-mosealed vials from the Spanish Type Culture Collection(Autonomous University of Barcelona Barcelona Spain)Freeze-dried cultures were rehydrated in tryptone soy brothat 37∘C for 18 h and then were used to inoculate tryptone soyagar and malt extract agar plates all microorganisms wereincubated at 37∘CexceptCandida albicans and Saccharomycescerevisiae which were incubated at 25∘C Individual colonies

were maintained on specific agar slants stored at 4∘C andsubcultured every 15 days

Disc Diffusion Assay Antimicrobial activity of oil extractedfromGCPS andRCPSwas carried out using the disc diffusionmethod [26] Petri plates were filled with sim20mL of steriletryptone soy agar for bacteria and malt extract agar for fungiThe test cultures were swabbed on the top of the solidifiedmedia and allowed to dry for 10 minutes Serial dilutions(10ndash50 120583gmL) of the seed oil from a stock solution (1mgmL)were prepared in 20 DMSO and 10 120583L loaded onto thesterile blank discs (BBL Sensi-Disc) of 6 millimetersof diameter On the media surface the loaded disks wereplaced and left for 30 minutes at room temperature toallow compound diffusion The seed oil was serially dilutedin MuellerndashHinton broth medium and duplicate tubes ofeach dilution (10ndash100 120583gmL) were inoculated with 5 times106 cells of the test bacteria strain and culturesThe antibioticagents Sensi-Disc streptomycin ampicillin and sulfamethox-azoletrimethoprim (BBL Sensi-Disc) were used as positivecontrols at the same concentration level After plates wereincubated at 37∘C for 24 h the diameters of the inhibitionzones were recorded in millimeters Three independentrepetitions were performed and tests were made in triplicate

25 GC-MS Analysis The GC-MS analysis was performedwith a GC-MS HP-5890 (Hewlett-Packard Company PaloAlto California USA) equipped with a Flame IonizationDetector (FID) and a ZB-WAX fused silica capillary column(60m times 025mm id times 025mm film thickness) packedwith 5 phenylmethylpolysiloxane (Phenomenex TorranceCA) To obtain the methyl esters the cactus pear seed oilswere saponified and derivatized using KOH 1N (IUPAC1969) Changes in the fatty acids of the oils samples werecompared against a standard mixture of 37 components offatty acids methyl esters (FAMEs) (Food Industry FAMEsMix Restek) comprised by methyl esters with chains C40C60 C80 C100 C110 C120 C130 C140 C141 C150C151 C160 C161 C170 C171 C180 C181n9c C181n9tC182n6c C182n6t C183n6 C183n3 C200 C201n9 C202C203n6 C203n3 C204n6 C205n3 C210 C220 C221n9C222 C226n3 C230 C240 and C241n9 The samplevolume injected was of 2 120583L (split ratio 20 2) at an injectorand detector temperatures of 225 and 225∘C respectively N2was used as carrier gas at a flow rate of 12mLsdotminminus1 Fattyacids were calculated as percentage of total FAMEs

26 Statistical Analysis All values were obtained by triplicateand expressed as means plusmn standard deviations (SD) Datawere analyzed using the SPSS V15 software (SPSS InstituteInc Cary NC) An ANOVA was carried out to determinedifferences between oils extracted as well as its antimicrobialactivity that were significant at the 5 level of probability anda Tukey test was used for comparison of data

3 Results and Discussion

31 Yield Comparison between Extraction Solvents Hexaneethanol and ethyl acetate were used to extract the oil from

Journal of Food Quality 3

1183

669

1013

511

106

381

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

2

4

6

8

10

12

14

Oil

yiel

d (

)

Figure 1 Oil yields () extracted from GCPS and RCPS withhexane ethanol and ethyl acetate

cactus pear seeds The extraction yields are compared inFigure 1 which shows that the higher amount of oil () wasobtained from the green cultivar and that yield depended onthe solvent used Oil extraction with hexane was higher forboth fruit varieties (1183 for GCPS and 689 for RCPS)followed by ethanol which reached the same yield as ethylacetate for GCPS (asymp10) Ethyl acetate was the least effectivesolvent for RCPS The extraction yields were similar to thosereported (asymp7 to 11) for several varieties of Opuntia ficusindica [27ndash29] This extraction yields will vary depending onseveral factors as fruit variety harvest period maturationgeographic region percentage of oil in the seed and chemicalcompounds found in the source and by the extractionmethod[30] Researchers have determined that solvent extractioncombinedwith othermethods could increase oil yield as highpressure or supercritical fluid combined with solvent reacheda yield of 933 from tobacco seeds (Nicotiana tabacum L)while sonication and Soxhlet reached a 775 and 1372respectively [31]

32 Free Radical Scavenging Activity Solvent extraction isusually used for isolation of antioxidants the extractiondepends on the solvent selected based on the different antiox-idant compounds with varying polarity [32 33] DPPH is astable free radical that accepts an electron or hydrogen radicalto become a stable diamagnetic molecule [34 35]The DPPHassay has also been used to predict the oxidative stability ofedible oils [36 37] The antioxidant activity determined byDPPH of the oil extracted from RCPS and GCPS is shownin Figure 2 Oil from the GCPS extracted with ethanol andethyl acetate exhibited the higher antioxidant activity (119901 lt005) of 323 and 316 120583mol TE20mg extract respectivelyfollowed by RCPS oil extracted with ethyl acetate (274120583molTE20mg extract) and ethanol (247 120583mol TE20mg extract)These results demonstrate that the extraction solvent hada significant effect on the free radical scavenging capacityof the oil where the hexane had the lower values In ourstudy the green variety exhibited a higher antioxidant activityregardless of solvent Different results may depend mainly

e

d

a

c

ab

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

50

100

150

200

250

300

350

휇m

ol T

E20

mg

extr

act

Figure 2 Antioxidant activity of GCPS and RCPS oils extractedwith different solvents andashdDifferent letters above bars indicate thatsamples are significantly different (119901 lt 005)

on the content and concentration of bioactive compounds inthe oil but other factors such as solvent polarity solubilityof the extracts in different testing systems stereoselectivityof the radicals [38] and strong synergism between fattyacids [6] may affect antioxidant activities Other studies havealso reported diverse antioxidant activity among oils fromdifferent Opuntia varieties [20 39 40]

33 Antibacterial and Antifungal Activity The most recom-mended way to prevent or inhibit microbial growth in foodsis the use of food preservatives Essential oils are secondarymetabolites of plants that have wide applications in thefood flavoring and preservative industry [41] Six differentbacterium and two fungi species were used to screen theantimicrobial potential of the oils extracted from the twovarieties of cactus pear seeds Oil extracted with ethanolexhibited the highest antioxidant activity and therefore itwas used to evaluate the antibacterial and antifungal activityFigure 3 shows the results from the microbial assay wheremost microorganisms showed an inhibition zone whenexposed to GCPS and RCPS oils except Salmonella Typhiand Escherichia coli O157H7 (image not shown) From thesetwo microorganisms the first showed an inhibition zonein the presence of antibiotic agents streptomycin (S) ampi-cillin (AMP) and sulfamethoxazoletrimethoprim (STX) indiameters of 146 113 and 273mm respectively (Table 1)while Escherichia coli O157H7 was only inhibited by SXT(253mm) which agrees with other reports of multiantibi-otic resistance of E coli O157H7 due to the presence ofthe gene cluster AMR-SSuT [42] and production of beta-lactamase [43] On the other hand Saccharomyces cerevisiaewas highly inhibited (38ndash40mm) by the extracted oils butgrew in presence of the antimicrobial agents (Figure 3)Similar results were observed for Candida albicans althoughinhibition zones were smaller and similar for both oilsThese observations demonstrate that certain compounds inthe cactus pear seed oil have antimicrobial activity Otherresearchers also reported similar observations for cactus

4 Journal of Food Quality

Table 1 Diameters of growth inhibition zones (mm) in the presence of oil extracted from cactus pear seeds and conventional antimicrobialsA

Microbial cultures Extract Antimicrobial agentGCPS RCPS S AMP SXT

Saccharomyces cerevisiae (CECT1942) 383 plusmn 42a 403 plusmn 45a ND ND NDEscherichia coli O58H21 (ATCC 10536) 119 plusmn 07d 114 plusmn 09d 195 plusmn 14b 178 plusmn 15c 299 plusmn 09a

Escherichia coli O157H7 (CCUG 44857) NDB ND ND ND 253 plusmn 10Staphylococcus aureus (ATCC 13565) 121 plusmn 10c 111 plusmn 11c 183 plusmn 09b 281 plusmn 15a 333 plusmn 19a

Listeria monocytogenes (CCUG15526) 133 plusmn 15c 114 plusmn 09d 213 plusmn 12a 173 plusmn 08c 376 plusmn 18a

Pseudomonas aeruginosa (ATCC15442) 164 plusmn 21c 151 plusmn 20c 201 plusmn 15b 241 plusmn 25a 366 plusmn 29a

Salmonella typhi (CCUG29478) ND ND 146 plusmn 04b 113 plusmn 18c 273 plusmn 08a

Candida albicans (ATCC 10231) 111 plusmn 10a 110 plusmn 18a ND ND NDAInhibition zone diameters for oil and reference antibiotics are means plusmn SE of three replicas GCPS green cactus pear seed oil extract RCPS red cactus pearseed oil extract S streptomycin (10120583gdisc) AMP ampicillin (10 120583gdisc) and SXT sulfamethoxazoletrimethoprim (10120583gdisc) BND not detected activityandashdDifferent letters in the same row indicate significant differences

RG

SXT

S

AMP

(a)

RG

SXT

S

AMP

(b)

R G

SXTS

AMP

(c)

RG

SXTS

AMP

(d)

RG

SXT

S

AMP

(e)

R G

SXT

S

AMP

(f)

Figure 3 Antimicrobial activity of oil extracted from green cactus pear (G) oil extracted from red cactus pear seeds (R) streptomycin(S) ampicillin (AMP) and sulfamethoxazoletrimethoprim (SXT) Candida albicans (ATCC 10231) (a) Escherichia coli O58H21 (ATCC10536) (b) Staphylococcus aureus (ATCC 13565) (c) Listeria monocytogenes (CCUG15526) (d) Pseudomonas aeruginosa (ATCC15442) (e)Saccharomyces cerevisiae (CECT1942) (f)

pear fruit cv Opuntia stricta [44] and for other plants asfennel (Foeniculum vulgare L) and chamomile (Matricariachamomilla L) [5] Differences in the levels of antimicrobialactivity may be partially attributed to variable chemicalcomposition of the oils [45] Mnayer et al [46] suggestedthat oil compounds can act on different bacterial structureswhile Gill et al [47] mentioned that whole oils have a greater

antibacterial activity than the major component mixed sothat minor components are critical for the activity and exerta synergistic effect [16 48 49]

In the present study the antimicrobial activity of cactuspear seed oil was more effective against fungi comparedto bacteria cultures These interesting results suggest thatthere is a link between the oil chemical contents and the

Journal of Food Quality 5

Table 2 Percentages of FAMEs in crude cactus pear seed oil extracts

FAMEs Green cactus pear seed oil extract Red cactus pear seed oil extractC140 0078 plusmn 000 0066 plusmn 001C160 12327 plusmn 009 12887 plusmn 002C161 0429 plusmn 002 0570 plusmn 001C162 0073 plusmn 000 0540 plusmn 000C170 0060 plusmn 001 0075 plusmn 000C180 3436 plusmn 001 3389 plusmn 007C181 16215 plusmn 003 17061 plusmn 001C182 67448 plusmn 008 65407 plusmn 001C183 Ni 0372 plusmn 001C220 Ni 0160 plusmn 001Means of 3 replicates plusmn SE Ni not identified

140

160

181

182

18017

016

116

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(a)14

0 161

162

170

180

181

182

183

220

160

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(b)

Figure 4 Chromatograms of FAMEs of cactus pear seed oil extract (a) Green cactus pear seed oil extract (b) red cactus pear seed oil extractIn both oils extracts were identified myristic (C140) palmitic (C160) palmitoleic (C161 cis-9) hexadecadienoic (C162 cis-9 12) margaric(C170) stearic (C180) oleic (C181 cis-9) linoleic (C182 cis-9 12) except linolenic (C183 cis-6 9 12) and behenic (C220) fatty acids thatwere identified only in red cactus pear seed

antimicrobial activity The membrane disruption could beone mechanism of action by inactivating microbial adhesionenzymes and proteins transport [15 46] RCPS and GCPSextracts inhibited most of the evaluated bacterial and fungispecies (Table 1) however antimicrobial activity was notdetected for Salmonella Typhi which is a gram-negative bac-terium In general gram-negative bacteria have an effectiveoutermembrane that restricts the penetration of amphipathiccompounds and has a mechanism to extrude toxins across[50]Thismay explain the apparent antimicrobial ineffective-ness of the oils against the permeability barrier in addition tothe presence of multidrug resistance encoding plasmids [51]

34 Fatty Acid Profile FAMEs chromatograms and percent-ages are shown in Figure 4 and Table 2 Cactus pear seed oilscontained saturated and unsaturated fatty acids the linoleicfatty acid being the predominant (674 and 654 in GCPSand RCPS oils resp) Minimal amounts of myristic (C140)palmitoleic (C161) hexadecadienoic (C162) and margaric(C170) fatty acids in both oils were also identified The fattyacids profiles of the two cactus pear varieties were similarhowever theGCPS had a slightly higher content of the linoleicacid (C182)while the fatty acids linolenic (C183) and behenic(C220) were in minimal amounts only in the RCPS

Different studies have established that factors as cultivartype temperature and harvest time have a strong influence inparameter as pH Brix vitamin C sugars and fat content [5253] Oumato et al [52] found differences in linoleic fatty acid(C182) content among cactus pear cultivars In other studythe oleic acid (C181) content was significantly influenced bythe cultivar and location interaction [53] providing uniquecharacteristics to the oil

In comparison with other plants oils the linoleic acid(C182) content of the cactus pear fruit was similar to thelevels reported for sunflower oil (62) [54] and higher thanwheat germ oil (5505) [55] and soybean oil (5270)[56] The contents of other FAMEs in cactus pear varietiessuch as palmitic (C160) oleic (C181) and stearic (C180)were similar to those reported for Castilla blackberry (Rubusglaucus Benth) with 1124 passion fruit (Passiflora edulis)with 1547 [57] and grape (Vitis vinifera) with 35 [58]

Other researchers have reported similar fatty acidsprofile to our findings for different plant materials andhave analyzed the antimicrobial effectiveness against dif-ferent microorganisms For instance fatty acids found inAllium cepa were found to effectively inhibit Staphylococcusaureus Bacillus subtilis Enterococcus faecalis Escherichia coliand Klebsiella pneumoniae [59] Oil extracted from SwieteniaMacrophylla king seed oil inhibited growth of S aureus

6 Journal of Food Quality

S Typhimurium and P aeruginosa [60] These studies de-monstrate that seed oil can inhibit fungi and bacteria buttheir efficacy would depend on their concentration levels andspecific pathogen [15]

4 Conclusions

Oil yield from the green cactus pearwas higher in comparisonto the red cultivar andwas also influenced by the solvent usedHexane exhibited high extraction yield while oils extractedwith ethanol had the better antioxidant activity The resultsdemonstrated that oil extracts from both varieties have anoticeable antimicrobial activity against gram-positive andgram-negative bacteria comparable to antimicrobial com-pounds such as ampicillin streptomycin and sulfamethoxa-zoletrimethoprimThis research provides further incentivesto develop additives for the food cosmetic and pharmaceu-tical sectors seeking natural compounds with antimicrobialactivity Further studies are needed to determine the specificcomponent responsible for the antimicrobial activity in cac-tus pear seeds oil and determine the optimum levels of oilextract and the antimicrobial effectiveness in the foodmatrix

Additional Points

Practical Application Our results suggest that the oilsextracted from cactus pear seeds have the potential to be usedas a natural antioxidant and antimicrobial agents by the foodcosmetic and pharmaceutical sectors

Conflicts of Interest

The authors have declared that no conflicts of interest exist

Acknowledgments

This study was possible thanks to the financial supportfrom the Programa Integral de Fortalecimiento Institucional(PIFI 2013ndash2015) Mexico This research project was partiallysupported by the Food Hygiene Department Faculty ofVeterinary from the Autonomous University of BarcelonaSpain The authors acknowledge the Mexican associationCoMeNTuna (Consejo Mexicano del Nopal y la TunaHidalgo Mexico) for providing the plant materials

References

[1] B S Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Acids in Foods and Their Health Implications pp 263ndash301 CRC Press 3rd edition 2007

[2] D J Murphy I Hernandez-Pinzon and K Patel ldquoRole oflipid bodies and lipid-body proteins in seeds and other tissuesrdquoJournal of Plant Physiology vol 158 no 4 pp 471ndash478 2001

[3] A Kedia B Prakash P KMishra andN K Dubey ldquoAntifungaland antiaflatoxigenic properties of Cuminum cyminum (L)seed essential oil and its efficacy as a preservative in storedcommoditiesrdquo International Journal of Food Microbiology vol168-169 pp 1ndash7 2014

[4] S Singh S S Das G Singh C SchuffM P de Lampasona andC A Catalan ldquoComposition in vitro antioxidant and antimi-crobial activities of essential oil and oleoresins obtained fromblack cumin seeds (Nigella sativa L)rdquo BioMed Research Inter-national vol 2014 Article ID 918209 10 pages 2014

[5] M H H Roby M A Sarhan K A-H Selim and K I KhalelldquoAntioxidant and antimicrobial activities of essential oil andextracts of fennel (Foeniculum vulgare L) and chamomile(Matricaria chamomilla L)rdquo Industrial Crops and Products vol44 pp 437ndash445 2013

[6] G Kavoosi A Tafsiry A A Ebdam and V Rowshan ldquoEvalua-tion of antioxidant and antimicrobial activities of essential oilsfrom carum copticum seed and ferula assafoetida latexrdquo Journalof Food Science vol 78 no 2 pp T356ndashT361 2013

[7] S Lalas O Gortzi V Athanasiadis J Tsaknis and I ChinouldquoDetermination of antimicrobial activity and resistance tooxidation of Moringa peregrina seed oilrdquoMolecules vol 17 no3 pp 2330ndash2334 2012

[8] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extract of Laurus nobilis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

[9] R S Bhat and S Al-daihan ldquoAntimicrobial activity of Litchichinensis and Nephelium lappaceum aqueous seed extractsagainst some pathogenic bacterial strainsrdquo Journal of King SaudUniversitymdashScience vol 26 no 1 pp 79ndash82 2014

[10] J M Silvan E Mingo M Hidalgo S de Pascual-Teresa A VCarrascosa and A J Martinez-Rodriguez ldquoAntibacterial activ-ity of a grape seed extract and its fractions against Campylobac-ter spprdquo Food Control vol 29 no 1 pp 25ndash31 2013

[11] K Rakholiya M Kaneria D Desai and S Chanda ldquoAntimi-crobial activity of decoction extracts of residual parts (seedand peels) ofMangifera indica L var Kesar against pathogenicand food spoilage microorganismrdquo in Microbial pathogens andstrategies for combating them science technology and educationA Mendez-Vilas Ed vol 2 pp 850ndash856 2013

[12] N A Hasan M Z Nawahwi and H Ab Malek ldquoAntimicrobialactivity ofNigella sativa seed extractrdquo Sains Malaysiana vol 42no 2 pp 143ndash147 2013

[13] Z I Sajid F Anwar G Shabir G Rasul KM Alkharfy and A-H Gilani ldquoAntioxidant antimicrobial properties and phenolicsof different solvent extracts from bark leaves and seeds ofPongamia pinnata (L) pierrerdquoMolecules vol 17 no 4 pp 3917ndash3932 2012

[14] M Khoobchandani B K Ojeswi N Ganesh et al ldquoAntimicro-bial properties and analytical profile of traditional Eruca sativaseed oil comparisonwith various aerial and root plant extractsrdquoFood Chemistry vol 120 no 1 pp 217ndash224 2010

[15] V Kesari A Das and L Rangan ldquoPhysico-chemical charac-terization and antimicrobial activity from seed oil of Pongamiapinnata a potential biofuel croprdquo Biomass and Bioenergy vol34 no 1 pp 108ndash115 2010

[16] K Carovic-Stanko S Orlic O Politeo et al ldquoComposition andantibacterial activities of essential oils of seven Ocimum taxardquoFood Chemistry vol 119 no 1 pp 196ndash201 2010

[17] MM Tajkarimi S A Ibrahim andDO Cliver ldquoAntimicrobialherb and spice compounds in foodrdquo Food Control vol 21 no 9pp 1199ndash1218 2010

[18] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

Journal of Food Quality 7

[19] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[20] W Liu Y-J Fu Y-G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[21] B Matthaus and M M Ozcan ldquoHabitat effects on yield fattyacid composition and tocopherol contents of prickly pear(Opuntia ficus-indica L) seed oilsrdquo Scientia Horticulturae vol131 pp 95ndash98 2011

[22] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research vol 27 no 14 pp 1305ndash1314 2013

[23] KMobraten TMHaug C R Kleiveland and T Lea ldquoOmega-3 and omega-6 PUFAs induce the same GPR120-mediatedsignalling events but with different kinetics and intensity inCaco-2 cellsrdquo Lipids in Health and Disease vol 12 no 1 ArticleID 101 2013

[24] A BerraaouanA ZiyyatHMekhfi et al ldquoEvaluation of antidi-abetic properties of cactus pear seed oil in ratsrdquo PharmaceuticalBiology vol 52 no 10 pp 1286ndash1290 2014

[25] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[26] P R Murray E J Baron M A Pfaller F C Tenover and R HYolkeManual of Clinical Microbiology 1995 Washington DCUSA

[27] M Ennouri H Fetoui E Bourret N Zeghal and H AttialdquoEvaluation of some biological parameters of Opuntia ficusindica 1 Influence of a seed oil supplemented diet on ratsrdquoBioresource Technology vol 97 no 12 pp 1382ndash1386 2006

[28] Y Habibi L Heux M Mahrouz and M R Vignon ldquoMorpho-logical and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruitsrdquo Carbohydrate Polymers vol 72 no 1pp 102ndash112 2008

[29] MMoudenM Boujnah S Salmaoui S Zantar and A DouiraldquoEffect of two extraction methods and harvest period andperformance there statement of fatty oils of figs pear seedrdquoInternational Journal of Pure amp Applied Bioscience vol 4 no1 pp 1ndash8 2016

[30] A El Finti M Belayadi R El Boullani F Msanda and A ElMousadik ldquoAssessment of some agro-technological parametersof cactus pear fruit (Opuntia ficus-indica Mill) in Moroccocultivarsrdquo Journal of Medicinal Plants Research no 7 pp 2574ndash2583 2013

[31] S Majdi M Barzegar A Jabbari and M Agha AlikhanildquoSupercritical fluid extraction of tobacco seed oil and itscomparison with solvent extraction methodsrdquo Journal of Agri-cultural Science and Technology vol 14 no 5 pp 1043ndash10512012

[32] E M Marinova and N V Yanishlieva ldquoAntioxidative activity ofextracts from selected species of the family Lamiaceae insunflower oilrdquo Food Chemistry vol 58 no 3 pp 245ndash248 1997

[33] Y-Y Soong and P J Barlow ldquoAntioxidant activity and phenoliccontent of selected fruit seedsrdquo Food Chemistry vol 88 no 3pp 411ndash417 2004

[34] J R Soares T C P Dinis A P Cunha and L M AlmeidaldquoAntioxidant activities of some extracts of Thymus zygisrdquo FreeRadical Research vol 26 no 5 pp 469ndash478 1997

[35] I GulcinMOktay E Kirecci and O I Kufrevioglu ldquoScreeningof antioxidant and antimicrobial activities of anise (Pimpinellaanisum L) seed extractsrdquo Food Chemistry vol 83 pp 371ndash3822003

[36] J Lee H Chung P-S Chang and J Lee ldquoDevelopment of amethod predicting the oxidative stability of edible oils using 22-diphenyl-1-picrylhydrazyl (DPPH)rdquo Food Chemistry vol 103no 2 pp 662ndash669 2007

[37] A Fazio P Plastina J Meijerink R F Witkamp and BGabriele ldquoComparative analyses of seeds of wild fruits ofRubus and Sambucus species from Southern Italy fatty acidcomposition of the oil total phenolic content antioxidant andanti-inflammatory properties of the methanolic extractsrdquo FoodChemistry vol 140 no 4 pp 817ndash824 2013

[38] R L Prior X Wu and K Schaich ldquoStandardized methods forthe determination of antioxidant capacity and phenolics infoods and dietary supplementsrdquo Journal of Agricultural andFood Chemistry vol 53 no 10 pp 4290ndash4302 2005

[39] A Cardador-Martınez C Jimenez-Martınez and G SandovalldquoRevalorization of cactus pear (Opuntia spp) wastes as a sourceof antioxidantsrdquo Ciencia e Tecnologia de Alimentos vol 31 no3 pp 782ndash788 2011

[40] Z Ghazi M Ramdani M Tahri et al ldquoChemical compositionand antioxidant activity of seeds oils and fruit juicerdquo Journalof Materials and Environmental Science vol 6 no 8 pp 2338ndash2345 2015

[41] V K Bajpai K-H Baek and S C Kang ldquoControl of Salmonellain foods by using essential oils a reviewrdquo Food ResearchInternational vol 45 no 2 pp 722ndash734 2012

[42] K Ziebell R P Johnson A M Kropinski et al ldquoGenecluster conferring streptomycin sulfonamide and tetracyclineresistance in Escherichia coli O157H7 phage types 23 45 and67rdquo Applied and Environmental Microbiology vol 77 no 5 pp1900ndash1903 2011

[43] O Chandra K J Putra and I Wayan ldquoAntibiotic resistanceprofiles of Escherichia coli O157H7 in cattle at Suth-KutaBadung Regency Bali Indonesiardquo Global Veterinaria vol 15no 5 pp 480ndash484 2015

[44] E Moosazadeh M R Akhgar and A Kariminik ldquoChemicalcomposition and antimicrobial activity of Opuntia stricta Fessential oilrdquo Journal of Biodiversity and Environmental Sciencesvol 4 pp 94ndash101 2014

[45] S Burt ldquoEssential oils their antibacterial properties and poten-tial applications in foods - a reviewrdquo International Journal ofFood Microbiology vol 94 no 3 pp 223ndash253 2004

[46] D Mnayer A-S Fabiano-Tixier E Petitcolas et al ldquoChemicalcomposition antibacterial and antioxidant activities of sixessentials oils from the Alliaceae familyrdquo Molecules vol 19 no12 pp 20034ndash20053 2014

[47] A O Gill P Delaquis P Russo and R A Holley ldquoEvaluationof antilisterial action of cilantro oil on vacuum packed hamrdquoInternational Journal of FoodMicrobiology vol 73 no 1 pp 83ndash92 2002

[48] M Turgis K D Vu C Dupont and M Lacroix ldquoCombinedantimicrobial effect of essential oils and bacteriocins againstfoodborne pathogens and food spoilage bacteriardquoFoodResearchInternational vol 48 no 2 pp 696ndash702 2012

[49] H Zengin and A H Baysal ldquoAntibacterial and antioxi-dant activity of essential oil terpenes against pathogenic andspoilage-forming bacteria and cell structure-activity relation-ships evaluated by SEM microscopyrdquo Molecules vol 19 no 11pp 17773ndash17798 2014

8 Journal of Food Quality

[50] G Tegos F R Stermitz O Lomovskaya and K Lewis ldquoMul-tidrug pump inhibitors uncover remarkable activity of plantantimicrobialsrdquo Antimicrobial Agents and Chemotherapy vol46 no 10 pp 3133ndash3141 2002

[51] M Baltazar A Ngandjio K E Holt et al ldquoMultidrug-resistantSalmonella enterica serotype typhi Gulf of Guinea RegionAfricardquo Emerging Infectious Diseases vol 21 no 4 pp 655ndash6592015

[52] J Oumato S ZriraM Boujnah andB Saidi ldquoEffect ofmaturitystage onmorphological and chemical characteristics ofOpuntiaficus indica from Moroccordquo International Journal of Innovationand Applied Studies vol 20 no 1 pp 400ndash410 2017

[53] M deWit A Hugo N Shongwe and R van derMerwe ldquoEffectof cultivar season and locality on lipid content and fatty acidcomposition of cactus pear seed oilrdquo South African Journal ofPlant and Soil no 33 pp 279ndash288 2016

[54] Australian Oilseeds Federation Incorporated 2015 Section 1ldquoQuality standards technical information amp typical analysisrdquono 14 pp 31ndash40 2016 (Accessed 1 November 2015)

[55] A Awad A Adel A A M Nady and AAE ldquoWheat germ anoverview on nutritional value antioxidant potential andantibacterial characteristicsrdquo Food and Nutrition Sciences vol6 no 2 pp 265ndash277 2015

[56] P Pumrojana S Terapuntuwat and P Pakdee ldquoInfluence offatty acid composition of soybean oil vs beef tallow on egg yolkfatty acid profiles of laying hensrdquo Pakistan Journal of Nutritionvol 14 no 7 pp 383ndash387 2015

[57] A F Ceron M O Osorio and B A Hurtado ldquoIdentificacionde acidos grasos contenidos en los aceites extraıdos a partir desemillas de tres diferentes especies de frutasrdquo Acta Agronomicavol 61 no 2 pp 126ndash132 2012

[58] J Orsavova L Misurcova J Vavra Ambrozova R Vicha andJ Mlcek ldquoFatty acids composition of vegetable oils and itscontribution to dietary energy intake and dependence of car-diovascular mortality on dietary intake of fatty acidsrdquo Interna-tional Journal of Molecular Sciences vol 16 no 6 pp 12871ndash12890 2015

[59] M Derbali A Elaissi I Cheraief and M Aouni ldquoFatty acidcomposition and antimicrobial activity against sensitive andmulti-drug resistant bacteria of Tunisian Allium cepa seedextractrdquo Research amp Reviews Journal of Hospital and ClinicalPharmacy vol 2 no 2 pp 30ndash34 2016

[60] M B Suliman A H Nour M M Yusoff P Kuppusamy A RYuvaraj and S A Mazza ldquoFatty acid composition and antibac-terial activity of Swietenia macrophylla king seed oilrdquo AfricanJournal of Plant Science vol 7 no 7 pp 300ndash303 2013

Page 4: Natural Preservatives to Improve Food Quality and Safety

Copyright copy 2017 Hindawi All rights reserved

This is a special issue published in ldquoJournal of Food Qualityrdquo All articles are open access articles distributed under the Creative Com-mons Attribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Editorial Board

Encarna Aguayo SpainRiccarda Antiochia ItalyJorge Barros-Velaacutezquez SpainJoseacute A Beltraacuten SpainAacute A Carbonell-Barrachina SpainMarina Carcea ItalyMaria Rosaria Corbo ItalyEgidio De Benedetto ItalyAlessandra Del Caro ItalyAntimo Di Maro Italy

Rossella Di Monaco ItalyHuumlseyin Erten TurkeySusana Fiszman SpainAndrea Galimberti ItalyEfstathios Giaouris GreeceVicente M Goacutemez-Loacutepez SpainElena Gonzaacutelez-Fandos SpainAlejandro Hernaacutendez SpainJesuacutes Lozano SpainSara Panseri Italy

Mariacutea B Peacuterez-Gago SpainWitoon Prinyawiwatkul USAEduardo Pueacutertolas SpainJuan E Rivera MexicoFlora V Romeo ItalyJordi Rovira SpainAmy Simonne USAGiuseppe Zeppa Italy

Contents

Natural Preservatives to Improve Food Quality and SafetyMoreno Bondi Andrea Laukovaacute Simona de Niederhausern Patrizia Messi and Chrissanthy PapadopoulouVolume 2017 Article ID 1090932 3 pages

Natural Food Additives and Preservatives for Fish-Paste Products A Review of the Past Present andFuture States of ResearchKhawaja Muhammad Imran Bashir Jin-Soo Kim Jeong Hyeon An Jae Hak Sohn and Jae-Suk ChoiVolume 2017 Article ID 9675469 31 pages

Development of a Chemically Defined Medium for Better Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31Wenli Liu Lanwei Zhang and Huaxi YiVolume 2017 Article ID 9017452 8 pages

Lipid Oxidation Color Changes and Microbiological Quality of Frozen Beef Burgers Incorporatedwith ShiraziThyme Cinnamon and Rosemary ExtractsHadi Hashemi Gahruie Seyed Mohammad Hashem HosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan ShadVolume 2017 Article ID 6350156 9 pages

Optimization of Ultrasound Extraction of Cactus Pear (Opuntia ficus indica) Seed Oil Based onAntioxidant Activity and Evaluation of Its Antimicrobial ActivityMariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-Cansino Ernesto Alaniacutes-GarciacuteaLuis Delgado-Olivares Joseacute Alberto Ariza-Ortega Esther Ramiacuterez-Morenoand Joseacute de Jesuacutes Manriacutequez-TorresVolume 2017 Article ID 9315360 9 pages

Antioxidant and Antimicrobial Properties of Cactus Pear (Opuntia) Seed OilsEsther Ramiacuterez-Moreno Raquel Carintildeo-Corteacutes Nelly del Socorro Cruz-Cansino Luis Delgado-OlivaresJoseacute Alberto Ariza-Ortega Vanessa Yelina Montantildeez-Izquierdo Mariacutea Manuela Hernaacutendez-Herreroand Tomaacutes Filardo-KerstuppVolume 2017 Article ID 3075907 8 pages

EditorialNatural Preservatives to Improve Food Quality and Safety

Moreno Bondi1 Andrea Laukovaacute2 Simona de Niederhausern1

Patrizia Messi1 and Chrissanthy Papadopoulou3

1Department of Life Sciences University of Modena and Reggio Emilia Via G Campi 287 Modena Italy2Institute of Animal Physiology Slovak Academy of Sciences Soltesovej 4-6 040 01 Kosice Slovakia3Microbiology Department Faculty of Medicine School of Health Sciences University of Ioannina Ioannina Greece

Correspondence should be addressed to Moreno Bondi morenobondiunimoreit

Received 12 October 2017 Accepted 12 October 2017 Published 12 December 2017

Copyright copy 2017 Moreno Bondi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Food products can be contaminated by a variety of path-ogenic and spoilage microbiota the former causing food-borne diseases and the latter causing significant economiclosses for the food industry due to undesirable effects onthe food properties According to the Centers for DiseaseControl and Prevention (CDC) each year in the UnitedStates 48 million people get sick 128000 are hospitalizedand 3000 die because of foodborne infections Howeveralthough foodborne outbreaks are well recorded sporadiccases are not because not all patients visit the doctor orenter the hospital and the causative agent is not alwaysidentified A considerable number of foodborne pathogens ofgreat public health importance (eg VTEC E coli serotypesCampylobacter jejuni Listeria monocytogenes and Yersiniaenterocolitica) have emerged during the recent two decadescausing severe illness and foodborne outbreaks worldwide

Microbial food spoilage is also an area of immenseconcern for the food industry It is estimated that as much as25 of all food produced is lost after harvest due to microbialactivity While the growth of spoilage microbiota in foodsis not harmful for the human health it has negative impacton the shelf-life textural characteristics and overall qualityof the finished products affects the consumer choices andresults in significant commercial losses Thus prevention orinhibition of microbial growth in foods is of outmost impor-tance for the current globalized food production Hencethere is still the need for new processing methods to be usedeither alone or in combination with the already existing onesable to reduce or eliminate foodborne pathogens and spoilagebacteria

Chemical additives have been extensively used to preventthe survival and proliferation of microorganisms but their

safety and impact on human health are under discussionSince the reduction or elimination of pathogens and spoilagemicroorganisms in food is the foremost priority the currenttrends in food processing are focusing on the use of naturalcompounds which are considered as safe alternatives andsatisfy the consumer preferences for more ldquogreen foodsrdquoHence the increased awareness on the safety of food additivesand preservatives and the consumerrsquos trend to avoid foodscontaining chemicals which in the long-term may haveadverse impact on their health have generated a significantnumber of studies and publications on the potential useof various natural substances recognized as GRAS (Gener-ally Recognized as Safe) to be used as food preservativesChemical compounds added to foods as antioxidant agentsare also of concern particularly when important proteinsources (eg burgers steaks) are involved in the daily diet ofwesternized consumer living in the developed countries [1 2]Synthetic antioxidants such as BHT TBHQ and BHA havedemonstrated various adverse effects on the human healthincluding allergy headache asthma and dermatitis Recentstudies on the utilization of natural antioxidants (eg herbalessential oils and extracts) indicate their capacity and safety[3 4] Also the antimicrobial properties of natural substancessuch as plant essential oils and extracts have been extensivelystudied with promising results [5] The proper recycling anduse of fruit-processing plants by-products like fruit seedsor skins discarded and piling up in huge amounts everyyear are of great interest for the food industry particularlytheir potential to be a useful source of oil and meal [6]Additionally the oil from plant seeds can be used by thefood industry for manufacturing more ldquonaturalrdquo or ldquogreenrdquofoods and also can sufficiently extend the shelf-life of the

HindawiJournal of Food QualityVolume 2017 Article ID 1090932 3 pageshttpsdoiorg10115520171090932

2 Journal of Food Quality

food product [7] The oils derived from fruit seeds oils mayalso have some more useful properties beyond being justldquoediblerdquoThe oil derived from the seed extract of twoMexicanvarieties of cactus pear (Opuntia albicarpa and Opuntia ficusindica) has been found to have sufficient antioxidant andantimicrobial properties [8] Furthermore some biologicalactive compounds produced by microorganisms are widelyused in the food industry as well A good alternative toconventional chemically synthesized food preservatives is theuse of natural antimicrobials such as bacteriocins producedby lactic acid bacteria (LAB) with Nisin being officiallyemployed by the food industry and thus the most widelyused Bacteriocins are peptides actually microbial toxinsproduced from various microorganisms and so far someof them (eg enterocins produced mostly by enterococci)have shown remarkable antimicrobial potential and theirapplication as a natural barrier against pathogens and foodspoilage has been proven to be very efficient when used inthe form of purified or semipurified extracts or as protectivecultures [9 10] Therefore as the developments in foodpreservation are focusing on the implementation of naturalantimicrobials and antioxidants this special issue exploresthe potential of alternatives to currently used preserva-tives through the publication of five high-quality articleswhich aim to address recent advancements in the field ofnatural food preservatives and antioxidants The prospectto replace synthetic preservatives with natural substanceshas been demonstrated by comparing the effects of Shirazithyme cinnamon and rosemary extracts (denoted as naturalantioxidants) with those of the synthetic antioxidant BHT onprotein and lipid oxidations physicochemical microbial andsensory characteristics of frozen beef burgers during storageSpecifically the oxidative stability of the beef burgers contain-ing Shirazi thyme cinnamon and rosemary extracts was welldemonstrated and the antibacterial activitywas documentedas the total microbial counts of the tested burgers were wellbelow the maximum allowed limit Besides the evaluationof the antimicrobial and antioxidant properties of naturalsubstances it is important to optimize their recovery Withregard to bacteriocins to enhance Enterocin Y31 productionand simplify the steps of separation and purification a propersimplified and defined medium (SDM) has been developedfor the Enterococcus faecium Y31 growth and enhancementof the Enterocin Y31 production The bacterial growth didnot result in Enterocin Y31 production in MRS medium andtherefore both the growth rate and the EnterocinY31 produc-tion were set as the goal for the investigation Single omissionexperiments revealed that 5 gL NaCl five vitamins twonucleic acid bases MgSO4sdot7H2O MnSO4sdot4H2O KH2PO4K2HPO4 CH3COONa fourteen amino acids and glucosewere essential for the adequate strain growth and EnterocinY31 production As a result a novel simplified and definedmedium (SDM) was formulated containing 30 ingredientsin which the Enterocin Y31 production yield was higherwhen compared to either MRS or CDM The developmentof the SDM improved the Enterocin Y31 production andsimplified the steps of purification (only two steps) whichis very promising and increases its potential applicationsReferring to seedsrsquo oils the optimization of the extraction

conditions of cactus pear seed oil has been obtained usingultrasound in a closed system based on the antioxidantactivity and using response surface methodology The yieldextraction and antioxidant and antimicrobial activity werecompared with those obtained using both conventional andunconventional methods such as Soxhlet and macerationusing heat agitation or long extraction times microwavesupercritical fluids and ultrasound-assisted extraction inan open and in a closed system The results have shownthat ultrasound exhibited lower oil yield and antioxidantactivity but had the potential to achieve comparable resultsif multiple ultrasound extractions are performed in the timeneeded by conventional methods Seed oils showed similarantimicrobial activity despite the extraction method and canbe an alternative extraction method of seed oils from fruitssuch as cactus pear Lastly the replacement of chemicaladditives with natural compounds has been addressed for fishfoods as well Fish-paste products also known as fish cakes orsurimi-based products are worldwide favorites Surimi a wetprotein concentrate of fish muscle is used as an intermediateraw material to produce surimi seafood The flavor texturetaste shelf-life and market value of surimi-based productsdepend on several factors including the additives used toprepare the surimi While preparing surimi with chemicaladditives several problems have been observed such as alack of unique characteristics inferior acceptability and poorfunctionality In this context a systematic review of fish-paste products prepared using natural food additives (eganimal seafood and plant source additives herbs and orientalmedicines grains and roots and functional food materials)has been performed which summarizes the existing relevantknowledge in the production of new value-added foodstuffsof interest for the surimi industry

In conclusion this special issue offers to the readers thechance to be informed on the recent advancements relatedto the antimicrobial and antioxidant properties of naturalsubstances that are of interest for the contemporary foodindustry Their prospective use in the food production hasthe potential to lead towards the production of safer andhealthier foods not excluding their contribution to a moreefficient preservation of the environment when chemicalswill be replaced with natural substances

Moreno BondiAndrea Laukova

Simona de NiederhausernPatrizia Messi

Chrissanthy Papadopoulou

References

[1] G Comi E Tirloni D AndyantoMManzano and L IacuminldquoUse of bio-protective cultures to improve the shelf-life andthe sensorial characteristics of commercial hamburgersrdquo LWT -Food Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[2] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWT - FoodScience and Technology vol 68 pp 385ndash390 2016

Journal of Food Quality 3

[3] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[4] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[5] H Sakkas P Gousia V Economou V Sakkas S Petsios and CPapadopoulou ldquoIn vitro antimicrobial activity of five essentialoils on multidrug resistant Gram-negative clinical isolatesrdquoJournal of Intercultural Ethnopharmacology vol 5 no 3 pp212ndash218 2016

[6] B Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Fatty Acids in Foods and their Health ImplicationsThirdEdition vol 20073230 of Food Science and Technology pp 263ndash301 CRC Press 3rd Edition edition 2007

[7] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

[8] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research (Formerly Natural Product Letters)vol 27 no 14 pp 1305ndash1314 2013

[9] R Iseppi F Pilati M Marini et al ldquoAnti-listerial activity of apolymeric film coated with hybrid coatings doped with Ente-rocin 416K1 for use as bioactive food packagingrdquo InternationalJournal of Food Microbiology vol 123 no 3 pp 281ndash287 2008

[10] A Laukova and P Turek ldquoEffect of enterocin 4231 in Slovak fer-mented salami puchov after its experimental inoculation withListeria Innocua Lirdquo ACTA Scientiarum Polonorum TechnologiaAlimentaria vol 10 no 4 pp 423ndash431 2011

Review ArticleNatural Food Additives and Preservatives forFish-Paste Products A Review of the Past Present andFuture States of Research

Khawaja Muhammad Imran Bashir1 Jin-Soo Kim2 Jeong Hyeon An1

Jae Hak Sohn13 and Jae-Suk Choi13

1Seafood Research Center IACF Silla University 606 Advanced Seafood Processing Complex Wonyang-roAmnam-dong Seo-gu Busan 49277 Republic of Korea2Department of Seafood and Aquaculture Science Gyeongsang National University 38 Cheondaegukchi-gilTongyeong-si Gyeongsangnam-do 53064 Republic of Korea3Food Biotechnology Division of Bioindustry College of Medical and Life Sciences Silla University 140 Baegyang-daero700 beon-gil Sasang-gu Busan 46958 Republic of Korea

Correspondence should be addressed to Jae-Suk Choi jsc1008sillaackr

Received 9 June 2017 Revised 15 August 2017 Accepted 17 September 2017 Published 27 November 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Khawaja Muhammad Imran Bashir et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Fish-paste products also known as fish cakes or surimi-based products are worldwide favorites Surimi a wet protein concentrateof fish muscle is used as an intermediate raw material to produce surimi seafood The flavor texture taste shelf-life and marketvalue of surimi-based products depend on the source of the fish meat type of applied heat treatment and additives used toprepare the surimi While preparing surimi with chemical additives several problems have been observed such as a lack of uniquecharacteristics inferior acceptability and poor functionality Various types of fish-paste products have been developed by usingdifferent ingredients (eg vegetables seafood herbs and oriental medicines grains and roots including carrots and functionalfood materials) However a systematic review of fish-paste products prepared using natural food additives has not yet beenperformedTherefore the quality characteristics of fish-paste products and their functionalities were elucidated in this study Withthe increasing demand for surimi seafood products the functional properties physiochemical properties and shelf-life of surimi-based products need to be improved This review will aid the preparation of new value-added products in the surimi industry

1 Introduction

Fish-paste products popularly known as fish cakes areproduced from frozen surimi (ie they are a kind of surimi-based product) and are popular in Korea and Japan [1] Inthe Korean Food Standards Codex fish cakes are known asa processed marine product comprising salt-soluble proteinsisolated from fish meat [2] Fish muscle is mechanicallydeboned washed with water and blended with cryoprotec-tants to prepare a wet concentrate of proteins called surimiSurimi is a Japanese term that is also known as washed fishmince It is a refined fish myofibrillar protein manufacturedthrough numerous step-by-step processes including headinggutting filleting deboning (mincing) washing dewatering

refining mixing with cryoprotectants freezing and metaldetection for HACCP [3] The myofibrillar proteins make itan excellent ingredient for developing food products It hasexcellent gelling properties and forms strong and elastic gelsupon heating [4]

The setting and deformation are important to preparesurimi and surimi-based products Setting also known asldquosuwarirdquo in Japanese is a very important process which hasa significant influence on the physiological and rheologicalproperties of surimi-based products Setting is a vital processin the quality estimation of surimi because it helps to improvethe water-holding capacity as well as the gel texture of surimi-based productsWhen fishmince paste (sol) is heated at a lowtemperature (up to 50∘C) a loose network (suwari) is formed

HindawiJournal of Food QualityVolume 2017 Article ID 9675469 31 pageshttpsdoiorg10115520179675469

2 Journal of Food Quality

from myosin and actomyosin molecules this process isreferred to as setting Setting is species dependent and occursover a range of temperatures (up to 50∘C) and to a varyingextent As the temperature is increased to around 70∘Csuwari is partially disrupted to form a broken net structure(modori) a phenomenon attributed to the dissociation ofmyosin from actin and the possible fragmentation of the actinfilament [5ndash7]

Most of the surimi-based products are different types offish-paste products while less than 10 include fish burgersfish ham and fish sausages [3] Surimi-based products areprepared by mixing the raw or frozen surimi with saltsand other ingredients molded and heated to form the finalproduct in the specified shape and texture and pasteurizedbefore packaging The kind of heat treatment depends on theflavor texture and appearance of the desired final productand may include broiling steaming deep-fat frying andboiling [8] while fish-paste products in South Korea aremostly prepared by frying [9] Textural characteristics suchas gel strength are the major determinant of surimi priceand quality [10] Several studies have attempted to enhancethe textural quality of surimi or surimi-based products usingvarious protein additives [11ndash14]

Surimi quality and gelling property are mainly affectedby both intrinsic factors (effect of fish species seasonalitysexual maturity and freshness or rigor) and extrinsic fac-tors (harvesting handling water characteristics processingtime and temperature solubilization of myofibrillar proteinsduring processing the activity of the endogenous or addedprotein oxidants and proteolytic enzymes washing cyclessalinity and pH) [3 134] Surimi forms thermoirreversiblegels upon heating which do not deform with further changein the temperature This phenomenon of surimi and surimi-based products is similar to that observed in other proteinssuch as egg white milk-lactoglobulin and wheat glutenAdditionally surimi produces gels of very high deformabilityand strength This heat-induced gelation property of surimimakes it a very valuable food ingredient [134]

The gel-forming ability and capacity of surimi areadversely affected by the proteolytic degradation of myofib-rillar proteinsThe presence of indigenous proteinases causedgel softening in surimi made from fish species for examplethreadfin bream [135] arrow tooth flounder [136] Pacificwhiting [137] and lizard fish and bigeye snapper [20 59]Various active proteinases in fish muscle are responsible forsoftening of the surimi gels Nakamura and Ogawa and Anet al testified that cathepsins L and B were the most activecysteine proteinases in Pacific whiting surimi and fish filletsrespectively [7 138] The myofibril-associated proteinasesobserved in lizardfish surimi were serine proteinases andcysteine while a serine proteinase was reported in the bigeyesnapper surimi [20 59]

Seasonal analysis of the compositional properties ofAlaska pollock and Pacific whiting showed higher proteincontents in winter while the moisture contents were higherin summer [139 140] Surimi prepared from cold-water fishspecies with low thermostability of myofibrillar proteinsmakes setting easier Normally a myofibrillar protein withlow thermostability is optimum to do setting because its

reactivity is increased due to the loose internal structure bysodium chloride addition and heat denaturation In contrastthe myofibrillar protein of tropical fish species with high heatstability is difficult to denature and form the myofibrillarprotein network structure in surimi [3]

Several research groups have studied ways to enhance thequality of surimi-based products by investigating the changesin microbial content enzyme activity nutrient content andacceptability characteristics the use of raw materials thestandardization of the manufacturing process storage andmarketing Natural and chemical food-grade additives suchas konjac flour proteinase inhibitors egg white and hydro-colloids have been used to enhance the gelling properties ofsurimi [12 17 20 23 34 141ndash143] The trypsin inhibitor inegg white plays a major role in improving the gel strengthof surimi The addition of egg white inhibits the proteolyticactivity of the modori-inducing enzyme in fish meat andsuppresses the decrease of elasticity in surimi Serum pro-teins have strong inhibiting abilities against the action ofvarious proteases with different active centers such as SHgroups and serine groups In addition they also containtransglutaminases that accelerate the setting Egg white andserum proteins also play an important role in inhibiting theenzymatic activity of the parasites Apart from the use ofadditives gel strengthening can be achieved by treating thegels at low temperatures (0ndash40∘C) before cooking [144 145]Furthermore the gel quality of surimi and surimi-basedproducts can also be enhanced by using alternate fish speciesor by acid and alkali washing to increase the myofibrillarprotein concentrations [7 146 147]

Surimi production worldwide reached around800000MT by 2011-2012 [3] while South Korea alonecontributed approx 156000MT in 2013 Over the yearsthe size of the market for Korean fish-paste products hasgradually increased reaching sim350 million US dollars in2013 (based on the amount produced) [148] Howevermanufacturers have had several problems in producingsurimi-based products such as a lack of unique character-istics and inferior acceptability and functionality Thereforethere have been several attempts to develop new fish-pasteproducts with excellent acceptability and functionalityTo this end numerous types of fish-paste products havebeen developed using various natural ingredients such asvegetables seafood animals plants herbs and orientalmedicines seaweed and functional food materials It is ofworldwide interest to use these natural food preservativesinstead of chemical or synthetic ones However to date nosystematic review of fish-paste products supplemented withvarious food raw materials has been performed Thereforethe quality characteristics of fish-paste products and theirfunctionalities were elucidated in this study

2 Improvement of the Gel Properties ofFish-Paste Products

Various food additives derived from animals (eg beefswine and chicken) seafood (eg fish invertebrates) plants(eg legumes cereals) sugars polyols and functional mate-rials used in fish-paste products to improve their gelling

Journal of Food Quality 3

capabilities and strength are listed in Table 1 and describedbelow

21 Animal Source Additives Various food-grade proteaseinhibitors from animal sources are used to enhance thephysical properties of surimi-based products as well to pre-vent the protein degradation The ability of beef plasma andother food-grade additives in surimi and fishmince preparedfrom Pacific whiting (Merluccius productus) was studied byMorrissey et al [12] The strongest proteolytic inhibitionwas observed with beef plasma protein at a concentrationas low as 1 Reppond and Babbitt reported the increase ingel strength of gels prepared by arrow tooth flounder at aconcentration of 2 with a yellow hue color [16] Weeras-inghe et al characterized the inhibitory activity of these food-grade inhibitors and reported that the inhibitory activity wasmainly because of specific serine proteinase inhibitors [17]The addition of 2 dried bovine plasma to steamed fish-pasteslightly increased the chewiness and hardness but it showeda negative effect on the gel strength [18] Duangmal andTaluengphol reported that the higher levels of beef plasmaprotein unfavorably affected gel characteristics of red tilapiasurimi gels [19]

The effect of porcine plasmaprotein on the bigeye snapper(Priacanthus tayenus) surimi gel characteristics was investi-gated by Benjakul et al [14]The gels supplemented with 05porcine plasma protein had the highest level of deformationand breaking force Benjakul and colleagues later reportedthe effect of porcine plasma protein on the gel characteristicsof surimi from bigeye croaker (Pennahia macrophthalmus)bigeye snapper (P tayenus) barracuda (Sphyraena jello)and threadfin bream (Nemipterus bleekeri) [20] The porcineplasma protein was effective in increasing the deformationand breaking force of kamaboko gels Higher breaking forcesand levels of deformation occurred when chicken plasmaprotein was supplemented to sardine kamaboko gels at levelsup to 2 [21] The inhibitory activities of cysteine proteinaseinhibitor fraction from chicken plasma on Pacific whitingand arrow tooth flounder mince were reported by Rawdkuenet al [22] Furthermore similar results were observed intheir extended study onPacificwhiting surimi where chickenplasma at a level of 2 inhibited the degradation of myosinheavy chain proteins [23]

Ovomucoid is a mucoprotein obtained from egg whitethat has been tested for its potential as a gel-degradationinhibitor [24 25] The addition of 2 ovomucoid couldincrease the breaking strength and gel deformation [28]The autolytic activities of lizardfish (Saurida tumbil) surimiand mince under the application of protease inhibitors wereinvestigated by Yongsawatdigul and Piyadhammaviboon[26] At all preincubation conditions egg white enhancedthe gel-forming capability of S tumbil surimi to a greaterextent than did whey protein concentrateThe addition of 1egg white and preincubation at 25∘C increased the breakingforce by twofold Campo-Deano and Tovar [27] reportedthat the addition of egg albumen at 15 and 2 for Alaskapollock and Pacific whiting surimi respectively enhancedthe gel strength of crab sticks According to Hunt et al theincorporation of 2-3 special dried egg white improved

the gel textural characteristics of Alaska pollock and Pacificwhiting surimi [28]

Whey is the complete set of proteins isolated fromthe watery portion of milk Whey protein is comprisedof 20 milk protein and 80 casein [149] Whey proteinconcentrates have generally been used as an emulsifierfiller water binder protein supplement foam stabilizer andthickener as well as gelling agent [150] Rawdkuen andBenjakul investigated the effect of whey protein concentrateon the gelling characteristics of surimi prepared fromgoatfish(Mulloidichthys vanicolensis) bigeye snapper (P tayenus)lizardfish (S tumbil) and threadfin bream (N bleekeri) [29]All the tested surimi supplemented with 3 whey proteinconcentrate displayed inhibitory activity against autolysis andsignificantly reduced gel whiteness However better water-holding capacity was obtained by increasing concentrationsof whey protein concentrate

Plasma proteins produced from pig cow and chickenbyproducts are relatively affordable and easily collectiblesources [143 151 152] However outbreaks of foot-and-mouthdisease avian influenza andmad cow disease as well as a banonproteins frompig bone and skin in some states for religiouscauses have made it essential to search alternative sources[153 154] Various fish plasma proteins have been testedincluding those from rainbow trout and salmon [31 35 36]

22 Seafood Additives The effects of shrimp head proteinhydrolysate fromdifferent shrimp namely black tiger shrimp(Penaeus monodon) northern pink shrimp (Pandalus eous)and endeavour shrimp (Metapenaeus endeavouri) on thegelling properties of lizardfish (Saurida spp) surimi wereinvestigated by Ruttanapornvareesakul et al [30] It wasreported that the freeze-induced denaturation of lizardfishmuscle protein could be reduced by the supplementation ofshrimp head protein hydrolysate at a concentration of 5resulting in higher Ca-ATPase activity and gel strength Theeffects of rainbow trout plasma proteins on the gelling prop-erties of surimi prepared by Alaska pollock were investigatedby Li et al [31] Gel degradation deformation the breakingforce water-holding capacity and whiteness enhanced withincreasing amounts of rainbow trout plasma protein anddecreased at higher concentrationsThe rainbow trout plasmaprotein at a concentration of 075mgg could be used asa potential protease inhibitor to inhibit gel weakening inAlaska pollock surimi Li et al reported the higher inhibitoryactivities of the recombinant chum salmon cystatin againstautolysis of Alaska pollock surimi [155]

Fish gelatin is extracted from the collagen of fish skinand it is used as a food additive Hernandez-Briones et alstudied the functional and mechanical properties of Alaskapollock surimi gels while using fish gelatin as an additive[32] The increasing concentration of gelatin affected thewhiteness but the sensory panelists were unable to detect itThese results showed that fish gelatin was not effective as afunctional additive in Alaska pollock surimi Nevertheless itcould be added at up to 10 gkg without negatively affectingthe mechanical properties of surimi Yin et al reported asignificant improvement in the endogenous transglutaminaseactivity of Alaska pollock surimi prepared with nanoscaled

4 Journal of Food Quality

Table1Naturalfood

additiv

esused

toim

provethe

gelpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Animalsource

additiv

es

Beefplasma

hydrolysate

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Atlanticmenhaden

(Brevoortia

tyrann

us)

Alaskap

ollock

(Theragra

chalcogram

ma)

Moistu

recontentproteincontent

cook

inglossw

ater-holding

capacitytexturetorsio

ntest

05

ndash15

[15]

Bovine

plasma

Bostaurus

Heatedin

awater

bath

Powder

Arrow

toothflo

under

(Atheresthessto

mias)

Walleye

pollo

ck

Moistu

recontentpu

nchtorsion

colortest

2[16]

Beefplasma

protein

Bostaurus

mdashPo

wder

Pacific

whitin

g(M

erlucciusp

rodu

ctus)

Proteincontentinhibitory

assay

4[17]

Drie

dbo

vine

plasma

Bostaurus

Steaming

Powder

Alaskap

ollock

(Tchalco

gram

ma)

Nutrie

ntcontentpH

water-holding

capacitytexture

and

sensoryevaluatio

n2

[18]

Beefplasma

protein

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Redtilapia

(Oniloticus

xO

placidus)

Colortextureexpressiblewater

protein

totalsulfhydrylcon

tent

2gkg

[19]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Bigeye

snapper

(Pria

canthu

stayenus)

Expressib

ledrip

amou

ntcolor

texturesetting

cond

ition

s05

[14]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Threadfin

bream

(Nem

ipterus

bleekeri)Bigeyes

napp

er(Ptayenus)

Baracuda

(Sphyraena

jello)and

Bigeye

croaker

(Penna

hiamacrophthalmus)

Trichloroacetic

acid-solub

lepeptidescolortextureprotein

content

05

[20]

Chickenplasma

protein

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Sardine

(Sardinella

gibbosa)

Colortextureexpressiblemoistu

re

proteincontentautolysis

activ

ity2

[21]

Cyste

inep

roteinase

inhibitorfrom

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Arrow

toothflo

under

(Astomias)Pacific

whitin

g(M

produ

ctus)

Autolysis

andinhibitory

activ

ity

pHprotein

content

3[22]

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Pacific

whitin

g(M

produ

ctus)

Torsionandfracture

test

dynamic

rheologicalattribute

2[23]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[24]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[25]

Eggwhite(EW)

Gallusgallusd

omesticus

Heatedin

awater

bath

Powder

Lizardfish(Saurid

atumbil)

mince

andsurim

iAu

tolytic

activ

itytexturalattributes

EW1

[26]

Eggalbu

min

Gallusgallusd

omesticus

Heatedin

thec

ooking

roller

Eggwhite

itself

Surim

i-based

crab

sticksfrom

Alaskap

ollock

(AP)

Pacific

whitin

g(PW)

(Mprodu

ctus)

Transie

nttest

streng

thtest

texture

dynamicrheologicaland

physical

attributes

AP

15

PW2

[27]

Journal of Food Quality 5

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Regu

lard

riedegg

white(REW

)speciald

riedegg

white(SEW

)liq

uideggwhite

(LEW

)

Gallusgallusd

omesticus

Heatedin

awater

bath

Spray-dried

powder

Pacific

whitin

g(M

produ

ctus)

Totalsulfhydrylgroup

sfracture

test

dynamicrheologicalattribute

SEW2-3

[28]

Wheyprotein

concentrate

Bostaurus

Heatedin

awater

bath

Wheyprotein

concentrate

Bigeye

snapper(Ptayenu

s)Goatfish

(Mulloidich

thys

vanicolen

sis)

Threadfin

bream

(Nblee

keri)

and

Lizardfish(Stum

bil)

Water-holding

capacitycolor

autolytic

activ

ity3

[29]

Seafoo

dadditiv

esSh

rimphead

proteinhydrolysate

from

northern

pink

shrim

pendeavou

rshrim

pand

blacktig

ershrim

p

Pand

alus

eous

Metapenaeus

endeavouri

Pena

eusm

onodon

Heatedin

awater

bath

Drie

dmatter

Lizardfish

(Saurid

aspp)

Gelstr

engthcolorgel-forming

abilityC

a-AT

Pase

activ

ity5

[30]

Rainbo

wtro

utplasmap

rotein

Oncorhynchu

smykiss

Heatedin

awater

bath

Freeze-drie

dplasma

Alaskap

ollock

Proxim

atea

nalysisw

ater-holding

capacitycolortextureprotein

content

075

mgg

[31]

Fish

gelatin

Com

mercialfishgelatin

(Gelatin

Rousselot)

Heatedin

awater

bath

Powder

Alaskap

ollock

Colorm

echanicalfunctio

nal

sensoryattributes

10gkg

[32]

Nanoscaled

fish-bo

neof

Pacific

whitin

gMprodu

ctus

Heatedin

awater

bath

Powder

Alaskap

ollock

Texturescanning

electron

microscop

y1g10

0g[33]

Nanoscaled

fish-bo

ne(N

FB)+

driedeggwhite

(DEW

)

Mprodu

ctusGallus

gallu

sdom

esticus

Heatedin

awater

bath

Powder

Pacific

whitin

g(M

produ

ctus)

Rheologicaland

texturalattributes

DEW

1+

10mgNFB

Cag

surim

ipaste

[34]

Salm

onbloo

dplasma

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)

Scanning

electronmicroscop

yproteincontentdynamic

rheologicalattributes

1g10

0g[35]

6 Journal of Food QualityTa

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Freeze-drie

dchinoo

ksalm

onplasma(

FSP)

and

concentrate

salm

onplasma

(CSP

)

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)surim

iand

Salm

onmince

Proteolytic

inhibitio

nautolysis

proteincontent

Salm

onminceC

SPgt

FSP

Pacific

whitin

gsurim

iFSP

[36]

Partially

purifi

edtrypsin

inhibitor

from

ther

oeof

yello

wfin

tuna

fish

Thun

nusa

lbacares

Heatedin

awater

bath

Freeze-drie

dBigeye

snapper

(Pria

canthu

smacracanthu

s)Proteolysis

colorw

ater-holding

capacitygellin

gprop

ertie

s3g

100g

[37]

Squidink

tyrosin

ase(SIT)

+tann

icacid

(TA)

Todarodesp

acificus

Heatedin

awater

bath

Mixture

Sardine

(Sardinella

albella)

Tyrosin

asea

ctivityinvitro

oxidationassaycolortexturaland

sensoryattributes

SIT

500U

gprotein+

TA1

[38]

Plantsou

rcea

dditives

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soybean

protein

Wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[39]

Soyprotein

eggwhite(EW)

wheyprotein

concentrate

(WPC

)La

ctalbumin

(LA)

milk

proteiniso

late

(MPI)

Glycinem

ax

Gallusgallusd

omesticus

Bostaurus

Coo

kedin

aste

amcooker

Powder

AlaskaP

ollock

(Tchalco

gram

ma)

Textureexpressib

lemoistu

recontentwater

retentionprop

ertie

sEW

andMPI

[4041]

Legu

mes

eed

extractfrom

blackcowpea

whitecowpea

soybeanseeds

Mun

gbean

peanut

Vignaun

guicu

lata

Glycinem

axVignaradiata

Arachish

ypogaea

mdash

Freeze-drie

dproteinase

inhibitor

extracts

Threadfin

bream

(Nem

ipterid

ae)

ThermalstabilitypHprotein

contentproteinase

inhibitory

assay

Blackcowpea

soybeanseeds

30mgg

[42]

Legu

mes

eed

extractfrom

Cow

pea

pigeon

pea

bambara

grou

ndnu

ts

Vignaun

guicu

lata

Cajanu

scajan

Vo

andzeia

subterranea

mdashPartially

purifi

edTrypsin

Threadfin

bream

(Nem

ipterid

ae)

Sarcop

lasm

icmod

ori-ind

ucing

proteinase

activ

itycolor

30ku

nits

g[43]

bambara

grou

ndnu

tprotein

isolate

Vignasubterranea

Heatedin

awater

bath

Powder

Threadfin

bream

(Nblee

keri)

Colorautolysis

025

g100g

[44]

Soyproteiniso

late

Glycinem

axHeatedin

awater

bath

Com

mercial

soyprotein

isolate

(JinQ

ui1200)

Alaskap

ollock

(Tchalco

gram

ma)

Com

mon

carp

(Cyprin

uscarpio)

Totaln

itrogen

andmoistu

recontentgelstre

ngthcolor

10

[45]

Journal of Food Quality 7Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soyprotein

wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[46]

Dietary

fiber

(DF)

from

peaa

ndchicory+

microbial

transglutaminase

(MTG

ase)

Cichorium

intybu

sPisum

sativ

umHeatedin

awater

bath

Powder

Hake(Mcapensis)

Gilthead

seabream

(Sparusa

urata)

Seab

ass(Dice

ntrarchu

slabrax)

Meagre(Argyrosomus

regius)

Dyn

amicrheologicalattributes

MTG

ase100U

g[47]

Proteiniso

lates

from

Mun

gbean

(MBP

I)black

bean

(BBP

I)bam

bara

grou

ndnu

t(BG

PI)

Phaseolusa

ureus

Phaseolusv

ulgarisV

igna

subterranea

mdashFreeze-drie

dpo

wder

mdash

Scanning

electronmicroscop

yproteolytic

autolyticandtrypsin

inhibitory

activ

ityassaycolor

texturetrichloroacetic

acid-solub

lepeptidec

ontent

1g10

0g[48]

Partially

purifi

edtrypsin

inhibitor

from

adzukibean

Vignaangularis

Heatedin

awater

bath

Freeze-drie

dpo

wder

Threadfin

bream

(Nblee

keri)

Proteincontenttexturecolor

trypsin

inhibitory

activ

ityautolytic

activ

ityassay

3g10

0g[49]

Amylose(A)a

ndam

ylop

ectin

(AP)

mdashHeatedin

awater

bath

Powder

Walleye

pollo

ck(T

chalcogram

ma)

Gelationandbreaking

strength

Amylose70+

Amylop

ectin

4

[50]

Wheatsta

rch

Triticum

aestivum

Heatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Com

pressio

ntest

dynamic

viscoelasticityscann

ingele

ctron

microscop

y

Starch10g

+Surim

i10g

[51]

Natives

weetp

otato

starch(N

SPS)

and

Mod

ified

sweet

potato

starch

(MSP

S)

Ipom

oeabatatas

Heatedon

acontrolled

stress

rheometer

Powder

Alaskap

ollock

(T

chalcogram

ma)

Dyn

amicrheologicalattributes

5[52]

Potato

starch

Solanu

mtuberosum

Heatedin

the

Krehalon

ecasin

gfilm

Powder

Pacific

sand

lance(Am

modytes

personatus

Gira

rd)

Proxim

atea

nalysis

protein

compo

sition

colorfoldingtext

texturalandsensoryattributes

8[53]

Rice

flour

Oryza

sativa

Fried

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorrheologicaland

sensoryattributes

10ndash15

[54]

Rice

flour

Oryza

sativa

Fried

Powder

Threadfin

bream

(Nem

ipterid

ae)

Moistu

recontentpH

color

texturalandsensoryattributes

50

[55]

Rice

flour

Oryza

sativa

Fried

Powder

Goldenthreadfin

bream

(Nem

ipterusv

irgatus)

Gelstr

engthsensoryattributes

14

[56]

Cryoprotectantsa

ndhu

mectants

Xanthan(X)

locustbean

(LB)

gumsa

loneX

LB

ratio

Ceratoniasiliqua

Heatedin

awater

bath

Powder

Silver

carp

(Hypophthalm

ichthys

molitrix)

Torsiontest

gel-formingability

mechanicalattributes

XLB

025075

[57]

Pectin

gum

(HM

LM)+

CaCl2

mdashHeatedin

awater

bath

Gum

and

powder

Silver

carp

(Hm

olitrix)

Water-holding

capacitym

echanical

andtexturalattributes

Pectin

gum1+

CaCl202

[58]

8 Journal of Food Quality

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Chito

san7B

from

praw

nshell

Not

mentio

ned

Heatedin

awater

bath

Not

mentio

ned

Barred

garfish

(Hem

iramphus

far)

ProteincontentSE

Mtextural

attributes

1[59]

Konjac

glucom

annan

aqueou

sdisp

ersio

nAm

orphophallu

skonjac

Heatedin

awater

bath

Aqueou

sdispersio

n

Giant

squid(D

osidicu

sgigas)

Alaskap

ollock

(T

chalcogram

ma)

ProteinsolubilitypH

texturaland

viscoelasticrheologicalattributes

1[60]

Carrageenan+

NaC

lorK

Clmdash

Heatedin

awater

bath

Hydrocollo

idAlaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorcompressio

ntest

Carrageenan1+

KCl15

[61]

Amorphophallu

skonjac

flour

(AKF

)Am

orphophallu

skonjac

Heatedin

awater

bath

Flou

rGiant

squid(D

gigas)

Water

retentionabilitycolor

texturalandsensoryattributes

10

[62]

NaC

l+high

hydrostatic

pressure

(HHP)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Proxim

atea

nalysis

FTIR

SEM

colormechanicalrheologicaland

sensoryattributes

HHP

300MPa

+NaC

l03

[63]

Sodium

chlorid

esugarspolyols

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Larim

ichthys

polya

ctis)

Water

activ

ityV

BNcolor

moistu

recontent

Sodium

chlorid

e4

Glucose10

Glycerin

10

[64]

Starchglycine

sodium

lactate

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Lpolya

ctis)

Water

activ

ityV

BNcolorm

oistu

recontent

Sodium

lactate75

[65]

Glycerol

mdashSteamed

Liqu

idMackerel(Scom

berjaponicu

s)andBrazilian

sand

perch

(Pseud

opercis

semifa

sciata)

Water

activ

itytexturaland

sensory

attributes

20

[66]

Naa

ndCa

salts

ofpo

lyuron

ides

and

carboxym

ethyl

cellu

lose

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gel-

streng

theningeffects

2ndash6

[67]

L-ascorbicacid

(AsA

)and

dehydro-L-

ascorbicacid

(DAs

A)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthanalysis

DAsA

10120583

gg

[68]

Sodium

-L-

ascorbate

(SA)

mdash

Steamed

inNojax

cellu

lose

casin

g

Powder

Alaskap

ollock

(T

chalcogram

ma)

pHtexturaland

sensoryattributes

02

[69]

120596-3

fatty

acids

from

algae

Not

mentio

ned

Heatedin

awater

bath

Oil

Cod

(Gadus

morhu

a)TB

ARS

fattyacid

contentcolor

500m

g85

g[70]

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)

Microscop

icob

servation

viscosity

gel-formingability

10

[71]

Journal of Food Quality 9Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)Th

readfin

bream

(Nem

ipterid

ae)White

croaker(Ge

nyonem

uslin

eatus)

andJapanese

jack

mackerel(Trachu

rus

japonicus)

Proxim

atea

nalysis

color

water-holding

capacityphysic

alattributes

5ndash30

[72]

120596-3

PUFA

s-ric

hoils

Flaxseedalgae

menhaden

krillblend

(flaxseed

algae

krill

811)

Heatedin

awater

bath

Oil

Alaskap

ollock

(T

chalcogram

ma)

Torsiontest

andrheological

attributes

9g10

0g[73]

Ethano

licKiam

woo

dextract

(EKW

E)+

commercialtann

in(C

T)

Hopea

sp

Heatedin

awater

bath

Overdrie

dpo

wder

Strip

edcatfish

(Pangasiu

shypophthalmus)

pHV

BNT

BARS

color

TCA-

solublep

eptid

emoistu

re

proteincontents

texturalattributes

EKWE

008

CT002

ndash004

[74]

Cocon

uthu

skextractw

ithethano

l60(C

HE-E6

0)

80(C

HE-E8

0)

Cocosn

ucifera

Heatedin

awater

bath

Freeze-drie

dpo

wder

Sardine

(Salbella)

Totalpheno

licexpressible

moistu

reT

CA-solub

lepeptideand

proteincontents

colortextual

rheologicalandsensoryattributes

CHE-E6

00125

[75]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Solutio

nMackerel

(Rastre

lligerk

anagurta)

SEMexpressiblemoistu

reprotein

contentcolortexturalandsensory

attributes

OFA

040

OTA

050

OCF

050

OCT

010

[76]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Bigeye

snapper

(Ptayenus)

SEMexpressiblemoistu

reprotein

andfre

eaminoacid

contentcolor

texturalandsensoryattributes

OFA

020

OTA

005

OCF

015

OCT

005

[77]

Eggwhitepo

wder

(EW)whey

protein

concentrate(WPC

)

Gallusgallusd

omesticus

Triticum

aestivum

Heatedin

awater

bath

Powdera

ndconcentrate

Lizardfish

(Stum

bil)mince

andsurim

i

Autolytic

activ

ityT

CA-solub

leoligop

eptid

esprotein

content

texturalattributes

EW4

WPC

4

[26]

Zinc

sulfate

(ZnS

O4)sodium

tripolypho

sphate

(STP

P)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Yello

wstr

ipetrevally

(Sela

roideslep

tolep

is)

Expressib

lemoistu

relipid

phosph

olipidand

proteincontent

Ca-ATP

asea

ctivitycolortextural

attributes

ZnSO460120583

molkg+

STPP

05

[78]

SEMscann

ingelectro

nmicroscop

yFT

IRFou

rier-transfo

rminfrared

spectro

scop

yVBN

volatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stancesT

CAtric

hloroacetic

acid

10 Journal of Food Quality

fish bones [33] Furthermore a study on the rheologicaland textural attributes of Pacific whiting surimi showedthat slow heating and the addition of nanoscaled fish bonessignificantly enhanced gel strength [34]

Fowler and Park reported an enhanced gelling strengthand effectively inhibited proteinase activity in Pacific whitingsurimi gels heated ohmically [35] Fowler and Park laterstudied the effects of salmon plasma from Chinook salmonon proteolytic inhibition of surimi [36] Salmon plasmaeffectively inhibited both serine and cysteine proteases as wellas proteases isolated from Pacific whiting Salmon plasmaconcentrated by ultrafiltration performed slightly better thanfreeze-dried salmon plasma at inhibiting autolysis in salmonmince

Klomklao et al reported inhibitory activity of a par-tially purified trypsin inhibitor (TIYTR) from yellowfintuna (Thunnus albacores) on the gelling characteristics ofbigeye snapper (Priacanthus macracanthus) surimi [37] Theincorporation of TIYTR with a level of 30 g100 g resultedin the enhanced deformation and breaking force of surimigels suggesting that the TIYTR could be employed as anaffordable and alternative proteinase inhibitor to enhance thegel strength of surimi prepared by bigeye snapper

Vate and Benjakul investigated the effects of squid inktyrosinase mixtures of tannic acid and protein on the gellingcharacteristics of sardine surimi [38] The highest deforma-tion and breaking force were obtained when surimi gels wereallowed to react for 90min while being supplemented with1 tannic acid and 500Ug squid ink tyrosinase proteinHowever gels with an added squid ink tyrosinasetannicacid mixture were whiter than the control The surimi gelssupplemented with squid ink tyrosinasetannic acid mixtureshowed the maximum overall acceptance scores suggestingthat it could be used as an additive to increase the surimi gelproperties

23 Plant Source Additives The chicken plasma proteinegg white and beef plasma protein are considered as themost effective protease inhibitors for surimi [17 22 23156] However the use of chicken plasma and beef plasmaprotein has been forbidden because of the occurrence of avianinfluenza and mad cow disease respectively In additionhigher concentrations of beef plasma proteins have also beenassociated with off-flavors while egg white is expensive andhas an unwanted egg-like odor [29 156] Additionally veg-etarians would not want to consume surimi-based productsprepared with additives from animal or even seafood sourcesTherefore alternate food-grade additives are still desired toenhance the gel strength of surimi without affecting thecustomer demandVarious natural additives derived from theplant sources have been briefly described below

231 Legumes Theeffects of vegetable protein contentmois-ture heating and setting conditions on the physical attributesof kamaboko were examined by Yamashita [39] A firm gelwas obtained at 60∘C for kamaboko with soybean proteinand at 80∘C with wheat gluten When the kamaboko gelswere supplemented with 5 vegetable protein the changes injelly strength softness and expressiblewater of the kamaboko

with wheat gluten were somewhat greater than those of thekamaboko with soybean protein According to the results ofChung and Lee the addition of plant proteins including soyprotein isolate lactoalbumin and wheat gluten remarkablylessened the strength of non-animal protein-incorporatedsurimi gels [40] The textural and sensory attributes offiberized surimi gel products were categorized as an increasein overall textural desirability and an increase in gel strengthIn another study egg white and milk protein isolate showedhigher water retention ability than whey protein concentratesoy protein isolate and lactoalbumin [41]

Protein isolates from legume seeds can be used as alter-nate protein additives for the quality improvement of surimigels Legume seed isolates comprise trypsin inhibitors andhave been used as the protease inhibitor in the prepara-tion of surimi and surimi-based products [42 43] Ben-jakul et al reported higher protease inhibitory activities ofinhibitor extracts from soybean and black cowpea seeds[42] A reduced gel-degradation activity (modori) and ahigh thermal stability were reported In another study theyreported inhibitory effects of proteinase inhibitor extractsfrom Bambara groundnuts (Voandzeia subterranea) pigeonpea (Cajanus cajan) and cowpea (Vigna unguiculata) onautolysis and gel-degradation activity (modori) of threadfinbream surimi [43] The whiteness of surimi gels reducedslightly with the addition of proteinase inhibitor Similarresults were obtained by Oujifard and colleagues [44] TheBambara groundnut protein extracts at a level of 025 g100 gshowed improved autolytic inhibition deformation andbreaking force in surimi prepared by threadfin bream (Nbleekeri) [44] However a slight reduction in whiteness wasobserved at increasing levels of Bambara groundnut proteinisolates These studies show that the addition of Bambaragroundnut protein extracts at a suitable level could serve asan alternative food inhibitor to enhance the gelling propertiesof surimi

Plant protein isolates mainly soy protein isolates havebeen used in the surimi industry because of their safety andrational price [45] Luo et al indicated the legumin andvicilin two main legume seed storage proteins as bindersand cogelling agents in surimi gels [45] Protease inhibitorsisolated from legume seeds not only can help to reduce thegel-degradation process in surimi but can also improve thesurimi gel properties by acting as filler or binder Luo etal reported higher breaking force and quality characteristicsof silver carp surimi when supplemented at a ratio of 10soy protein isolate [46] Cardoso et al studied the effects ofdietary fiber and microbial transglutaminase from chicoryand pea on the rheological properties of protein paste fromgilthead sea bream hake meagre and seabass [47] It wasfound that a high degree of protein denaturation boosted gelhardness while a low degree of protein denaturation createdgels with high deformability It shows that the addition ofmicrobial transglutaminase could serve as a possible additivefor gels of those species having lesser protein unfoldingability

Kudre et al studied the effects of black bean (Phaseolusvulgaris) and mung bean (Phaseolus aureus) protein isolateson gelling properties and proteolysis of sardines (Sardinella

Journal of Food Quality 11

albella) surimi [48] An increase in deformation breakingforce and water-holding capacity as well as a lower levelof degradation was observed while the whiteness of kam-aboko gels reduced slightly Therefore mung bean or blackbean protein isolates could be effectively used to retardthe proteolysis in sardine surimi leading to improved gelstrength Klomklao and Benjakul studied the effects of thepartially purified trypsin inhibitor from adzuki bean on thegelling properties and proteolysis of threadfin bream (Nbleekeri) surimi [49] An increase in autolysis and inhibitoryactivity against sarcoplasmic proteinases aswell as an increasein deformation and breaking force of kamaboko gel wasobserved at increasing levels of trypsin inhibitor while gelwhiteness decreased slightly

232 Starch Starch is widely used to make fish-paste prod-ucts as it enhances elasticity and increases the weight ofthe products In attempts to control thermal stability stick-iness andor wetness under different serving and storageconditions the functional characteristics of surimi seafoodproducts have been widely studied using modified starchesStarch is the second most abundantly used ingredient in themanufacturing of fish-paste products because of its higherwater-holding ability and capacity to replace fish proteinspartially while preserving the desired gel features at a reducedcost [69 157ndash161]

Kim et al reported a positive correlation between theamount of added starch and the quality of the food products[162] Konoo et al studied the effects of adding starch andamylose to amylopectin contents of starch on the gela-tion properties of frozen walleye pollack surimi [50] Thebreaking strength of gel was not affected by the changein amylose amylopectin ratio However it increased as thecontent of amylose increased in pregelatinized starch [51]A lower packing effect was observed at 90∘C which hypoth-esized that the gelatinization of starch in fish meat can beprevented at this temperature A strong correlation betweenthe amylose to amylopectin contents and the textural andrheological properties of starch-containing surimi gels wasalso reported by Lanier et al [134]

The addition of normal and modified potato or sweetpotato starch resulted in reductions in the characteristicstorage modulus of surimi sols during heating [52] Surimigels supplemented with potato starch showed the highestfirmness and cohesiveness Yoo reported the best texturalproperties of the sand lance (Ammodytes personatus) fish-paste products at a level of 8 potato starch [53] Thesestudies show that potato or sweet potato starch can also beused as a potent food additive for the production of surimi

233 RiceRice Flour Fish meat and wheat flour are themajor ingredients used for the production of surimi-basedproducts Rice flour however can be an important ingredientto enhance the rheological properties of surimi-based prod-ucts Several attempts have been made to evaluate the poten-tial of rice flour as an alternate of wheat flour in the prepara-tion of surimi products [41] The effect of rice flour additionmethods and milling types on the sensory and rheologicalattributes of surimi products were studied by Cho et al [54]

Roll-mil rice at a concentration of 10ndash15 displayed highergel strength and sensory properties which show that roll-millrice had strong potential for replacing wheat flourThe surimiproducts containing rice flour showed similar rheological andsensory characteristics to those of a finest commercial surimiproduct Hence rice flour might be an effective alternative towheat flour for high-quality surimi products

To replace wheat flour Kwon and Lee examined thequality characteristics of fried fish cakes containing rice flour[55] The total content of corn starch and rice flour was2883 of the total content of fish cake doughThere were nonoteworthy differences in the pHmoisture level appearancecolor flavor taste and overall acceptance as compared tothe control group The addition of 50 rice flour to surimi-based products could be an effective way to increase thecontent of rice flour without decreasing texture acceptabilityYoon et al optimized the content of water and rice flourin surimi-based products [56] The surimi-based productsmanufactured under optimal environment were comparablein gel strength to the commercial products However highersensory evaluation scores were observed compared to thoseof the commercial products These studies advocate that therice flour not only can be employed as an alternative to wheatflour but can also be used to enhance the quality of surimiand surimi-based products

234 Potato Powder The food additives extracted frompotato and potato protease inhibitors used in the preparationof fish-paste products are discussed in Sections 21 232 and244

24 Cryoprotectants and Humectants To inhibit denatura-tion and to lessen the damage of gel quality during coldstorage cryoprotectants are usually added to surimi productsPolyunsaturated fatty acids protein additives polyols sugarsamino acids salts and plant extracts are frequently usedas cryoprotectants and humectants to avoid fluctuationsin myofibrillar proteins promoted by freezing storage orthawing [163] Mechanical properties of surimi gels can beimproved by the addition of numerous hydrocolloids such askonjac carrageenan locust bean xanthan gum and differentmicrobial transglutaminases during the preparation of surimiproducts [57 164ndash166] In contrast the addition of alginateshas been reported to weaken surimi gels [69]

241 Saccharides Xanthan is a nongelling polysaccharideproduced by the aerobic fermentation of Xanthomonascampestris [167] The property of xanthan to form highlyviscous and stable solution at low levels makes it acceptablein the food industry [168] Xanthan displays quite remarkablesynergistic interactions with other nongelling polysaccha-rides of the galactomannan family leading to increases in gelformation and viscosity [168 169] The three commerciallyavailable galactomannans are tara gum locust bean gum andguar gum

The impact of low methoxyl pectin on the mechanicalproperties of silver carp surimi gels was studied by Barreraet al [58] An increase in hardness shear stress and water-holding capacity of the surimi gel was observed while no

12 Journal of Food Quality

significant improvement in the mechanical properties wasobserved as compared to the control Benjakul et al reportedthe effects of prawn-shell chitosan on surimi prepared bybarred garfish (Hemiramphus far) [59] Prawn-shell chitosanat a level of 1 of the surimi gel showed an increase in gel-enhancing effect on the heat-induced gelation of myofib-rillar proteins The addition of microbial transglutaminasegenerally increases the deformation and breaking force ofsurimi gel However this effect was significantly retardedin the presence of prawn-shell chitosan resulting in lowermagnitudes of deformation and breaking force

The viscoelastic properties and the thermal stability oflow-grade squid (Dosidicus gigas) surimi were investigated byIglesias-Otero et al [60] The konjac glucomannan aqueousdispersion at a level of 1 expressed the best rheologicalproperties suggesting that the konjac glucomannan aqueousdispersion may be used to enhance the quality characteristicsof low-grade squid surimi gel Ramırez et al evaluated theeffect of protein-hydrochlorides on the gel-forming ability ofmyofibrillar proteins [142] The xanthanlocust bean gum ata ratio of 025075 showed a positive improvement in themechanical attributes of surimi gels Eom et al investigatedthe impact of carrageenan on the gelation property of salt-based Alaska pollock surimi [61] The addition of 15KCl rather than 2 NaCl significantly enhanced the gellingproperty of 120581-carrageenan-induced surimi gel and showedincreased gel strength breaking force and whiteness values

242 Salts Salts help in protein-protein interaction and theaddition of salt is critical during the processing of fish-pasteproducts However the high levels of sodium in foods andconsequently human consumption of sodium have becomea global issue The prime harmful effects of excess sodiumintake are hypertension and increased blood pressure Sub-sequently these conditions lead to cardiovascular diseasesincluding instances of stroke heart attack and relateddiseases as well as gastric cancer and osteoporosis [170ndash172] Therefore to reduce sodium intake levels in fish-pasteproducts Hwang et al prepared the sodium-reduced friedfish cakes containing potassium as a substitute for sodium [1]The quality characteristics of 30 sodium-reduced fried fishcakes were not notably different from those of full-sodiumfried fish cakes however the addition of potassium changedthe color and reduced consumer acceptance To increase theconsumer preference for sodium-reduced fried fish cakes theuse of different food additives might be advantageous

The weak gel-forming ability and the strong fishy smellof the giant squid (D gigas) make it undesirable for themanufacturing of surimi-based products To overcome theseproblems Choi and Kim used Amorphophallus konjac flourto enhance the quality characteristics of giant-squid surimiproducts [62]The increasing levels ofA konjac flour showedincreases in gel texture and water retention ability while areduction in color and taste was observed as compared tothe commercial surimi products The incorporation of theseasoning ingredients such as sweeteners might be helpfulin removing the fishy smell of D gigas ultimately improvingthe gel properties of giant-squid surimi Cando et al reportedthat the sensory and mechanical properties of surimi gels

with reduced-NaCl contents can be improved by the appli-cation of 300Mpa high hydrostatic pressures [63] The gelsmade with lower-NaCl contents revealed stronger and stablenetworks as showed by the ones with higher-NaCl contents

243 Water Activity It has been reported that humectantshad the greatest effect on lowering water activity (119886

119908) with

the efficiency of the reduction in 119886119908value decreasing in the

order of NaCl sodium lactate glycerin propylene glycoland sorbitol when each of them was combined with otherhumectants [173] Kim and Park reported the impact ofhumectants such as sodium chloride sugars and polyols tolower the water activity (119886

119908) of various model kamaboko gels

[64]The effect of sodium chloride on lowering water activity(119886119908) was the highest among all of the examined treatments

while glucose caused browning reaction on the surface ofkamaboko In another study they examined the effect ofstarch glycine and sodium lactate in lowering the wateractivity (119886

119908) of model kamaboko gels [65] Sanchez Pascua et

al reported that glycerol (15ndash50) was effective in reducingthe water activity (119886

119908) in Brazilian sand perch (Pseudopercis

semifasciata) and mackerel (Scomber japonicus marplatensis)[66] Among the tested humectants the efficiency of thereduction in water activity (119886

119908) was observed decreasing in

the order of sodium lactate glycine and starch

244 Polyuronides The effect of sodium and calcium salts ofcarboxymethyl and polyuronides cellulose on the strength-ening of kamaboko gels was investigated by Niwa et al [67]It was reported that the calcium salts of pectinic acid pecticacid alginic acid and carboxymethyl cellulose enhancedthe breaking force of Alaska pollock surimi whereas theirsodium salts except Na-pectinate failed to increase the break-ing force The increase in the breaking force induced by cal-cium carboxymethyl cellulose vanished upon increasing thedegree of substitution of hydroxyl groups to carboxymethylgroups Furthermore fine cellulose particles enhanced thebreaking strain and breaking force and reduced the amount ofexpressible water but were unsuccessful in the case of coarserparticlesThe addition of potato starch can increase the effec-tiveness even in the presence of coarse particles of cellulose

245 Ascorbic Acid The addition of dehydro-L-ascorbicacid and L-ascorbic acid to Alaska pollock surimi increasedthe gel strength [68] It was suggested that the positiveeffect of L-ascorbic acid on gel formation might be due tothe oxidation of sulfhydryl groups in fish proteins Lee etal studied the effects of sodium-L-ascorbate on the gel-forming abilities of surimi prepared by Alaska pollock [69]Sodium-L-ascorbate remarkably enhanced the gel firmnesscohesiveness strength and sensory properties of the fiber-ized products at a level of 02 It directly influenced thesurimi quality regardless of vacuum treatment indicatingthat airborne oxygen was not important Freeze-syneresisstimulated by ascorbate during frozen storage was lessenedby the application of hydroxypropylated-modified starch

246 Unsaturated Fatty Acids The addition of nutritionallybeneficial 120596-3 fatty acids during surimi preparation could

Journal of Food Quality 13

enhance the gel strength and stability [70] For the effectiveuse of highly unsaturated fatty acids such as docosahexaenoicacid (DHA) and eicosapentaenoic acid (EPA) in surimi-basedproducts Okazaki et al studied the gel-forming properties offrozen walleye pollock surimi containing DHA and EPA [71]They reported that to achieve a good quality product thevigorous agitation of surimi with fish oil is essential to allowthe heat-induced gelation of its emulsified product throughthe formation of fine oil droplets

Fukushima et al investigated changes in the physi-cal properties of heat-treated surimi gels prepared fromthreadfin breamwalleye pollock Japanese jackmackerel andwhite croaker [72] The breaking strain breaking strengthand water-holding capacity of the heat-treated gels becamegreater as the amount of fish oil increased Furthermoresurimi seafood was nutritionally enhanced with 120596-3 polyun-saturated fatty acid- (PUFA-) rich oils isolated from natu-ral sources such as algae flaxseed menhaden blend andkrill [73] The Alaska pollock surimi supplemented with120596-3 PUFA-rich oils showed improved protein fundamentaltextural properties heat-induced gelation and endothermaltransitions These studies show that the interaction of unsat-urated fatty acids and surimi proteins could contribute to theimprovement in gel properties without altering the texturalattributes

247 Plant Ethanol Extracts The effect of commercial tan-nin and ethanolic Kiam wood extract on the gelling char-acteristics of ice stored mackerel (Rastrelliger kanagurta)surimi was investigated by Balange et al [74] During12 d of iced storage pH TBARS TCA-soluble peptide andtrimethylamine (TMA) contents as well as total volatilebase (TVB) of mackerel mince increased while gel-formingability myosin heavy chain band intensity and whitenessdecreased consistently Deterioration lipid oxidation andprotein degradation proceeded as storage time increasedAn increase in deformation and breaking force of surimigel was observed with the addition of 030 commercialtannin or 015 ethanolic Kiam wood extract during the first6 d of storage Therefore commercial tannin and ethanolicKiam wood extract had not shown a gel-enhancing effecton mackerel surimi Furthermore Buamard and Benjakulinvestigated the effects of coconut husk ethanolic isolateson the gel-forming ability of sardine (S albella) surimi [75]Breaking force increasedwith the increasing levels of coconuthusk ethanolic isolates while a decrease in whiteness and nodetrimental effect on the sensory attributes of surimi gel wasobserved It was concluded that the addition of coconut huskextracts at a suitable concentration could enhance the gelstrength of sardine surimi with increased acceptability

25 Compound Additives The effect of different oxidizedphenolic compounds such as tannic acid OTA ferulic acidOFA caffeic acid OCF and catechin OCT on the gellingattributes of mackerel (R kanagurta) surimi was studied byBalange and Benjakul [76] Gels supplemented with 050OTA 040 OFA 010 OCT or 050 OCF showedincreases in deformation and breaking forces while a decreasein the expressible moisture content and myosin heavy chain

band intensity was observed In another study they inves-tigated the effects of oxidized phenolic compounds on thegel-forming abilities of bigeye snapper (P tayenus) surimi[77] An increase in breaking force and deformation witha decrease in expressible moisture contents was observedGels supplemented with the oxidized phenolic compoundshad a finer matrix with smaller strandsThe physicochemicalcharacteristics of natural actomyosin advocate that oxidizedphenolics could trigger the induction of disulfide bondformation or the conformational changes and cross-linkingthrough amino groups Therefore the addition of oxidizedphenolic compounds at an optimum concentration couldenhance the strength of surimi gel

Yongsawatdigul and Piyadhammaviboon reported aninhibition in autolysis of surimi and mince preparedby lizardfish (S tumbil) caused by p-tosyl-L-phenylalanylchloromethyl ketone and phenylmethanesulfonyl fluorideindicating the involvement of myofibrillar-associated serineproteinase Tropomyosin and myosin heavy chain proteinswere mainly hydrolyzed resulting in poor textural prop-erties [26] Arfat and Benjakul investigated the effect ofzinc chloride (ZnCl

2) and zinc sulfate (ZnSO

4) on the gel-

forming abilities of surimi produced by yellow stripe trevally(Selaroides leptolepis) [78] The kamaboko gels with ZnSO

4

added up to levels of 60120583molkg showed increased deforma-tion whiteness and breaking force as well as highly denserand interconnected gels Therefore ZnSO

4at a suitable

concentration could enhance gel strength and whiteness ofdark-fleshed fish surimi

3 Improvement in Quality andFunctionality of Fish-Paste Products

Various food additives from seafood (eg fish invertebratesand seaweed) plants (eg vegetables fruits and herbalmedicines) mushrooms animal sources and functionalmaterials used to improve the quality and functionality offish-paste products are listed in (Table 2) and describedbelow

31 Seafood Additives It has been reported that various typesof seafood namely fish including dried anchovy (Engraulisjaponicus) powder [79 80] pufferfish (Lagocephalus lunaris)powder [88] and skate (Raja kenojei) powder [81 82] andinvertebrates including warty sea squirt (Styela clava) groundflesh [83] its freeze-dried tunic powder [84] omandungi(Styela plicata) ground flesh [85] shrimp (Acetes japonicus)powder [86] and seaweed such as green laver (Ulva spp) [87]have been used to enhance the quality and functionality offish-paste

The boiled and dried Japanese anchovy (E japonicus)is a popular fisheries product in Korea and Japan As theflesh can be eaten together with bone boiled and driedanchovy products are regarded as good sources of calcium[174] Bae and Lee evaluated the properties of fried fish-paste with added anchovy (E japonicus) powder containinga high amount of calcium [79]The fish-paste containing 10anchovy powder displayed the highest values of adhesivenesshardness and strength In the overall acceptance of sensory

14 Journal of Food QualityTa

ble2Naturalfood

additiv

esused

toim

provethe

functio

nalpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Seafoo

dadditiv

es

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

1-2

[79]

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

5[80]

Skate

Rajakenojei

Fried

Hot

wind-dried

skin

and

cartilage

(64)p

owder

Seab

ream

Moistu

recontentcolortextural

andsensoryattributes

3[81]

Skate

Rajakenojei

Steamed

Ferm

ented

flesh

Nemipterusv

irgatus

Aminoacidand

moistu

recontentcolortexturaland

sensoryattributes

20

[82]

Wartyseas

quirt

Styelacla

vaFried

Groun

dflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

5[83]

Wartyseas

quirt

Styelacla

vaFried

Freeze-drie

dtunicp

owder

Frozen

Itoyori

Colortexturaland

sensory

attributes

1[84]

Pleatedseas

quirt

Styelaplica

taFried

Grin

dedflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

15

[85]

Shrim

pAc

etesjaponicus

Fried

Powder

Frozen

seab

ream

surim

iMoistu

recontentcolortextural

andsensoryattributes

5[86]

Green

laver

Ulva

spp

Fried

Powder

Frozen

seab

ream

surim

iColorsensory

attributes

5[87]

Pufferfish

Lagocephalus

luna

risFried

Powder

Nemipterusspp

Moistu

recrude

protein

lipid

colortexturalandsensory

attributes

5[88]

Maesaengi

Capsosiphon

fulve

scens

Fried

Freeze-drie

dpo

wder

Frozen

seab

ream

surim

iColortexturaland

sensory

attributes

5[89]

Redsnow

crab

Chionoecetes

japonicus

Fried

Leg-meat

powder

Frozen

Alaskap

ollock

(Tchalco

gram

ma)

Physiochem

icalandsensory

attributes

6[90]

Plantsou

rcea

dditives

Mulberryleaf

Morus

alba

Fried

Powder

Seab

ream

Colortexturesensory

attributes

05

[91]

Onion

Alliu

mcepa

Fried

Ethano

lextract

Cutla

ssfishpaste

Moistu

recontentTB

CVBN

colorsensoryattributes

3[70]

Lotusleaf

Nelumbo

nucifera

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

05

[92]

Beetroot

andSpinach

Beta

vulga

risand

Spinaciaoleracea

Microwave

inkamaboko

shape

mold

Freshbeet

rootspinach

dish

Not

mentio

ned

Moistu

retexture

analysis

Beetroot10

Spinach15

[93]

Citrus

fruits

Citru

slim

onC

junosC

unshiu

Fortun

ellajaponica

varmargarita

Steamed

Groun

dflesh

pulpwith

out

seeds

Min

Daegu

flesh

Colortexturaland

sensory

attributes

Cumqu

at[94]

Journal of Food Quality 15

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Oatbran

+SiO2

Avenasativa

Boiled

Powder

Frozen

Alaskap

ollock

surim

iColortexturaland

physiochem

icalattributes

6gOatbran10

0gSiO2

[95]

Yam

Dioscorea

japonica

Fried

Powder

Pollo

cksqu

idshrim

pFo

ldingtest

colortexturaland

sensoryattributes

2[96]

WolfberryC

hinese

Goji

Fructuslycii

Fried

Powder

Seab

ream

Texturalandsensoryattributes

3[97]

Redginseng

Pana

xginsengCA

Meyer

Fried

Powder

Not

describ

edColorlipid

oxidation

sensory

attributes

1[98]

Korean

angelicar

oot

Angelicae

gigantis

Radix

Fried

Powder

Seab

ream

Texturalandsensoryattributes

05

[99]

Turm

eric

Curcum

alongaL

Fried

Powder

Pollo

cksqu

idshrim

pColorrheologicalandsensory

attributes

3[100]

Wasabi

Wasabiajaponica

Fried

Freeze-drie

dpo

wder

Silver

pomfre

t(Pam

pusa

rgenteus)

ColorT

BCviablec

ellcou

nt

texturalandsensoryattributes

18

[101]

Wolfip

oriaextensa

Poria

cocos

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

3[102]

Mushroo

madditiv

es

Butto

nmushroo

mAg

aricu

sbisp

orus

Fried

Chop

ped

fresh

Argyrosomus

argentatus

Texturalandsensoryattributes

10

[103]

Enok

imushroo

mFlam

mulina

velutip

esFried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

5[104]

Shiitakem

ushroo

mLentinus

edodes

Fried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

10

[105]

King

oyste

rmushroo

mPleurotuseryngii

Fried

Paste

Silver

whitecroaker(Penn

ahiaargentata)

Texturalandsensoryattributes

10

[106]

King

oyste

rmushroo

mPleurotuseryngii

Steamed

Paste

Cuttlefish

(Sepiaesculen

ta)

Texturalphysio

chem

ical

sensoryattributes

40

[107]

Animalsource

additiv

es

Poultrychicken

Gallusgallus

domesticus

Fried

Breastmeat

batte

r

Itoyori

Japanese

threadfin

bream(Ne

mipterus

japonicus)

Chem

icalcompo

sition

color

fatty

acid

compo

sition

TBARS

sensoryattributes

746

or1493

[108]

Functio

nalfoo

dadditiv

es

Long

-chain

cellu

lose

mdashBo

iled

Powdered

cellu

lose

Alaskap

ollock

surim

iTexturalandrheological

attributes

6[109]

Dietary

fiber

from

ascidian

tunic

Halocynthiaroretzi

Boiled

Refin

eddietaryfib

erAlaskap

ollock

surim

iColortexturalph

ysiological

andsensoryattributes

5[110]

16 Journal of Food Quality

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Fibera

nd120596-3

oil

mdashHeatedin

awater

bath

Powdered

fiber120596

-3oil

Alaskap

ollock

surim

iTexturalandrheological

attributes

Fiber6ndash

10g

and120596-3100

g[111]

Flaxseed

orsalm

onoil

Not

describ

edCoo

kedin

awater

bath

Oil

Frozen

Alaskap

ollock

surim

i(Tchalco

gram

ma)

TBARS

colortexturaland

sensoryattributes

2g10

0gfranks

[112]

Soybeanoil

Glycinem

axHeatedin

awater

bath

Oil

Frozen

silverc

arpsurim

iColortexturalattributes

Soybeanoilgt3

[113]

Calcium

powdero

fcuttlefish

bone

treated

with

aceticacid

Sepiaesculen

taHeatin

gin

awater

bath

Calcium

powder

Alaskap

ollock

surim

iMoistu

recontentcolortextural

andsensoryattributes

009

[114]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Alaskap

ollock

meatp

aste

Colortexturaland

sensory

attributes

017

[115]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Sand

lance

(Hypoptychus

dybowskii)

Acid

andperoxide

valueVBN

sensoryattributes

02

[116]

Cheong

gukjang

Ferm

entedGlycine

max

byBa

cillussp

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

2[117]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 17

evaluation small and large size fish-paste with 1 and 2respectively of added anchovy powder was preferred Thesimilar increasing trend of calcium intensity was observedby Bae et al [80] However the fried fish-paste productscontaining 20 anchovy powder displayed the highest valuesof adhesiveness hardness and strength Regarding overallacceptance in the sensory evaluation the fried fish-pastecontaining 5 anchovy was preferred The optimal amountsof added anchovy in the results from Bae and Lee and Bae etal were different which might have been due to the differentdrying methods and sizes of the anchovies used in each study[79 80] Despite the differences in the two studies the resultssuggest that anchovy powder could be applied to fried fish-paste products to achieve high calcium contents

Skate contains many essential fatty acids includinglinolenic acid linoleic acid arachidonic acid DHA andEPA [175] Skate skin contains high percentages of collagenprotein and calcium [176] while its cartilage is rich inchondroitin sulfate [177] To improve quality and nutrientlevels Cho and Kim prepared fried fish-paste with skate (Rkenojei) powder (hot wind-dried skin and cartilage powder[6 4]) [81] According to Park et al preference testingusing steamed fish-paste product with different levels ofadded 14-day-fermented flesh of skate showed significantincreases in brownness smoothness and skate flavor scores[82] The amino acid contents of fish cake samples with20 skate added had the highest overall preference scoresConsequently the addition of 20 skate powder was optimalfor the steamed fish cake to improve its quality characteristicswith higher protein contents

Warty sea squirt (S clava) aquaculture in the Masanarea of Korearsquos south coast contains abundant unsaturatedfatty acids and essential amino acids in its flesh [178] andglycosaminoglycan in its tunic [179] Warty sea squirt has aunique taste and distinct antioxidant and anticancer activities[180] Fried fish-paste supplemented with 20 warty seasquirt (Korean name miduduk) displayed improved qualityand functionality [83] Choi et al reported a fried fish-paste containing freeze-dried byproduct of warty sea squirt(S clava tunic) [84] The hardness and strength of fish-paste increased with increasing amounts of tunic powderFor overall acceptance in sensory evaluation a fish-pastesupplemented with 1 S clava tunic obtained a relativelyhigher score The results suggested that S clava flesh andtunic could be used for fish-paste products to improve theirquality and functionality Park et al reported improvementin the functional properties of fish-paste by adding S plicata(Korean name omandungi) [85] Fried fish-paste containing20 S plicata indicated the highest values of adhesivenesshardness and strength For overall acceptance in sensoryevaluation a fish-paste containing 15 S plicata obtained thehighest score

Seo and Cho reported the preparation of fish-paste withadded shrimp (A japonicus) powder [86] The hardnessspringiness and cohesiveness increased with the increasingconcentration of shrimp powder However the brittlenessand gumminess reduced In the sensory evaluation the fish-paste prepared with 5 shrimp powder was most preferredCho and Kim reported the preparation of fish-paste with

added green laver (Ulva spp) powder [87] The hardnessspringiness and cohesiveness increased with the increasingconcentration of green laver powder However the brittlenessand gumminess decreased upon the addition of green laverpowder In the sensory evaluation a fish-paste prepared with5 green laver powder was preferred over other fish-pastesThese results suggest that green laver powder could be appliedto fish-paste to improve its quality and functionality

Pufferfish containing taurine hydroxyproline lysine andglycine impart a characteristic taste to food [181] To improvethe taste of fish-paste products Park prepared a fish-pasteby adding green rough-backed pufferfish (L lunaris) pow-der [88] The hardness strength gumminess springinessand chewiness of the fish-paste increased depending onpufferfish powder contentThe preparation of fish-paste withadded Capsosiphon fulvescens powder was reported by Park[89] The hardness springiness strength and cohesivenessincreased with the increasing concentrations of C fulvescenspowder However the brittleness and gumminess reducedwith the addition of C fulvescens powder In the sensoryevaluation overall the fish-pastes prepared with 5 Cfulvescens powderwere preferred over other fish-pastesThusthe results show that C fulvescens powder could be used tocreate fish-paste products with high quality and functionality

Kim et al reported the changes in the sensory and physic-ochemical properties of a fish-paste containing red snow crab(Chionoecetes japonicus) leg-meat powder [90] Hardnessgumminess springiness and cohesiveness increased withincreasing levels of red snow crab leg-meat powder Based onthe sensory evaluation it was concluded that the addition ofred snow crab leg-meat powder at a level of 6 could improvethe quality characteristics of fish-paste products

32 Plant Source Additives It has been reported that variousplant sources namely vegetables (eg mulberry beetrootand spinach) fruits (eg citrus) and herbal medicines (egChinese matrimony vine Korean Angelica root) have asignificant effect in improving the quality and functionalityof fish-paste products

Mulberry (Morus alba) leaf has been used traditionallyto treat a disease symptomized by thirst and stroke [182]Ever since mulberry leaf was included as a food material inthe Food Codex in 1988 by the Ministry of Food and DrugSafety (MFDS Osong Chungju South Korea) Mulberry leafpowder has been used in various processed food productsand health functional foods Shin and Park reported theuse of mulberry leaf powder in the preparation of fish-pasteproducts [91] In a texture meter test the hardness increasedbut the cohesiveness springiness gumminess and brittlenessdecreased with increasing levels of mulberry leaf powder Insensory evaluation the fish-paste with 05 mulberry leafpowder revealed the highest acceptance scores in terms offlavor texture and overall quality

Garden onion (bulb onion Allium cepa) is a perennialplant belonging to Liliaceae and is widely used as a spice andseasoning vegetable in both the East and the West Park etal investigated the quality characteristics of fried fish-pastesupplemented with flavonol-rich ethanol extract of onion[183] In the sensory evaluation as the amount of ethanol

18 Journal of Food Quality

extract of onion increased so did the favorability in termsof flavor and taste Notably 3 ethanol extract of onion hadthe best score in overall acceptance The results indicate thatethanol extract of onion can be used to prepare fried fish-paste products with high quality and functionality

Shin reported the production of fish-paste with addedlotus (Nelumbo nucifera) leaf powder [92] The flavor adhe-siveness and hardness increased with the increasing levels oflotus leaf powder The fish-paste with 05 lotus leaf powderdisplayed the highest acceptance scores in terms of springi-ness pleasant taste appearance texture flavor and overallquality Thorat et al prepared kamaboko containing greenchili coriander ginger garlic spice mixture and groundbeetroot or a spinach dish and then subjected the preparationto microwave cooking [93] Kamaboko prepared with 10beetroot and a 15 spinach dish was found to be superior tothe others

Yang and Cho developed a steamed fish cake with added5 ground citrus fruits with skin [94] The addition of citrusfruits did not disturb the flexibility of surimi The pH ofsurimi samples increased in the following order lemon (Cit-rus limon) citron (Citrus junos) tangerine (Citrus unshiu)kumquat (Fortunella japonica var margarita) and controlThe hardness of surimi was highest for lemon followed bycitron tangerine kumquat and control surimi In the sensoryevaluation surimi containing kumquat demonstrated higherscores in terms of color taste and textural properties Theseresults suggest that surimi could be prepared by adding citrusfruits to improve the quality and functionality

Oat bran is a gluten-free dietary fiber that may decreasethe risk of diabetes and heart diseases The physicochemicalproperties of surimi gels supplemented with oat bran werestudied by Alakhrash et al [95] The oat bran and SiO

2

incorporation (6 g100 g) greatly improved water-holdingcapacity and gel texture while a reduction in whiteness wasobserved Kim and Byun conducted tests on the sensoryand physicochemical characteristics of fish-paste with addedyam (Dioscorea japonica) powder [96] The addition of yampowder increased gumminess strength springiness andcohesiveness In the sensory evaluation the addition of 2yam powder had the best scores in terms of taste color andoverall preference

Fructus lycii is a fruit produced by Lycium barbarumL that has been used for nourishment tonicity and nour-ishment of the blood it has antibacterial anticancer andantioxidant properties [182ndash186] Shin et al prepared friedfish-paste containing dried F lycii powder [97] In the texturalanalysis cohesiveness increased while brittleness and gum-miness decreased with increasing levels of F lycii powderThe 3 F lycii powder sample had the highest acceptancescores in terms of appearance texture taste flavor andoverall acceptability

Red ginseng-based fried fish-pastes containing differentsizes and amounts of red ginseng powder were preparedand their biological properties including lipid oxidation toimprove fish-paste quality were investigated [98] The fish-paste products containing red ginseng powder showed asignificant increase in hardness and chewiness Furthermorean inhibitory effect on lipid oxidation and reduced number

of total microbes during storage were observedThese resultssuggest that high-quality fish-pastes could be achieved withthe addition of 1 red ginseng powder which effectivelyimproved both sensory evaluation and physicochemicalproperties

Angelicae Gigantis Radix (the dried root ofAngelica gigasNikai) more popularly known as Korean Angelica is one ofthe widely used herbal medications [187] It has been usedin Korean medicine as an important medication for anemiaand blood circulatory disorders It has also been used formenstrual pains and postmenopausal syndromes Shin et alreported the development of fish-paste with A gigas powder[99] In a texture test hardness chewiness and brittlenessincreasedwith increasing concentrations of AngelicaeGigan-tis powderHowever cohesiveness and springiness decreasedIn the sensory evaluation the fish-paste with 05 AngelicaeGigantis powder showed the highest acceptance scores forappearance flavor taste texture and overall quality

Turmeric (Curcuma longa) has been used in Ayurvedicmedicine from ancient times as a treatment for inflammatoryconditions It has been reportedly used for its various bio-logical activities including antibacterial antiviral antifungalantioxidative and antiatherogenic effects [188] Turmeric hasbeen grown as a special crop in the central and southern areasaround Jindo in South Korea [189] Choi et al investigatedthe sensory and rheological properties of fish-paste preparedwith turmeric powder [84] In terms of textural attributesthe addition of C longa powder decreased springiness andimproved strength In the sensory evaluation the addition of3 C longa powder was associated with the best scores fortaste and overall preference

Wasabi (Wasabia japonica) has various beneficialhealth properties including antioxidative antimicrobialand antimutagenic activities [190 191] Jang et al reporteda high-quality fried fish-paste product made with silverpomfret (Pampus argenteus) which is one of the savorysoft and delicious types of fish prepared by adding wasabipowder [101] Notably hardness gumminess and chewinessincreased significantly with the addition of wasabi powderIn the sensory evaluation 18 wasabi powder showed thebest score in overall acceptability These results show thatwasabi could be used as a food additive or preservative infish-paste products

White Poria cocos wolf is the inner white part of P cocosa parasite found on Pinus densiflora It is used to treat edemachronic gastritis gastric atony nephrosis acute gastroentericcatarrh emesis dizziness and vomiting [192 193] Shin et alprepared a fried fish cake with added white P cocos powderand studied the textural and sensory characteristics [102]In texture tests brittleness was observed to increase whilespringiness decreased with increasing concentrations of Pcocos powder The fish-paste product containing 3 whitePoria cocos powder showed the highest acceptance scores forflavor appearance texture taste and overall quality

Milk-vetch root is one of the most produced herbalmedicines in Korea It is a peeled and dried root of the herba-ceous perennial herb known as Astragalus membranaceuswhich belongs to the Fabaceae family [194] It has been

Journal of Food Quality 19

reported that milk-vetch root exerts diuretic tonic anti-hypertensive hypoglycemic immune-enhancing antitumorand antiviral effects [195] Kim investigated the sensoryand physicochemical properties of fish-paste prepared withmilk-vetch root powder [196] The strength cohesivenessbrittleness and gumminess of the fish-paste increased whileits springiness decreased with an increasing amount of milk-vetch root powder In the sensory evaluation the addition of10 milk-vetch root powder indicated best scores for tastetexture color and overall preference

33 Mushroom Additives Mushroom is a nutritional andfunctional food as well as a vital source of physiologicallybeneficial medicines Mushrooms have been used as tradi-tional medicines in Korea Japan China and other Asiancountries for curing various diseases including lymphaticdisease gastroenteric disorder oral ulcer and various can-cers [197] It has been reported that edible mushrooms inKorea number approximately 350 species [198] Several ediblemushrooms that are highly preferred have been added to fish-paste to enhance their quality and functionality

Ha et al prepared a fried fish-paste product with addedAgaricus bisporus which is a product described as having aracy flavor and taste [103]The elasticity hardness brittlenessand gumminess of fish-paste with the added mushroomincreased however no significant difference in strengthwas observed Regarding overall acceptance in a sensoryevaluation a fish-paste supplemented with 10 A bisporusmushroom showed the highest scores

Enoki mushroom (Flammulina velutipes) is well knownfor its anticarcinogenic and blood pressure-reducing prop-erties To utilize its functional properties enoki mushroomwas added to fried fish cake [104] The sample containing15 mushroom received the highest values for strengthgumminess and brittleness In the sensory evaluation thefish cakes with 5 mushroom obtained favorable scores foroverall acceptance

Shiitake mushroom (Lentinus edodes) is known for itshigh level of 120573-glucans Son et al investigated the effectsof shiitake mushroom on the textural properties of friedfish cake [105] The fish cake containing shiitake mushroomreceived the highest values for strength hardness gummi-ness and brittleness In the sensory evaluation the fish cakeswith 10 shiitake mushroom sample obtained the best scorefor overall acceptance

Kim et al prepared a fried fish cake using cultured kingoyster mushroom (Pleurotus eryngii) and silver white croaker(Pennahia argentata) surimi to enhance its physiologicaleffects [106] In assessing its quality properties fish cake towhich 10 mushroom was added received the highest valuesfor strength hardness gumminess and brittlenessThe effectof king oyster mushroom on the textural and physicochem-ical properties of steamed cuttlefish (Sepia esculenta) fishcake was investigated by Chung et al [107] The fish-pastewith added king oyster mushroom paste revealed significantdecreases in gumminess cohesiveness and hardness whilethe springiness increased with increasing concentrations ofking oystermushroompasteOn the sensory evaluation basisthe cuttlefish-paste supplemented with 30ndash50 king oyster

mushroom showed higher overall acceptability In the studiesby Kim et al and Chung et al the optimal amounts of kingoyster mushroom differed which might have been due tothe different cooking methods and surimi used in each study[106 107]

34 Animal Source Additives Jin et al investigated the effectof chicken meat on the quality characteristics of Itoyori(Japanese threadfin bream Nemipterus japonicus) surimi[108] The physicochemical properties such as fatty acidcomposition shear force and gel characteristics were affectedby substitution with spent laying hen meat batter Howeversensory characteristics were less affected by this substitutionA huge amount of waste in the processing of grass carp isdiscarded To deal with this waste Gao et al studied theprocessing technology used for fish and mushroom pastewith salted fish cubes mushroom soybean and fermentedsoybeans [199]

35 Functional Food Additives Functional food additivesincluding dietary fiber 120596-3-rich oil calcium additives andpropolis have been used in the preparation of fish-pasteproducts to increase their quality and functionality Westernpopulations have an inadequate quantity of health beneficialdietary fiber in their diets Besides fiber most Western pop-ulations also consume an insufficient amount of 120596-3 PUFAswhile their sodiumconsumption greatly surpasses the recom-mended maximum Debusca et al prepared Alaska pollocksurimi fortified with commercial long-chain cellulose as asource of dietary fiber [109] Fiber fortification up to a level of6 improved both texture and color a slight decline in thesevalues was observed at levels of 8 fiber An increase in gelelasticity and thermal gelation of the fish cake was observed

Yook et al prepared a fish-paste by adding dietaryfiber extracted from ascidian (Halocynthia roretzi) tunic toenhance its physiological properties [110] The hardnessgumminess adhesiveness shear force and chewiness of thefish-paste improved with the incorporation of the ascidiandietary fiber The fish-paste with 5 ascidian dietary fiberscored the highest and was generally preferred by sensorypanels Tolasa et al reported that the oxidative stability andthe uniform dispersion of 120596-3 unsaturated fatty acids can beattained in a highly consistent surimi gel system without theuse of antioxidants [200]

Surimi and surimi-based products are famous through-out the world In fact US consumption increased in the1980s while the rate leveled off thereafter The nutrificationof food products with 120596-3 PUFAs increases the health ben-efits of food consequently increasing their market demandPietrowski et al prepared surimi seafood products nutrition-ally enhanced with 120596-3 PUFAs [201] Although the nutrifica-tion of 120596-3 PUFAs indicated an increase in lipid oxidationit was within limits acceptable to consumers The color ofsurimi seafood nutrified with 120596-3 PUFAs generally improvedbut no effect on textural characteristics was observed

Debusca et al reported that the fortification of Alaskapollock surimi with either 120596-3 oil or dietary fiber alone orin combination improved both the textural and rheologicalproperties [111]The120596-3 oil and fiber in combination revealed

20 Journal of Food Quality

greater gelation of surimi and a slight reduction in color prop-erties indicating their interaction with myofibrillar proteinsThus it was suggested that the 120596-3 oils and fiber could beeffectively used as a fortifying agent to prepare high-qualitysurimi products with nutritional benefits Sell et al preparedsurimi franks fortified with salmon oil or flaxseed [112]The textural properties showed differences between franktypes with the flaxseed franks being cohesive less gummysofter and chewy while the sensory evaluation showed nosignificant differences

Chang et al determined the effects of soybean oil andmoisture contents on the physical properties of surimi gels[113] The increasing levels of soybean oil and moisturecontents resulted in an increase in whiteness and reductionin the chewiness hardness and breaking force Setting incombination with soybean oil improved the textural andcolor parameters of surimi gels indicating that soybean oilcould be used to improve the color and textural properties ofsurimi seafood products

Kim et al prepared boiled fish cake using acetic acid-treated cuttlefish bone as a calcium additive agent [114] Theresults of sensory evaluation of texture and whiteness weresimilar to those without this supplementation In the mineralcontent analysis of heat-induced surimi gel calcium contentincreased depending on the increasing concentration ofacetic acid-treated cuttlefish bone powder while phosphoruscontent did not change The optimal concentration of aceticacid-treated cuttlefish bone powder for the preparation ofhigh-quality heat-induced surimi gel was 009

Kim et al prepared Alaska pollock fried fish-pastesupplemented with propolis [115] The addition of propolisenhanced the antispoiling and antioxidative ability as well asgel strength of fried fish-paste In the sensory evaluation theaddition of 017 propolis showed the best score in overallacceptability In another study Kim et al later studied sand-lance (Hypoptychus dybowskii) meat paste prepared withpropolis [116] Similar to the previous report the addition ofpropolis on the fried fish-paste showed higher antioxidativeand antispoiling activities The fried sand-lance meat pasteprepared with 02 added propolis was the most acceptableFurthermore the bitter taste of the sand-lancemeat paste wasreduced by adding 2 sweet amber powder

Cheonggukjang is an ancient Korean food prepared byfermented soybean It contains high levels of dietary fiberoligosaccharides isoflavones saponin lecithin phytic acidand phenolic compounds among others Its many benefi-cial properties have been reported such as thrombolyticanticancer antimicrobial hepatoprotective antioxidant andcholesterol-lowering effects [202] Park et al reported theuse of fish-paste containing cheonggukjang powder [117]Theincreasing concentrations of cheonggukjang resulted in anincreased value of springiness cohesiveness and hardnesshowever a reduction in brittleness and gumminess values offish-paste was observed

4 Shelf-Life Extension of Fish-Paste Products

Fish-paste products may easily spoil due to residualmicrobes that are not removed by sterilization during the

manufacturing process or by contamination in packagingor the distribution process For such reasons even vacuum-packed fried fish-paste products have a shelf-life of fewerthan 10 days during cold storage which is relatively short[121 122] Various efforts have been made to develop long-term storage solutions for fish-paste products via physicaland chemical methods [118ndash122] Although these methodswere found to be very effective for the long-term storageof fish-paste products they require sensitive and complexmanipulation and are costly

The addition of appropriate food additives to fish-pasteproducts as an effective preservation protocol is anotherstrategy Potassium sorbate is a typical synthetic food preser-vative and is commonly used in processed foods includingfish-paste productsThis material is effective in inhibiting thegrowth of variousmicroorganisms as it has a slight sterilizingeffectThe use of this material is permitted to a concentrationof less than 20 gkg in processed fish meat products (FoodCode Ministry of Food and Drug Safety Republic of Korea)According to the results of Walker sorbates and sorbic acidexert a very low level of mammalian toxicity even in chronicstudies as up to 10 of the diet did not show any carcinogenicactivity [203] In addition Thakur and Patel summarizedthe application of sorbates in the shelf-life extension of fishand fish-based products [204] The physical and chemicalmethods along with natural food preservatives for the long-term storage of fish-paste products are listed in Table 3 andbriefly described below

41 Physical and Chemical Methods Various efforts havebeen focused on developing long-term storage solutions forfish-paste products via physical methods including highpressurization [118] microwave pasteurization [93] highhydrostatic pressure treatment [119] and even irradiation[118 121] In addition it has also been reported that treatmentwith chlorine dioxide solution at an appropriate concentra-tion which is harmless to humans could be used to preventspoilage and to extend the shelf-life [122]

High hydrostatic pressure technology has graduallygained popularity in the food industry over the last twodecades [205] In 2013 the worldwide market for highhydrostatic pressure equipment was estimated to be $350million and it is expected to grow Besides high hydrostaticpressure technologies several types of radiation have alsobeen tested including ultraviolet microwaves and gammairradiation treatments Radiation is generally used to controlbiological hazards in the production of fish-paste productsand to prolong the shelf-life of such products [206 207]Gamma radiation exerts potent antimicrobial effects whereasultraviolet rays are effective for the surface but not interiorsterilization of porous dried fish products (eg fish-pasteproducts) However gamma irradiation treatment demandslarge-scale facilities and higher costs [207 208]

Miyao et al reported that growth of the majority of thepathogenic microorganisms present in surimi was inhibitedat a high pressure of between 300 and 400Mpa [118] Severalpressure-resistant strains were isolated from surimi and wereidentified as Moraxella sp Acinetobacter sp Streptococcusfaecalis and Corynebacterium sp It was suggested that

Journal of Food Quality 21

Table3Naturalfood

additiv

esandph

ysicochemicalmetho

dsused

toim

provethe

shelf-life

offish-paste

prod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Physicalandchem

icalmetho

ds

Highhydrostatic

pressure

mdash

High-pressure

treatmento

rheattre

atment

insampletub

ewith

vacuum

packaging

mdashFrozen

Alaskap

ollock

Microbialactiv

ity40

0MPa

[118]

Highhydrostatic

pressure

mdashNot

cooked

mdash

Tuna

fishpaste

Mackerelp

astewith

paprika

mackerelp

astewith

garlic

mackerelp

astealon

eand

salm

onpaste

Microbialactiv

ity200M

Pa[119]

Co-60

Gam

mar

ays

mdashGrilled

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

texturalsensorym

icrobial

physiochem

icalattributes

75kG

y[120]

Co-60

Gam

mar

ays

mdashFried

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

pHtexturalmicrobial

physiochem

icalattributes

3kGy

[121]

Chlorin

edioxide

(ClO2)

mdashSteamed

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

VBN

TBA

RSpHm

icrobial

physicochemicalsensory

attributes

50pp

m[122]

Naturalfood

additiv

esRe

dpepp

erethano

lextract(RP

EE)

andchop

pedfre

shredpepp

er(C

FRP)

Capsicu

mannu

umFried

Ethano

lextract

andchop

ped

fresh

one

Frozen

Alaskap

ollock

TBC

sensoryattributes

RPEE

10

CF

RP5

[123]

Ethano

lextract(EE)

andwater

extract

(WE)

Phellodendron

amurense

Eugenia

caryophyllu

sPinu

srigida

Bletillastr

iata

andPa

eonia

albiflora

mdashmdash

mdashAntim

icrobialattributes

onpu

trefactiveisolatesfrom

fish

meatp

asteprod

ucts

EE2000

ppm

[124]

Eggwhitelysozyme

(EWL)

andor

sodium

hexametapho

sphate

(SHMP)sod

ium

pyroph

osph

ate(SP

P)

Gallusgallus

domesticus

Fried

Powder

Frozen

Alaskap

ollock

Viablecellcoun

tpH

VBN

biochemicalattributes

EWL5

+SP

P05

+SH

MP

01

[125]

Grapefruitseed

extract

Citru

sparadisi

mdashSolutio

nCom

merciallyavailablefi

shmeat

paste

prod

ucts

Proxim

atec

ompo

sition

textural

biochemicalrheologicalsensory

attributes

1000

ppm

[126]

22 Journal of Food Quality

Table3Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Cinn

amon

bark

extract

Cinn

amom

umcassia

Fried

Extracted

solutio

nFrozen

Alaskap

ollock

Antim

icrobialactiv

itySprayeddiluted

extract(11)

[127]

Alginicacid

hydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Relativev

iscositypHcolor

rheologicalattributes

03

[128]

Chito

sanhydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Viablecellcoun

tsrheological

sensoryattributes

03

[129]

Nisin(N

)and

or

sucrosefattyacid

esters(SFE

)mdash

Steamed

Powdera

ndsolutio

nFrozen

Alaskap

ollock

Viablecellcoun

tantim

icrobial

activ

ityN125120583

gg+

SFE10mg

[130]

Piscicolin

KH1

Carnobacteriu

mmaltalomaticu

mSteamed

Solutio

nCod

fish

Inhibitory

assayproteincontent

antim

icrobialactiv

ity50

AUg

[131]

Zein

andsoyprotein

isolate(SPI)fi

lms

containing

greentea

extract(GTE

)

Zeamays

Glycinem

axCa

melliasin

ensis

Fried

Ediblefilm

(GC-WPI)w

ithGTE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

TBARS

colorm

icrobial

physicalattributes

GTE

1

[132]

Gelidium

corneum

(GC)

-Wheyprotein

isolate(G

C-WPI)

blendfilm

containing

grapefruitseed

extract(GSE

)

Gelidium

corneum

Citru

sparadisiBo

staurus

Not

mentio

ned

Ediblefilm

(GC-WPI)w

ithGSE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

Water

vapo

rpermeability

microbiologicalanalysis

sensory

attributes

GSE

01

[133]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 23

damage to the cell membrane and degradation of ribonucleicacids occurred in the high-pressure-treated cells Malickiet al investigated the use of high hydrostatic pressure toprolong the shelf-life of traditionallymanufactured fish-pastestored under refrigeration (4∘C) for 6 weeks [119] Neitherbacteria nor molds or yeasts were detected in the highhydrostatic pressure-treated fish-paste samples at any timepoint analyzed irrespective of the pressurization conditionsIn conclusion these studies revealed the effectiveness of highhydrostatic pressure to prolong the shelf-life of traditionallymanufactured fish-paste stored under refrigerated conditionsfor up to 6 weeks

Kim et al reported a reduction in the total aerobicbacterial counts in the grilled fish-paste stored at 5∘C andirradiated by gamma rays at a level of 25 kGy or more[120] Additionally the treatment of gamma rays at a levelof 75 KGy at 30∘C showed a significant inhibition in aerobicbacterial growth Cho et al investigated the effect of Co-60 gamma irradiation on fried fish-paste and studied thephysicochemical properties of fish-paste products stored atlow temperature (3 plusmn 1∘C) and room temperature (10ndash20∘C)[121] There was no obvious difference between the vacuum-and air-packed groupsThe irradiation of 3 KGy extended theshelf-life of fish-paste up to 2 times at room temperature and3-4 times at low temperature In both studies the irradiationtreatment caused very little textural degradation and no effecton the sensory characteristics of the samples was observed

Shin et al investigated the effects of chlorine dioxide(ClO2) treatment on the physiochemical andmicrobial prop-

erties of fish-paste products [122] After ClO2treatment

fish-paste samples were individually packed and stored at4∘C The pH and VBN values of fish-paste decreased withincreasing ClO

2concentration ClO

2treatment significantly

reduced the populations of total bacteria yeast and moldduring storage In particular treatment with 50 ppm ClO

2

significantly decreased the total bacterial count the mostamong all ClO

2-treated fish-pastes showing that 50 ppm

chlorine dioxide was the optimum concentration to prolongthe shelf-life of fish-paste products

42 Natural FoodAdditives Theuse of natural food preserva-tives rather than chemical and synthetic food preservatives isofworldwide interest It has been reported that several naturalfood additives could extend the shelf-life of cooked fish andfish products Some examples include onion ethanol extract[183] egg white lysozyme [125] grapefruit seed extract [126]chitosan hydrolysate [129] cinnamon bark extract [127] andred pepper extract [123] as well as mixtures of lysozymessodium hexametaphosphate and sodium pyrophosphate

The shelf-life of fried fish-paste products prepared byadding red pepper ethanol extract was estimated by Yoonet al [123] The shelf-life of the fried fish-paste with added10 red pepper ethanol extract and 5 chopped fresh redpepper was 2 to 3 days longer than that of the commercialfish-paste product thus demonstrating the most effectivepreservation effects According to Ahn et al the extractsof Eugenia caryophyllus Pinus rigida Bletilla striata andPaeonia albiflora exerted strong inhibitory effects on thegrowth of microorganisms isolated from putrefied fish-paste

[124] Notably the ethanol extract was more effective thanwater extract in all tested microorganisms The inhibitionlevel of each extract was evident at 2000 ppm ethanol in thefish-paste

Kim et al investigated the inhibitory effects of lysozymesmixtures of lysozymes and other antibacterial substancessuch as sodium pyrophosphate and sodium hexametaphos-phate on bacterial growth in surimi products [125] Thelysozymes inhibited growth in most of the tested isolatesand themixture of antibacterial substances showed increasedeffects compared with those when they were used individ-ually A mixture of 05 sodium hexametaphosphate 05sodium pyrophosphate and 005 lysozyme in imitationcrab and kamaboko showed the highest inhibitory activ-ity

The stabilizing effects of grapefruit seed extract on fish-paste products were investigated by Cho et al [126] Texturalproperties decreased with increasing storage period Thetreatment of fish products with grapefruit seed extract pro-longed the deterioration of fish-paste product proteins duringstorage up to 4-5 daysThe chemical sensory and rheologicalevaluation revealed that the grapefruit seed extract could beused as an effective additive to extend the shelf-life of fish-paste products

The predominant bacterium in most of the isolatedmicroorganisms from packed and unpacked spoiled fish-paste products is Bacillus sp [127] Notably yeast andmolds are not reported in the vacuum-packed products Ahydrolysate of alginic acid has antimicrobial activity but ithas not been used at industrial scale The alginic acid ata concentration of 03 prolonged shelf-life of fish-pasteproducts by 4 days at 15∘Cand inhibited the growth ofBacillussp isolated from fish-paste products [128] According to theresults of Cho et al the chitosan hydrolysate made withchitosanase from Aspergillus oryzae ATCC 22787 revealedthe strongest antimicrobial activity and inhibited the growthof Bacillus sp isolated from fish-paste products [129] Theaddition of chitosan hydrolysate at a concentration of 03resulted in extended shelf-life of up to 6 days at 15∘C Jeonget al reported that spraying cinnamon bark extract on thesurface of the fried fish-paste products could inhibit thegrowth of spoilage bacteria and mold at room temperatureand resulted in prolonged shelf-life [127]

Yamazaki et al investigated the effects of nisin andsucrose fatty acid esters on the growth of spoilage bacteria infish-paste products [130] Nisin exerted antibacterial activityagainst Bacillus subtilis and Bacillus licheniformis in a liquidmedium at 20∘C and resulted in a longer shelf-life forfish-paste products It was concluded that the addition ofnisin could be used as a potential alternative method toprevent spoilage caused by spore-forming bacteria in fish-paste productsThe bacteriocin produced byCarnobacteriummaltalomaticum had the ability to inhibit both Enterococcussp and Leuconostoc sp which reduce the shelf-life of fish-paste products during preservation [131] The results showedthat the purified bacteriocin piscicolin KH1 andor nisin sig-nificantly inhibited the growth of Leuconostoc mesenteroidesand Enterococcus faecium and could be used as a food-gradepreservative for kamaboko gels

24 Journal of Food Quality

Sakai and Yamaguchi examined the possibility of inhibit-ing lipid oxidation in boiled fish-paste by adding yuzu skinto the surimi [209] The heat-treated control kamabokoand yuzu skin-added kamaboko (citron kamaboko) wererefrigerated at 0∘C for 2 days and after heating the surimithe malonaldehyde content in both kamabokos was reducedThese results suggest that the addition of citron skin sup-pressed lipid oxidation in fish-paste products

Various packing materials and wrapping techniques havealso been employed to keep fish-paste products fresh and freeof contaminants for a longer period of time Lee et al investi-gated the processing conditions and quality stability of retortpouched fried-mackerel fish-paste during storage [210] Themackerel fish-paste was ground with added ingredients friedin soybean oil cooled vacuum-packed in a laminated plasticfilm and finally sterilized at 120∘C for 20min in a hotwater circulating retortThe reported method showed a goodpreservation for 100 days at 25 plusmn 3∘CThe sensory evaluationshowed no significant differences between the prepared fish-paste products and that of products in the market Ha et alexamined the optimum storage conditions for maintainingthe quality of the fried fish-paste in retort pouches [211]Both hardness and gel strength increased with increasingsterilization temperature On the other hand no differenceswere observed in elasticity and water-holding capacity

Lee et al elucidated the antioxidative effects of soyandor zein protein films containing green tea extract on thephysiological properties of fish-paste products during storage[132]The soy protein films showed an increase in yellownesswhile a decrease in yellowness was observed with the zeinfilms The lipid oxidation was retarded at day 2 of storageby wrapping the fried fish-paste products with soy and zeinprotein films containing green tea extract Lim et al prepareda Gelidium corneum whey protein isolate (GC-WPI) blendfilm containing grapefruit seed extract and studied the effectof this film on pathogenic bacterial inhibition during storage[133]TheGC-WPI blend was effective in decreasing the pop-ulations of Salmonella typhimurium Listeria monocytogenesand Escherichia coli on films treated with 01 grapefruitseed extract These studies suggest that packaging fish-pasteproducts in plant-based protein films containing green tea orgrapefruit seed extract could be beneficial to prolong shelf-life

5 Conclusion

The production of surimi dates back to ancient times How-ever advancement in surimi processing technology startedin 1960 with the discovery of cryoprotectants which werehelpful in maintaining the gel quality and functionality offish-paste for relatively longer periods of frozen storage [3]As themarket share of quality-conscious consumers rises thedemand for the use of natural additives rather than chemicalingredients for surimi products will continue to increaseAccording to Park et al the worldwide production of surimi-related products reached around 800000MT by 2011-2012while the main fish sources for surimi products includePacificwhitingAlaska pollock jackmackerel Atkamackerelsouthern blue whiting northern blue whiting and hoki [3]

Surimi is subdivided into high-grade (FA SA and A) andlow-grade (KA KB and RA) types based on the quality ofthe raw fish sources Most of the high-grade surimi is soldin Japan for the production of kamaboko and other high-quality surimi products and in Korea for the production ofpremium crabsticks Low-grade surimi is sold in Europe andthe United States for the manufacturing of crab sticks andin Korea and Japan for the preparation of other fried fishproducts [3] With the technological advancements in thesurimi processing industry it has been possible to use low-grade surimi for the production of fish cakes fish balls andother surimi products

With increasing demand and new processing techniques(eg the pH-shift method) the use of other seafoodresources such as small pelagic species and giant squid forthe production of surimi and surimi products was possible[212] Notably the production of surimi products is cheaperinKorea than elsewhere but industry professionals are alwayssearching for the most inexpensive surimi seafood sourcesHence the production of surimi from aquaculture fish suchas catfish and carp is growing in demand

Food additives from animal and seafood sources suchas fish chicken beef plasma proteins and egg white areconsidered the most effective protease inhibitors for surimiHowever with the outbreak of avian influenza mad cow dis-ease undesirable resulting characteristics and some religiousconstraints there is limited use of these food additives Addi-tionally vegetarians in some parts of the world would notwish to consume surimi-based products containing additivesderived from animals or even from seafood sources Hencethere is a need to identify more effective and alternative food-grade ingredients (eg plant sources seaweed and microal-gae) to be used in the preparation of fish-paste products

Surimi is mainly used for human consumption As suchthe challenges of production cost composition nutritionalvalue and the shelf-life of surimi products can never beneglected This review has provided an overview of nat-ural and synthetic food additives and preservatives usedto enhance the quality functionality and shelf-life of fish-paste products In addition the improvements in the fish-paste product quality and functionality by various foodadditives from seafood plants mushrooms animal sourcesand functional materials were discussed

For decades surimi and surimi-based products have beenwell known in East Asian countries such as Japan and KoreaHowever with advancements in technology they are attract-ing attention in other Asian as well as European countriesWith the increasing consumption worldwide the manufac-turing and processing of fish-paste products may requirenew and improved additives to enhance their acceptability inthe market Continuous scientific innovations and improvedprocessing technology will aid in further advancements andimprovements in this area

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article and regarding thefunding received

Journal of Food Quality 25

Authorsrsquo Contributions

Khawaja Muhammad Imran Bashir and Jin-Soo Kim con-tributed equally to this work

Acknowledgments

This research was a part of the Project no PJT200885entitled ldquoDevelopment andCommercialization of TraditionalSeafood Products Based on the Korean Coastal MarineResourcesrdquo funded by the Ministry of Oceans and FisheriesSouth Korea

References

[1] H-J Hwang S-Y Choi and S-C Lee ldquoPreparation andquality analysis of sodium-reduced fried fish cakesrdquo PreventiveNutrition and Food Science vol 18 no 3 pp 222ndash225 2013

[2] KFDA Food code Article 1-5-12 Korea Food and Drug Admin-istration Seoul Korea 2012

[3] J W Park H Nozaki T Suzuki and J-L Beliveau ldquoHistoricalreview of surimi technology and market developmentsrdquo inSurimi and Surimi seafood J W Park Ed pp 3ndash24 CRC PressNew York NY USA 2013

[4] J A Ramırez R Dıaz-Sobac O G Morales and M VazquezldquoEvaluation of freeze-dried surimi from tilapia and fat sleeper asemulsifiers [Evaluacion de surimi liofilizado de tilapia y dormi-dor como emulsificantes evaluacion de surimi liofilizado detilapia e dormidor como emulsificantes]rdquo Ciencia y TechnologiaAlimentaria vol 2 no 4 pp 210ndash214 1999

[5] J M Aguilera and D W Stanley ldquoFood structuringrdquo inMicrostructural Principles of Food Processing and Engineeringvol 12 p 246 AN Aspen Publishers Gaithersburg MarylandUSA 1999

[6] A P Stone and D W Stanley ldquoMechanisms of fish muscle gela-tionrdquo Food Research International vol 25 no 5 pp 381ndash3881992

[7] S Nakamura and M Ogawa ldquoBiomolecular strategies forpreparation of high quality surimi-based productsrdquo PreventiveNutrition and Food Science vol 10 no 2 pp 191ndash197 2005

[8] M Okada ldquoHistory of surimi technology in Japanrdquo in Surimitechnology T C Lanier and C M Lee Eds pp 3ndash22 MarcelDekker Inc New York NY USA 1992

[9] MIFAFF ldquoStatistics of fisheries processingrdquo Ministry of FoodAgriculture Forestry and Fisheries Seoul Korea 2011

[10] T C Lanier ldquoMeasurement of surimi composition and junc-tional propertiesrdquo in Surimi technology T C Lanier and C MLee Eds pp 123ndash166 Marcel Dekker Inc New York NY USA1992

[11] K-H Chung and C-M Lee ldquoRelationships between physico-chemical properties of nonfish protein and textural propertiesof protein-incorporated surimi gelrdquo Journal of Food Science vol55 pp 972ndash975 1990

[12] M TMorrissey JWWuD Lin andHAn ldquoProtease inhibitoreffects on torsionmeasurements and autolysis of Pacific whitingsurimirdquo Journal of Food Science vol 58 no 5 pp 1050ndash10541993

[13] J W Park ldquoFunctional protein additives in surimi gelsrdquo Journalof Food Science vol 59 no 3 pp 525ndash527 1994

[14] S Benjakul W Visessanguan and C Srivilai ldquoGel propertiesof bigeye snapper (Priacanthus tayenus) surimi as affected by

setting and porcine plasma proteinsrdquo Journal of Food Qualityvol 24 no 5 pp 453ndash471 2001

[15] D D Hamann P M Amato M C Wu and E A FoegedingldquoInhibition of modori (gel weakening) in surimi by plasmahydrolysate and egg whiterdquo Journal of Food Science vol 55 pp665ndash669 1990

[16] K D Reppond and J K Babbitt ldquoProtease inhibitors affectphysical properties of arrowtooth flounder and walleye pollocksurimirdquo Journal of Food Science vol 58 pp 96ndash98 1993

[17] V C Weerasinghe M T Morrissey and H An ldquoCharacteriza-tion of active components in food-grade proteinase inhibitorsfor surimi manufacturerdquo Journal of Agricultural and FoodChemistry vol 44 no 9 pp 2584ndash2590 1996

[18] C-Y Yang ldquoEffect of the addition of bovine plasma on thequality properties of steamed fish pasterdquo The Korean Journal ofFood and Nutrition vol 21 pp 518ndash523 2008

[19] K Duangmal and A Taluengphol ldquoEffect of protein additivessodium ascorbate and microbial transglutaminase on the tex-ture and colour of red tilapia surimi gelrdquo International Journalof Food Science amp Technology vol 45 no 1 pp 48ndash55 2010

[20] S BenjakulW Visessanguan and C Chantarasuwan ldquoEffect ofporcine plasma protein and setting on gel properties of surimiproduced from fish caught inThailandrdquo LWT- Food Science andTechnology vol 37 no 2 pp 177ndash185 2004

[21] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoCysteine proteinase inhibitor from chicken plasma Fractiona-tion characterization and autolysis inhibition of fish myofibril-lar proteinsrdquo Food Chemistry vol 101 no 4 pp 1647ndash1657 2007

[22] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoEffect of chicken plasma protein and some protein additiveson proteolysis and gel-forming ability of sardine (SardinellaGibbosa) surimirdquo Journal of Food Processing and Preservationvol 31 no 4 pp 492ndash516 2007

[23] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoRheological and textural properties of pacific whiting surimigels as influenced by chicken plasmardquo International Journal ofFood Properties vol 11 no 4 pp 820ndash832 2008

[24] M Sugiyama T Mishiro Y Tsukamasa T Suzuki and KTakama ldquoPuncture properties of kamaboko with ovomucoidpasteurized at several temperaturesrdquo Nippon Suisan Gakkaishivol 64 no 1 pp 76ndash81 1998

[25] M Sugiyama T Mishiro Y Tsukamasa et al ldquoPhysical prop-erties of Kamaboko with ovomucoid pasteurized at severaltemperaturesrdquo Nippon Suisan Gakkaishi vol 64 no 1 pp 82ndash87 1998

[26] J Yongsawatdigul and P Piyadhammaviboon ldquoInhibition ofautolytic activity of lizardfish surimi by proteinase inhibitorsrdquoFood Chemistry vol 87 no 3 pp 447ndash455 2004

[27] L Campo-Deano and C Tovar ldquoThe effect of egg albumen onthe viscoelasticity of crab sticks made from Alaska pollock andPacific whiting surimirdquo Food Hydrocolloids vol 23 no 7 pp1641ndash1646 2009

[28] A Hunt J W Park and A Handa ldquoEffect of various types ofegg white on characteristics and gelation of fish myofibrillarproteinsrdquo Journal of Food Science vol 74 no 9 pp C683ndashC6922009

[29] S Rawdkuen and S Benjakul ldquoWhey protein concentrateAutolysis inhibition and effects on the gel properties of surimiprepared from tropical fishrdquo Food Chemistry vol 106 no 3 pp1077ndash1084 2008

26 Journal of Food Quality

[30] Y Ruttanapornvareesakul K Somjit A Otsuka et al ldquoCry-oprotective effects of shrimp head protein hydrolysate on gelforming ability and protein denaturation of lizardfish surimiduring frozen storagerdquo Fisheries Science vol 72 no 2 pp 421ndash428 2006

[31] D K Li H Lin and SM Kim ldquoEffect of rainbow trout (Oncor-hynchus mykiss) plasma protein on the gelation of Alaska pol-lock (Theragra chalcogramma) surimirdquo Journal of Food Sciencevol 73 no 4 pp C227ndashC234 2008

[32] A Hernandez-Briones G Velazquez M Vazquez and J ARamırez ldquoEffects of adding fish gelatin onAlaska pollock surimigelsrdquo Food Hydrocolloids vol 23 no 8 pp 2446ndash2449 2009

[33] T Yin Z H Reed and J W Park ldquoGelling properties of surimias affected by the particle size of fish bonerdquo LWT- Food Scienceand Technology vol 58 no 2 pp 412ndash416 2014

[34] T Yin and J W Park ldquoTextural and rheological properties ofPacific whiting surimi as affected by nano-scaled fish bone andheating ratesrdquo Food Chemistry vol 180 pp 42ndash47 2015

[35] M R Fowler and J W Park ldquoEffect of salmon plasma proteinon Pacific whiting surimi gelation under various ohmic heatingconditionsrdquo LWT- Food Science and Technology vol 61 no 2pp 309ndash315 2015

[36] M R Fowler and J W Park ldquoSalmon blood plasma Effectiveinhibitor of protease-laden Pacific whiting surimi and salmonmincerdquo Food Chemistry vol 176 pp 448ndash454 2015

[37] S Klomklao S Benjakul H Kishimura K Osako and BK Simpson ldquoTrypsin inhibitor from yellowfin tuna (Thunnusalbacores) roe Effects on gel properties of surimi from bigeyesnapper (Priacanthus macracanthus)rdquo LWT- Food Science andTechnology vol 65 pp 122ndash127 2016

[38] N K Vate and S Benjakul ldquoEffect of the mixtures of squid inktyrosinase and tannic acid on properties of sardine surimi gelrdquoJournal of Food Science and Technology vol 53 no 1 pp 411ndash420 2016

[39] T Yamashita ldquoEffects of commercial soybean protein andwheat gluten as subsidiary materials on physical properties ofkamabokordquo Nippon Shokuhin Kogyo Gakkaishi vol 38 no 12pp 883ndash890 1991

[40] K H Chung and C M Lee ldquoFunction of nonfish proteins insurimi-based gel productsrdquo Korean Journal of Society of FoodScience vol 10 pp 146ndash150 1994

[41] K-H Chung and C-M Lee ldquoEvaluation of wheat gluten andmodified starches for their texture-modifying and freeze-thawstabilizing effects on surimi based-productsrdquo Journal of FoodScience and Nutrition pp 190ndash195 1996

[42] S Benjakul S Karoon and A Suwanno ldquoInhibitory effects oflegume seed extracts on fish proteinasesrdquo Journal of the Scienceof Food and Agriculture vol 79 no 13 pp 1875ndash1881 1999

[43] S Benjakul W Visessanguan and P Thummaratwasik ldquoInhi-bition of gel weakening of threadfin bream surimi using Thailegume seed proteinase inhibitorsrdquo Journal of Food Biochem-istry vol 24 no 5 pp 363ndash380 2000

[44] A Oujifard S Benjakul M Ahmad and J Seyfabadi ldquoEffect ofbambara groundnut protein isolate on autolysis and gel prop-erties of surimi from threadfin bream (Nemipterus bleekeri)rdquoLWT- Food Science and Technology vol 47 no 2 pp 261ndash2662012

[45] Y Luo RKuwaharaMKaneniwa YMurata andMYokoyamaldquoEffect of soy protein isolate on gel properties of Alaska pollockand common carp surimi at different setting conditionsrdquoJournal of the Science of Food and Agriculture vol 84 no 7 pp663ndash671 2004

[46] Y Luo H Shen D Pan and G Bu ldquoGel properties of surimifrom silver carp (Hypophthalmichthys molitrix) as affected byheat treatment and soy protein isolaterdquo Food Hydrocolloids vol22 no 8 pp 1513ndash1519 2008

[47] C Cardoso B Ribeiro and R Mendes ldquoEffects of dietary fibreandmicrobial transglutaminase addition on the rheological andtextural properties of protein gels from different fish speciesrdquoJournal of Food Engineering vol 113 no 4 pp 520ndash526 2012

[48] T Kudre S Benjakul and H Kishimura ldquoEffects of proteinisolates from black bean and mungbean on proteolysis and gelproperties of surimi from sardine (Sardinella albella)rdquo LWT-Food Science and Technology vol 50 no 2 pp 511ndash518 2013

[49] S Klomklao and S Benjakul ldquoEffect of trypsin inhibitor inadzuki bean (Vigna angularis) on proteolysis and gel propertiesof threadfin bream (Nemipterus bleekeri)rdquo LWT- Food Scienceand Technology vol 63 no 2 pp 906ndash911 2015

[50] S Konoo H Ogawa and N Iso ldquoEffects of addition of amyloseand amylopectin on the breaking strength of fish meat gelrdquoNippon Suisan Gakkaishi vol 64 no 1 pp 69ndash75 1998

[51] C-S Kong H Ogawa and N Iso ldquoRheological analysis of theeffect of gelatinization of starch added to fish-meat gel based onvolume changesrdquo Fisheries Science vol 65 no 6 pp 930ndash9361999

[52] B-Y Kim W-W Kim and B Yoo ldquoEffect of native and acety-lated sweet potato starch on rheological properties of compositesurimi solrdquo Journal of Food Science and Nutrition vol 13 no 3pp 245ndash248 2008

[53] B-J Yoo ldquoThe effects of alkaline treatment and potato-starchcontent on the quality of fishmeat paste products prepared fromPacific sandlance Ammodytes personatus Girardrdquo Fisheries andAquatic Sciences vol 14 no 3 pp 161ndash167 2011

[54] S M Cho M S Yoon and S-B Kim ldquoEffects of rice flourmilling types and addition methods on rheological and sensoryproperties of surimi productsrdquo Korean Journal of Fisheries andAquatic Sciences vol 46 no 2 pp 139ndash146 2013

[55] Y-M Kwon and J-S Lee ldquoA study on the quality characteristicsof fish cakes containing rice flourrdquo Korean Journal of HumanEcology vol 22 no 1 pp 189ndash200 2013

[56] M Yoon J-S Kim D Kim J Jo and S Cho ldquoOptimization ofthe processing conditions for the preparation of surimi productscontaining rice flourrdquo Fisheries and Aquatic Sciences vol 17 no2 pp 167ndash173 2014

[57] J A Ramırez M Barrera O G Morales and M VazquezldquoEffect of xanthan and locust bean gums on the gelling prop-erties of myofibrillar proteinrdquo Food Hydrocolloids vol 16 no 1pp 11ndash16 2002

[58] A M Barrera J A Ramırez J J Gonzalez-Cabriales and MVazquez ldquoEffect of pectins on the gelling properties of surimifrom silver carprdquo Food Hydrocolloids vol 16 no 5 pp 441ndash4472002

[59] S Benjakul W Visessanguan S Phatchrat and M TanakaldquoChitosan affects transglutaminase-induced surimi gelationrdquoJournal of Food Biochemistry vol 27 no 1 pp 53ndash66 2003

[60] M A Iglesias-Otero J Borderıas and C A Tovar ldquoUse ofKonjac glucomannan as additive to reinforce the gels from low-quality squid surimirdquo Journal of Food Engineering vol 101 no3 pp 281ndash288 2010

[61] S-H Eom J-A Kim B-Y Son et al ldquoEffects of carrageenanon the gelatinization of salt-based surimi gelsrdquo Fisheries andAquatic Sciences vol 16 no 3 pp 143ndash147 2013

Journal of Food Quality 27

[62] S H Choi and S M Kim ldquoQuality properties of giant squid(Dosidicus gigas) surimi-based product manufactured withAmorphophallus konjac flourrdquo Korean Journal of Food Scienceand Technology vol 44 no 4 pp 422ndash427 2012

[63] D Cando B Herranz A J Borderıas and H M MorenoldquoEffect of high pressure on reduced sodium chloride surimigelsrdquo Food Hydrocolloids vol 51 pp 176ndash187 2015

[64] D-S Kim and Y-H Park ldquoEffect of food humectants onlowering water activity of casing kamaboko 1 Effect of loweringwater activity of sodium chloride sugars and polyolsrdquo Bulletinof the Korean Fisheries Society vol 14 pp 139ndash147 1981

[65] D-S Kim and Y-H Park ldquoEffect of food humectant on lower-ingwater activity of casing kamaboko 2 Effect of loweringwateractivity of starch glycine and sodium lactate and prediction ofthe water activity lowing ability of humectantsrdquo Bulletin of theKorean Fisheries Society vol 15 pp 74ndash82 1982

[66] G L Sanchez Pascua M R Casales and M I Yeannes ldquoInflu-ence of water and glycerol contents on the aw of fish pastesrdquoJournal of Aquatic Food Product Technology vol 10 no 1 pp89ndash100 2001

[67] E Niwa K Tsujimoto and S Kanoh ldquoKamaboko gel-strength-ening effect of polyuronides and other polysaccharidesrdquoNipponSuisan Gakkaishi vol 58 pp 85ndash88 1992

[68] R Yoshinaka M Shiraishi and S Ikeda ldquoEffect of AscorbicAcid on theGel Formation of FishMeatrdquoBulletin of the JapaneseSociety for the Science of Fish vol 38 no 5 pp 511ndash515 1972

[69] H G Lee C M Lee K H Chung and S A Lavey ldquoSodiumascorbate affects surimi gel-forming propertiesrdquo Journal of FoodScience vol 57 pp 1343ndash1347 1992

[70] Y Park S D Kelleher D J McClements and E A DeckerldquoIncorporation and stabilization of omega-3 fatty acids insurimi made from cod Gadus morhuardquo Journal of Agriculturaland Food Chemistry vol 52 no 3 pp 597ndash601 2004

[71] E Okazaki Y Yamashita and Y Omura ldquoEmulsification of fishoil in surimi by high-speed mixing and improvement of gel-forming abilityrdquo Nippon Suisan Gakkaishi vol 68 no 4 pp547ndash553 2002

[72] H Fukushima E Okazaki S Noda and Y Fukuda ldquoChangesin physical properties water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oilrdquoNippon Shokuhin Kagaku Kogaku Kaishi vol 54 no 1 pp 39ndash44 2007

[73] B N Pietrowski R Tahergorabi and J Jaczynski ldquoDynamicrheology and thermal transitions of surimi seafood enhancedwith 120596-3-rich oilsrdquo Food Hydrocolloids vol 27 no 2 pp 384ndash389 2012

[74] A K Balange S Benjakul and S Maqsood ldquoGel strengtheningeffect of wood extract on surimi produced frommackerel storedin icerdquo Journal of Food Science vol 74 no 8 pp C619ndashC6272009

[75] N Buamard and S Benjakul ldquoImprovement of gel properties ofsardine (Sardinella albella) surimi using coconut husk extractsrdquoFood Hydrocolloids vol 51 pp 146ndash155 2015

[76] A K Balange and S Benjakul ldquoEffect of oxidised phenolic com-pounds on the gel property of mackerel (Rastrelliger kanagurta)surimirdquo LWT- Food Science and Technology vol 42 no 6 pp1059ndash1064 2009

[77] A Balange and S Benjakul ldquoEnhancement of gel strength ofbigeye snapper (Priacanthus tayenus) surimi using oxidisedphenolic compoundsrdquo Food Chemistry vol 113 no 1 pp 61ndash702009

[78] Y A Arfat and S Benjakul ldquoEffect of zinc sulphate on gellingproperties of phosphorylated protein isolate from yellow stripetrevallyrdquo Food Chemistry vol 141 no 3 pp 2848ndash2857 2013

[79] M-S Bae and S-C Lee ldquoQuality characteristics of fried fishpaste containing anchovy powderrdquo Journal of the Korean Societyof Food Science and Nutrition vol 36 no 9 pp 1188ndash1192 2007

[80] M-S Bae J-U Ha and S-C Lee ldquoQuality properties of highcalcium fish paste containing anchovyrdquo Korean Journal of Foodand Cookery Science vol 23 pp 561ndash566 2007

[81] H-S Cho and K-H Kim ldquoQuality characteristics of fish pastecontaining skate (Raja kenojei) powderrdquo Journal of the EastAsian Society of Dietary Life vol 21 pp 808ndash813 2011

[82] Y H Park E Y Bum E R Jeon and LH Jung ldquoEffect of addedskate (Raja kenojei) on the quality characteristics of steamedfishmeat pasterdquo Food Science and Biotechnology vol 23 no 5 pp1453ndash1458 2014

[83] S-M Park B-B Lee Y-M Hwang and S-C Lee ldquoQualityproperties of fish paste containing Styela clavardquo Journal of theKorean Society of Food Science and Nutrition vol 35 pp 908ndash911 2006

[84] S-Y Choi E-Y Choi K-E Lee A-S Song S-H Park and S-C Lee ldquoPreparation and quality analysis of fish paste containingStyela clava tunicrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 41 no 11 pp 1591ndash1595 2012

[85] S-M Park H-K Seo and S-C Lee ldquoPreparation and qualityproperties of fish paste containing Styela plicatardquo Journal of theKorean Society of Food and Nutrition vol 35 pp 1256ndash12592006

[86] J-S Seo and H-S Cho ldquoQuality characteristics of fish pastewith shrimp powderrdquo Korean Journal of Food Preservation vol19 pp 519ndash524 2012

[87] H-S Cho and K-H Kim ldquoQuality properties of fish pastecontaining green laver powderrdquo Journal of the Korean Societyof Food Culture vol 29 pp 421ndash427 2014

[88] I-D Park ldquoQuality characteristics of fish paste containingLagocephalus lunaris powderrdquo Journal of the Korean Society ofFood Culture vol 28 pp 657ndash663 2013

[89] I Park ldquoQuality properties of fish paste containingCapsosiphonfulvescens powderrdquo Journal of The Korean Society of FoodCulture vol 31 no 4 pp 357ndash363 2016

[90] B-M Kim J-H Jung M-J Jung D-S Kim J-Y Jun and I-H Jeong ldquoThe quality characteristics and processing of fishpaste containing red snow crabChionoecetes japonicus leg-meatpowderrdquo Korean Journal of Fisheries and Aquatic Sciences vol49 pp 1ndash6 2016

[91] Y-J Shin and G-S Park ldquoQuality characteristics of fish-pastecontaining mulberry leaf powderrdquo Journal of the East AsianSociety of Dietary Life vol 15 pp 738ndash745 2005

[92] Y-J Shin ldquoQuality characteristics of fish paste containing lotus(Nelumbo nucifera) leaf powderrdquo Korean Journal of Food andCookery Science vol 23 pp 947ndash953 2007

[93] A D Thorat V R Joshi A U Pagarkar and A K BalangeldquoMicrowave pasteursation of fish paste product-Kamabokowith Beetroot and Spinachrdquo Ecology Environment and Conser-vation vol 13 no 1 pp 113ndash118 2007

[94] M-O Yang and E-J Cho ldquoQuality properties of surimi withadded citrus fruitsrdquo Journal of East Asian Society of Dietary Lifevol 17 pp 58ndash63 2007

[95] F Alakhrash U Anyanwu and R Tahergorabi ldquoPhysicochemi-cal properties of Alaska pollock (Theragra chalcograma) surimigels with oat branrdquo LWT- Food Science and Technology vol 66pp 41ndash47 2016

28 Journal of Food Quality

[96] J-S Kim and G-I Byun ldquoMaking fish paste with yam (Dios-corea japonica Thumb) powder and its characteristicsrdquo KoreanJournal of Culinary Research vol 15 pp 57ndash69 2009

[97] Y-J Shin J A Lee and G-S Park ldquoa Quality characteristics offish pastes containing Lycii fructus powderrdquo Journal of the EastAsian Society of Dietary Life vol 18 pp 22ndash28 2008

[98] D-W Shim J Jiang J-H Kim et al ldquoEffects of size adjustedwith red ginseng powders on quality of fish pastesrdquo Journal ofthe Korean Society of Food Science and Nutrition vol 41 no 10pp 1448ndash1453 2012

[99] Y-J Shin J A Lee and G-S Park ldquoQuality characteristics offish paste containing Angelicae gigantis Radix powderrdquo KoreanJournal of Food and Cookery Science vol 24 pp 699ndash705 2008

[100] S Choi ldquoQuality characteristics of fish paste containing Cur-cuma longa L powderrdquo The Korean Journal of Food and Nutri-tion vol 25 no 4 pp 833ndash841 2012

[101] J-A Jang H-A Kim and S-K Choi ldquoQuality characteristicsof fish cake made with silver pomfret (Pampus argenteus) withadded wasabi powderrdquo Journal of the East Asian Society ofDietary Life vol 20 pp 103ndash112 2010

[102] Y-J Shin K-S Kim and G-S Park ldquoTexture and sensorycharacteristics of fish paste containing white Poria cocos wolfpowderrdquo Korean J Food Cookery Sci vol 25 pp 119ndash125 2009

[103] J-U Ha S-G Koo H-Y Lee Y-M Hwang and S-C LeeldquoPhysical properties of fish paste containing Agaricus bisporusrdquoKorean Journal of Food Science and Technology vol 33 pp 451ndash454 2001

[104] S-G Koo Y-K Ryu Y-M Hwang J-U Ha and S-C LeeldquoQuality properties of fish-paste containing enoki mushroom(Flammuilna velutipes)rdquo Journal of the Korean Society of FoodScience and Nutrition vol 30 pp 288ndash291 2001

[105] M-H Son S-Y Kim J-U Ha and S-C Lee ldquoTexture prop-erties of surimi gel containing shiitake mushroom (Lentinusedodes)rdquo Journal of the Korean Society of Food Science andNutrition vol 32 pp 859-853 2003

[106] S-Y Kim M-H Son J-U Ha and S-C Lee ldquoPreparationand characterization of fried surimi gel containing king oystermushroom (Pleurotus eryngii)rdquo Journal of the Korean Society ofFood Science and Nutrition vol 32 pp 855ndash858 2003

[107] S I Chung S Y Kim Y J Nam andM Y Kang ldquoDevelopmentof surimi gel from king oyster mushroom and cuttlefish meatpasterdquo Food Science and Biotechnology vol 19 no 1 pp 51ndash562010

[108] S K Jin J H Park and S J Hur ldquoEffect of substituting surimiwith spent laying hen meat on the physicochemical character-istics of fried fish pasterdquo Food and Bioprocess Technology vol 7no 3 pp 901ndash908 2014

[109] A Debusca R Tahergorabi S K Beamer K E Matak and JJaczynski ldquoPhysicochemical properties of surimi gels fortifiedwith dietary fiberrdquo Food Chemistry vol 148 pp 70ndash76 2014

[110] H-S Yook J-W Lee H-J Lee B-S Cha S-Y Lee and M-W Byun ldquoQuality properties of fish paste prepared with refineddietary fiber from ascidian (Halocynthia roretzi) tunicrdquo Journalof the Korean Society of Food Science and Nutrition vol 29 pp642ndash646 2000

[111] A Debusca R Tahergorabi S K Beamer S Partington andJ Jaczynski ldquoInteractions of dietary fibre and omega-3-rich oilwith protein in surimi gels developed with salt substituterdquo FoodChemistry vol 141 no 1 pp 201ndash208 2013

[112] C Sell S Beamer J Jaczynski and K E Matak ldquoSensorycharacteristics and storage quality indicators of surimi franks

nutritionally enhanced with omega-3 rich flaxseed oil andsalmon oilrdquo International Journal of Food Science amp Technologyvol 50 no 1 pp 210ndash217 2015

[113] T Chang C Wang X Wang L Shi H Yang and M CuildquoEffects of soybean oil moisture and setting on the textural andcolor properties of surimi gelsrdquo Journal of Food Quality vol 38no 1 pp 53ndash59 2015

[114] J-S Kim M-L Cho and M-S Heu ldquoQuality improvement ofheat-induced surimi gel using calcium powder of cuttle Sepiaesculenta bone treated with acetic acidrdquo Journal of the KoreanFisheries Society vol 36 pp 198ndash203 2003

[115] G-W Kim G-H Kim J-S Kim et al ldquoQuality characteristicsof fried fish paste of Alaska pollack meat paste added withpropolisrdquo Journal of the Korean Society of Food Science andNutrition vol 37 no 4 pp 485ndash489 2008

[116] G-W Kim G-H Kim J-S Kim et al ldquoQuality of fried fishpaste prepared with sand-lance (Hypoptychus dybowskii) meatand propolis additiverdquo Journal of the Korean Fisheries Societyvol 41 pp 170ndash175 2008

[117] B Park H Cho and S Park ldquoStudy on quality characteristicsof fish paste containing cheonggukjang powderrdquo Journal of TheKorean Society of Food Culture vol 30 no 2 pp 213ndash219 2015

[118] SMiyao T Shindoh KMiyamori and T Arita ldquoEffects of highpressurization on the growth of bacteria derived from surimi(fish paste)rdquo Nippon Shokuhin Kogyo Gakkaishi vol 40 pp478ndash484 1993

[119] A Malicki Z Sysak S Bruzewicz J Zrodłowska-Danek andM Szpak ldquoApplication of high hydrostatic pressure to extendthe shelf-life of traditionally produced fish pasterdquo MedycynaWeterynaryjna vol 66 pp 695ndash698 2010

[120] J-H Kim J-Y Jeon S-R Ryu et al ldquoMicrobial quality andphysiochemical changes of grilled fish paste in a group-mealservice affected by gamma-irradiationrdquo Korean Journal of FoodPreservation vol 11 pp 522ndash529 2004

[121] H-O Cho J-H Kwon M-W Byun and M-K Lee ldquoPreserva-tion of fried fish-paste by Irradiationrdquo Korean Journal of FoodScience and Technology vol 17 pp 474ndash481 1985

[122] H-Y Shin Y-J Lee I-Y Park J-Y Kim S-J Oh and K BSong ldquoEffect of chlorine dioxide treatment onmicrobial growthand qualities of fish paste during storagerdquo Journal of the KoreanSociety for Applied Biological Chemistry vol 50 pp 42ndash47 2007

[123] S S YoonH Kim YM Lee E J Jeong andY J Cha ldquoShelf-lifeextension effects of fish paste product by adding pepper extractrdquoin Proceedings of the Korean Nutrition Society Conference p 216Seoul Korea 2001

[124] E-S Ahn M-S Kim and D-H Shin ldquoScreening of natu-ral antimicrobial edible plant extract for dooboo fish pastemakkoli spoilage microorganismrdquo Korean Journal of FoodScience and Technology vol 26 pp 733ndash739 1994

[125] Y-M Kim B-H Lee S-H Lee I-S Shin and T-S LeeldquoThe preservative effect of egg white lysozyme added surimiproductsrdquo Bulletin of the Korean Fisheries Society vol 21 pp269ndash275 1988

[126] S-H Cho I-S Joo I-W Seo and Z-W Kim ldquoPreservativeeffect of grapefruit seed extract on fish meat productrdquo Journalof Food Hygiene and Safety vol 6 pp 67ndash72 1991

[127] E-T Jeong M-Y Park E-W Lee U-T Park and D-S ChangldquoAntimicrobial characteristics against spoilage microorganismsand food preservative effect of cinnamon (Cinnamomum cassiaBlume) bark extractrdquo Korean Journal of Life Science vol 8 pp648ndash653 1998

Journal of Food Quality 29

[128] D-S Chang H-R Cho H-S Lee M-Y Park and S-M LimldquoDevelopment of alginic acid hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 823ndash826 1998

[129] H-R Cho D-S Chang W-D Lee E-T Jeong and E-WLee ldquoUtilization of chitosan hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 817ndash822 1998

[130] K Yamazaki T Tashiro S Shirahama J-Y Jun and Y KawaildquoGrowth inhibition of spore-forming bacteria in fish-pasteproducts by Nisinrdquo Nippon Shokuhin Kagaku Kogaku Kaishivol 61 no 2 pp 70ndash76 2014

[131] K Hashimoto M L Bari Y Inatsu S Kawamoto and J ShimaldquoBiopreservation of kamaboko (steamed surimi) using pisci-colin KH1 produced by Carnobacteriummaltalomaticum KH1rdquoJapanese Journal of FoodMicrobiology vol 28 pp 193ndash200 2011

[132] S H Lee M S Lee S K Park D H Bae S D Ha and K BSong ldquoPhysical properties of protein films containing green teaextract and its antioxidant effect on fish paste productsrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1063ndash1067 2004

[133] G-O Lim Y-H Hong and K B Song ldquoIncorporating grape-fruit seed extract into Gelidium corneum-whey protein isolateblend packaging film increases the shelf life of fish paste -Research noterdquo Journal of Food Science and Nutrition vol 13no 4 pp 370ndash374 2008

[134] T C Lanier J Yongsawatdigul and P Carvajal-RondanellildquoSurimi gelation chemistryrdquo in Surimi and Surimi Seafood J WPark Ed pp 101ndash139Marcel Dekker NewYork NYUSA 2013

[135] M Kinoshita H Toyohara and Y Shimizu ldquoPurification andproperties of a novel latent proteinase showing myosin heavychain-degrading activity from threadfin-bream musclerdquo TheJournal of Biochemistry vol 107 no 4 pp 587ndash591 1990

[136] D H Wasson J K Babbitt and J S French ldquoCharacterizationof a heat stable protease from arrowtooth flounder Atheresthesstomiasrdquo Journal of Aquatic Food Product Technology vol 1 no3-4 pp 167ndash182 1993

[137] T A Seymour M T Morrissey M Y Peters and H An ldquoPuri-fication and characterization of pacific whiting proteasesrdquoJournal of Agricultural and Food Chemistry vol 42 no 11 pp2421ndash2427 1994

[138] H An V Weerasinghe T A Seymour and M T MorrisseyldquoCathepsin degradation of Pacific whiting surimi proteinrdquoJournal of Food Science vol 59 pp 1013ndash1017 1994

[139] AFDF Ground fish quality chart Alaska fisheries departmentfoundation Anchorage Alaska 1992

[140] G Sylvia S Larkin and M T Morrissey ldquoQuality and resourcemanagement bioeconomic analysis of the Pacific whitingindustryrdquo in Recent Advances inMarine Science and TechnologyO Bellwood H Choat and N Saxena Eds James CookUniversity Townsville QS Australia 1994

[141] S H Choi and S M Kim ldquoDevelopment of giant squid(Ommastrephes bartrami) surimi-based products with gel tex-ture enhancers and the effects of setting on gel qualityrdquo Journalof the Korean Society of Food Science and Nutrition vol 41 no7 pp 975ndash981 2012

[142] J A Ramırez R M Uresti G Velazquez and M VazquezldquoFood hydrocolloids as additives to improve the mechanicaland functional properties of fish products A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1842ndash1852 2011

[143] S-K Kim H-G Byun P-J Park and F Shahidi ldquoAngiotensinI converting enzyme inhibitory peptides purified from bovine

skin gelatin hydrolysaterdquo Journal of Agricultural and FoodChemistry vol 49 no 6 pp 2992ndash2997 2001

[144] I Kimura M Sugimoto K Toyoda N Seki K-I Arai andT Fujita ldquoA study on the cross-links reaction of myosin inkamaboko rsquosuwarirsquo gelsrdquo Nippon Suisan Gakkaisi vol 57 pp1386ndash1396 1991

[145] H An M Y Peters and T A Seymour ldquoRoles of endogenousenzymes in surimi gelationrdquo Trends in Food Science amp Technol-ogy vol 7 no 10 pp 321ndash327 1996

[146] R Nopianti N Huda andN Ismail ldquoA review on the loss of thefunctional properties of proteins during frozen storage and theimprovement of gel-forming properties of Surimirdquo AmericanJournal of Food Technology vol 6 no 1 pp 19ndash30 2011

[147] A M Martın-Sanchez C Navarro J A Perez-Alvarez and VKuri ldquoAlternatives for efficient and sustainable production ofsurimi A reviewrdquo Comprehensive Reviews in Food Science andFood Safety vol 8 no 4 pp 359ndash374 2009

[148] Korea Agro-Fisheries and Food Trade Corporation Processedfood segmented market survey-fish cake market Korea Agro-Fisheries and Food Trade Corporation Seoul Korea 2014

[149] D Kraft and A DerMarderosian The A-Z guide to food asmedicine CRC Press Boca Raton Fla USA 2016

[150] C V Morr and E A Foegeding ldquoComposition and function-ality of commercial whey and milk protein concentrates andisolates a status reportrdquo Food Technology vol 44 pp 100ndash1121990

[151] A Saiga T Okumura T Makihara et al ldquoAngiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chickenbreast muscle extractrdquo Journal of Agricultural and Food Chem-istry vol 51 no 6 pp 1741ndash1745 2003

[152] B Li F Chen X Wang B Ji and Y Wu ldquoIsolation and iden-tification of antioxidative peptides from porcine collagenhydrolysate by consecutive chromatography and electrosprayionization-mass spectrometryrdquo Food Chemistry vol 102 no 4pp 1135ndash1143 2007

[153] A Trampuz R M Prabhu T F Smith and L M BaddourldquoAvian Influenza A New Pandemic Threatrdquo Mayo ClinicProceedings vol 79 no 4 pp 523ndash530 2004

[154] M C Gomez-Guillen B Gimenez M E Lopez-Caballeroand M P Montero ldquoFunctional and bioactive properties ofcollagen and gelatin from alternative sources A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1813ndash1827 2011

[155] D Li X Fu and S M Kim ldquoProduction of chum salmoncystatin from the recombinant Saccharomyces cerevisiae opti-mized using response surface methodologyrdquo Biotechnology andBioprocess Engineering vol 15 no 2 pp 314ndash323 2010

[156] H Akazawa Y Miyauchi K Sakurada H Wasson and K DReppond ldquoEvaluation of protease inhibitors in Pacific whitingsurimirdquo Journal of Aquatic Food Product Technology vol 2 no3 pp 79ndash95 1994

[157] A Hunt K J K Getty and J W Park ldquoRoles of starch in surimiseafood A reviewrdquo Food Reviews International vol 25 no 4 pp299ndash312 2009

[158] T Suzuki Fish and Krill Protein Processing Technology AppliedScience Publishers London UK 1981

[159] C M Lee ldquoSurimi process technologyrdquo Food Technology vol38 pp 69ndash80 1984

[160] M C Wu D D Hamann and T C Lanier ldquoRheological andcalorimetric investigations of starch-fish protein systems duringthermal processingrdquo Journal of Texture Studies vol 16 pp 53ndash74 1985

30 Journal of Food Quality

[161] M C Wu T C Lanier and D D Hamann ldquoRigidity and vis-cosity changes of croaker actomyosin during thermal gelationrdquoJournal of Food Science vol 50 no 1 pp 14ndash19 1985

[162] S-K Kim S-T Yang and E-H Lee ldquoThe starch content of fish-paste products onmarketrdquo Journal of the Korean Society of FoodScience and Nutrition vol 7 pp 41-42 1978

[163] G AMacDonald T C Lanier and P A Caruajal ldquoStabilizationof protein in surimirdquo in Surimi and Surimi Seafood J W ParkEd pp 91ndash125 Marcel Dekker Inc New York NY USA 2000

[164] J A Ramırez I A Santos O G Morales M T Morrisseyand M Vazquez ldquoApplication of microbial transglutaminaseto improve mechanical properties of surimi from silver carputilizacionde transglutaminasa microbiana paramellora-las-propiedades mecanicas de surimide carpaplateada utiliza-cionde transglutaminasamicrobiana paramejorarlaspropieda-des mecanicas de surimide carpaplateadardquo Ciencia y TecnologıaAlimentaria vol 3 no 1 pp 21ndash28 2000

[165] M C Gomez-Guillen A J Borderıas and P MonteroldquoSalt nonmuscle proteins and hydrocolloids affecting rigiditychanges during gelation of giant squid (Dosidicus gigas)rdquoJournal of Agricultural and Food Chemistry vol 45 no 3 pp616ndash621 1997

[166] J W Park ldquoIngredient technology and formulation develop-mentrdquo in Surimi and Surimi Seafood J W Park Ed pp 91ndash125Marcel Dekker Inc New York NY USA 2000

[167] F Garcıa-Ochoa V E Santos J A Casas and E Gomez ldquoXan-than gum production recovery and propertiesrdquo BiotechnologyAdvances vol 18 no 7 pp 549ndash579 2000

[168] A I Rodrıguez-Hernandez and A Tecante ldquoDynamic vis-coelastic behavior of gellan- 120580 -carrageenan and gellan-xanthangelsrdquo Food Hydrocolloids vol 13 no 1 pp 59ndash64 1999

[169] J A Casas and F Garcıa-Ochoa ldquoSophorolipid production byCandida bombicola Medium composition and culture meth-odsrdquo Journal of Bioscience and Bioengineering vol 88 no 5 pp488ndash494 1999

[170] H J Lim ldquoA study on the calcium and sodium intakes andurinary calcium excretion of preschool children in BusanrdquoKorean Journal of Nutrition vol 34 pp 786ndash796 2001

[171] WHO ldquoDiet nutrition and the prevention of chronic diseasesReport of a joint WHOFAO expert consultationrdquo Tech RepWHO World Health Organization Geneva Switzerland 2003

[172] L K Dahl ldquoPossible role of salt intake in the development ofessential hypertensionrdquo International Journal of Epidemiologyvol 34 no 5 pp 967ndash972 2005

[173] H-K Jeong D-S Kim S-J Chun K-S Jo and Y-H ParkldquoEffect of food humectant on lowering water activity of casingKamaboko 3rdquo Bulletin of the Korean Fisheries Society vol 16 pp88ndash96 1983

[174] J Han E Kim M Cheong S Chee and K Chee ldquoBioavailabil-ity and digestibility of organic calcium sources by bone healthindexrdquo Journal of Nutrition and Health vol 43 no 1 pp 12ndash252010

[175] M K Lee ldquoA study of the bio-functional evaluation of Rajaskates caught in Huksando areardquo Journal of the Kwangju HealthCollege vol 21 pp 253ndash265 1996

[176] S H Cho Extraction and characterization of gelatin andantimicrobial peptide from skate (Raja kenojei) skins ChonnamNational University Gwangju Korea 2003

[177] J H Choi ldquoIsolation and purification of in chondroitin sulfatefrom skate cartilagerdquo Tech Rep Pukyong National UniversityBusan Korea 2004

[178] Y G Jo ldquoThe sterol composition of Styela clavardquo Journal of theKorean Fisheries Society vol 11 pp 97ndash101 1978

[179] S H Ahn ldquoExtraction of glycosaminoglycans from Styela clavatunicrdquo Biotechnology and Bioprocess Engineering vol 18 pp180ndash185 2003

[180] J J Kim S J Kim S H Kim H R Park and S C LeeldquoAntioxidant and anticancer activities of extracts from Styelaclava according to the processing methods and solventsrdquoJournal of the Korean Society of Food Science and Nutrition vol35 pp 278ndash283 2006

[181] T Aoki K Takata and N Kunisaki ldquoComparison of nutrientcomponents of six species of wild and cultured fishesrdquo Bulletinof the Japanese Society for the Science of Fish vol 57 pp 1927ndash1934 1991

[182] Committee Donguibogam Translated Donguibogam Bubin-munwha Press Seoul Korea 1999

[183] Y-K Park H-J Kim and M-H Kim ldquoQuality characteristicsof fried fish paste added with ethanol extract of onionrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1049ndash1055 2004

[184] G L Dong J J Hyun and E-R Woo ldquoAntimicrobial prop-erty of (+)-lyoniresinol-3120572-O-120573-D- glucopyranoside isolatedfrom the root bark of Lycium chinense Miller against humanpathogenic microorganismsrdquo Archives of Pharmacal Researchvol 28 no 9 pp 1031ndash1036 2005

[185] C C Wang S C Chang B S Inbaraj and B H ChenldquoIsolation of carotenoids flavonoids and polysaccharides fromLycium barbarum L and evaluation of antioxidant activityrdquoFood Chemistry vol 120 no 1 pp 184ndash192 2010

[186] Z Zhang X Liu T Wu et al ldquoSelective suppression of cervicalcancer Hela cells by 2-O-120573-d- glucopyranosyl-l-ascorbic acidisolated from the fruit of Lycium barbarum Lrdquo Cell Biology andToxicology vol 27 no 2 pp 107ndash121 2011

[187] J S Kil M G Kim H M Choi et al ldquoInhibitory effects ofAngelicae GigantisRadix on osteoclast formationrdquo PhytotherapyResearch vol 22 no 4 pp 472ndash476 2008

[188] ANiranjan andD Prakash ldquoChemical constituents and biolog-ical activities of turmeric (Curcuma longa L) - a reviewrdquo Journalof Food Science and Technology vol 45 pp 109ndash116 2008

[189] K S Kim M G Choung and S H Park ldquoQuantitativedetermination and stability of curcuminoid pigments fromturmeric (Curcuma longaL) rootrdquo Korean Journal of CropScience vol 50 pp 211ndash215 2005

[190] I S Shin and J M Lee ldquoStudy on antimicrobial and antimuta-genic activity of horseradish (Wasabia japonica) root extractsrdquoJournal of the Korean Fisheries Society vol 31 pp 835ndash841 1998

[191] Y J ChoA study on the antioxidative and antimicrobial activitiesof wasabi (Wasabia koreana Cruciferae) extracts [PhD thesis]Sungshin Womens University Seoul Korea 2008

[192] A-S Kang T-S Kang H-R Shon et al ldquoStudies on improve-ment of artificial cultivation and antioxidative activity of Poriacocosrdquo The Korean Journal of Mycology vol 27 pp 378ndash3801999

[193] J-H Lee Y J Lee J-K Shin et al ldquoEffects of triterpenoidsfrom Poria cocos Wolf on the serotonin type 3A receptor-mediated ion current in Xenopus oocytesrdquo European Journal ofPharmacology vol 615 no 1ndash3 pp 27ndash32 2009

[194] K R Im M J Kim T K Jung and K S Yoon ldquoAnalysisof isoflavonoid contents in Astragalus membranaceus Bungecultivated in different areas and at various agesrdquo The KoreanSociety for Biotechnology and Bioengineering vol 25 pp 271ndash276 2010

Journal of Food Quality 31

[195] Y E Lee and S H Hong Oriental Medicine Food MaterialsKyomunsa Seoul Korea 2003

[196] D H Kim ldquoQuality characteristics of fish paste prepared withAstragalus membranaceus powderrdquo Food Engineering Progressvol 15 pp 362ndash369 2011

[197] S-E Kim B S Hwang J-G Song S W Lee I-K Lee andB-S Yun ldquoNew bioactive compounds from Korean nativemushroomsrdquoMycobiology vol 41 no 4 pp 171ndash176 2013

[198] National Institute of Agricultural Science The Mushrooms inKorea Dongbang Media Co Ltd Seoul Korea 2004

[199] Y-J Gao M Zhang and W-P Chen ldquoStudy on processing offish paste with waste of grass carprdquo Journal of Food Science andBiotechnology vol 31 pp 1031ndash1038 2012

[200] S Tolasa C M Lee and S Cakli ldquoPhysical and oxidativestabilization of omega-3 fatty acids in surimi gelsrdquo Journal ofFood Science vol 75 no 3 pp C305ndashC310 2010

[201] B N Pietrowski R Tahergorabi K E Matak J C Tou andJ Jaczynski ldquoChemical properties of surimi seafood nutrifiedwith 120596-3 rich oilsrdquo Food Chemistry vol 129 no 3 pp 912ndash9192011

[202] S H Kim J L Yang and Y S Song ldquoPhysiological function ofcheonggukjangrdquo Food Industry and Nutrition vol 4 pp 40ndash461999

[203] R Walker ldquoToxicology of sorbic acid and sorbatesrdquo Food Addi-tives amp Contaminants Part A vol 7 no 5 pp 671ndash676 1990

[204] B R Thakur and T R Patel ldquoSorbates in fish and fish productsmdasha reviewrdquo Food Reviews International vol 10 no 1 pp 93ndash1071994

[205] C-Y Wang H-W Huang C-P Hsu and B B Yang ldquoRecentadvances in food processing using high hydrostatic pressuretechnologyrdquo Critical Reviews in Food Science and Nutrition vol56 no 4 pp 527ndash540 2016

[206] J H Kwon M W Byun and J S Kim ldquoMicrobiological andorganoleptic qualities of boiled-dried anchovies during post-irradiation periodrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 25 pp 283ndash287 1996

[207] J Noh and J H Kwon ldquoThe quality and thermoluminescenceproperties of dried pollack during storage following irradia-tionrdquo Korean Journal of Food Science and Technology vol 36pp 711ndash716 2004

[208] I Tukenmez M S Ersen A T Bakioglu A Bicer and VPamuk ldquoDose dependent oxidation kinetics of lipids in fish dur-ing irradiation processingrdquo Radiation Physics and Chemistryvol 50 no 4 pp 407ndash414 1997

[209] T Sakai and T Yamaguchi ldquoEffects of yuzu peel addition onthe lipid oxidation in kamaboko Effects of yuzu peel additionon the lipid oxidation in kamabokordquo Bulletin of the Faculty ofAgriculture Miyazaki University vol 57 pp 101-102 2011

[210] E-H Lee K-S Oh J-G Koo H-S Park S-Y Cho and Y-J Cha ldquoStudies on processing and keeping quality of retortpouched foods (3) Preparation and keeping quality of retortpouched fried mackerel meat pasterdquo Bulletin of the KoreanFisheries Society vol 17 pp 373ndash382 1984

[211] J-H Ha E-H Lee J-S Kim S-G Ji and J-G Koo ldquoA study onthe thermal treatment conditions of retort pouched fried fish-paste 1 Influence of thermal treatment conditions on qualityrdquoBulletin of the Korean Fisheries Society vol 20 pp 573ndash581 1987

[212] P Guenneugues and J Ianelli ldquoSurimi resources and marketrdquoin Surimi and surimi seafood J W Park Ed pp 25ndash53 MarcelDekker Inc New York NY USA 2013

Research ArticleDevelopment of a Chemically Defined Medium forBetter Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31

Wenli Liu12 Lanwei Zhang23 and Huaxi Yi3

1College of Chemistry and Environmental Engineering Shenzhen University Shenzhen Guangdong 518060 China2School of Food Science amp Technology Harbin Institute of Technology 73 HuangHe Avenue Harbin Heilongjiang 150090 China3College of Food Science and Engineering Ocean University of China Yushan Road 5 Qingdao Shandong 266100 China

Correspondence should be addressed to Lanwei Zhang zhanglwhiteducn and Huaxi Yi yihxouceducn

Received 31 March 2017 Revised 17 July 2017 Accepted 2 August 2017 Published 6 September 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Wenli Liu et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The macro- and micronutrients in traditional medium such as MRS used for cultivating lactic acid bacteria especially forbacteriocin production have not been defined preventing the quantitative monitoring of metabolic flux during bacteriocinbiosynthesis To enhance Enterocin Y31 production and simplify steps of separation and purification we developed a simplifiedchemically definedmedium (SDM) for the growth of Enterococcus faeciumY31 and production of its bacteriocin Enterocin Y31Wefound that the bacterial growthwas unrelated toEnterocinY31 production inMRS therefore both the growth rate and theEnterocinY31 production were set as the index for investigation Single omission experiments revealed that 5 gL NaCl five vitamins twonucleic acid basesMgSO

4sdot7H2OMnSO

4sdot4H2OKH

2PO4 K2HPO4 CH3COONa fourteen amino acids and glucosewere essential

for the strainrsquos growth and Enterocin Y31 production Thus a novel simplified and defined medium (SDM) was formulated with30 components in total Consequently Enterocin Y31 production yield was higher in SDM as compared to either MRS or CDMSDM improved the Enterocin Y31 production and simplified the steps of purification (only two steps) which has broad potentialapplications

1 Introduction

Bacteriocins are ribosomally synthesised antimicrobial pro-teins or protein complexes that inhibit other bacteria andthey either have a narrow antimicrobial spectrum (againstthe same species) or broad antimicrobial spectrum (againstacross genera) [1 2] Bacteriocin produced by lactic acidbacteria (LAB) is generally regarded as safe (GRAS) andQualified Presumption of Safety (QPS) status [3 4] andit is a desirable trait as a food additive for extending theshelf-life of the fermented food and controlling the safetyof foods [5 6] Based on their molecular structure bac-teriocins can be divided into four groups class I bacte-riocins contain posttranslational modifications (lantibioticsand molecular weight le 5 kDa) class II bacteriocins areunmodified and include small heat-stable nonlanthionine-containing peptides [7] The third class includes large

heat-labile bacteriocins Finally the fourth class comprisescomplex bacteriocins containing a protein moiety with oneor more other lipids or carbohydrates [8] Most bacteriocinsproduced by the Enterococcus faecium group of LAB are classII bacteriocins One subgroup class IIa contains bacteriocinswith certain sequence motifs in their N-terminal halves andis active against the food pathogen Listeria monocytogenes[9] Class IIa bacteriocins have become a focus of researchowing to their low molecular weight good dispersity andhigh thermostability This is also a case of Enterocin Y31produced by E faecium Y31 in the current work [10]

Enterocin Y31 is a class IIa bacteriocin produced byE faecium Y31 [11] Previous research results showed thatEnterocin Y31 had broad spectrum inhibition activity againstBacillus subtilis ATCC 6633 Escherichia coli ATCC 25922Listeria monocytogenes ATCC 19111 Bacillus cereus CICC20463 Staphylococcus aureus and Salmonella enterica serovar

HindawiJournal of Food QualityVolume 2017 Article ID 9017452 8 pageshttpsdoiorg10115520179017452

2 Journal of Food Quality

TyphimuriumATCC 14028The isoelectric point of EnterocinY31 was 825 it was stable in both acidity and alkalescenceconditions hence Enterocin Y31 has a broad applicationprospect (not published) However two main drawbacks ofEnterocin Y31 with regard to application in foods are asfollows (1) bacteriocins are secreted in very small quan-tities in the production media and (2) the media used togrow the bacteriocin-producing strains are very complex[12] as the LAB are fastidious organisms requiring aminoacids B vitamins and various minerals for their growthThese components are normally provided by sources such assoybean meal yeast extract and meat extract All of thesesources contain proteins and peptides as sources of aminoacids which are often very closely related to the bacteriocinproduced Therefore purification of bacteriocin from sucha complex medium requires a series of steps At each stepthere is some loss and sometimes after the final purificationthe antimicrobial activity may be completely lost Complexmedia do not allow the examination of all individual mediumfactors [13 14] affecting bacteriocin production

Ricciardi reported a modified chemically defined med-ium to promote the growth of Lactobacillus casei and Lacto-bacillus plantarum groups [15] In the present study weimproved the chemically defined medium to improve theyield of Enterocin Y31 produced by E faecium Y31 Thereare four objectives of this study (1) to develop a newand improved production method for Enterocin Y31 (pro-duced by E faecium Y31) (2) to determine the macro- andmicronutrients necessary for cultivating E faecium Y31 andimproving Enterocin Y31 production (3) to develop a noveland simple separation and purificationmethod for EnterocinY31 (avoiding a series of chromatography steps and the lossof Enterocin Y31 activity) and (4) to compare Enterocin Y31production in a defined medium with that in a complexmediumThis is feasible using a completely defined mediumand a minimal medium for bacteriocin production can thusbe established

2 Materials and Methods

21 Strains and Growth Conditions The bacteriocin-pro-ducer strain E faecium Y31 isolated from Chinese traditionalfermented foods (fermented vegetable juice from Lanzhou)was previously found to produce class IIa bacteriocin [10]which wasmaintained as stock cultures inMRSmediumwith18 glycerol at minus80∘C

Escherichia coli ATCC 25922 was selected as a sensitivestrain for antimicrobial activity assays because the bacte-riocin produced by E faecium Y31 has the highest activityagainst E coli ATCC 25922 in gram-negative bacteria

22 Medium The growth of E faecium Y31 and productionof Enterocin Y31 in a defined medium in a fermenter werecompared with those in MRS (reference medium) used forthe optimisation of the growth of E faecium Y31 and theproduction of Enterocin Y31 This medium CDM consistedof 44 components described by Khan et al [12] (listed inTable 1) All chemicals used for the preparation of the definedmedium were of analytical grade and obtained from either

Sigma-Aldrich (St Louis MO USA) or BDH ChemicalsLtd (Poole UK) For all the experiments aqueous stocksolutions of the individual components were prepared inthe appropriate concentrations and sterilized by autoclav-ing with the exception of the heat-sensitive componentsThe heat-sensitive amino acids (asparagine glutamine andtryptophan) all of the B vitamins and FeSO

4were filter-

sterilized (pore size 022120583m membrane Millipore CorpBillerica MA USA) All the stock solutions were then storedat 4∘C except FeSO

4which was freshly prepared before each

experiment because it is prone to oxidation during storage Inaddition to the defined medium MRS medium was used asa reference for comparison with the defined medium beforeeach experiment

23 Determination of the Antimicrobial Activity of EnterocinY31 The antimicrobial activity of bacteriocin was monitoredusing the agar well diffusion assay (AWDA) as describedpreviously [16] with some modifications E faecium Y31 wascultured for two or three generations and then the cell-free supernatants (CFSs) of E faecium Y31 were preparedby centrifuging for 30min at 10000timesg Aliquots (80 120583L) ofthe cell-free supernatants (CFSs) of E faecium Y31 wereadded to the wells (6mm diameter) on double-layer agarplates previously inoculated with 02mL overnight cultureof the indicator strain E coli ATCC 25922 Plates were keptstatic at room temperature for 3 h to allow diffusion of theCFSs evenly in the agar and then the plates were incubatedfor 24 h at 37∘C The bacteriocin titre was determined byeliminating the effect of the organic acid eliminating theeffect of H

2O2 and protease verificationThe diameter of the

zone of inhibition (not including the wells) was measuredusing a Vernier caliper An arbitrary unit (AUmL) wasdefined as the reciprocal of the highest dilution that producedan inhibition zone Specific activity was expressed as that unitper milligram of protein

24 Protein Concentration Determination Protein concen-tration was determined by the BCA (bicinchoninic acid)microassay method (Pierce Rockford IL USA) [17]

25 Monitoring of the Growth of E faecium Y31 The ODvalue of the fermentation liquid of E faecium Y31 wasmonitored with UV spectrophotometry at 600 nm each hourSterile culture medium was used as blanks to subtract thebackground value Samples having an OD600 nm value ofmore than 07 were diluted with the sterile culture mediumand the corrected OD value was obtained by multiplying thedilution factor ODmax (600 nm) represents the maximumOD value of the growth of E faecium Y31 ODmax (600 nm)was calculated before any centrifugation

26 Determination of the Relative Growth Rate The relativegrowth rate was calculated according to Monod [18] Thefollowing equation was used to calculate the growth rate

120583 = [(lnOD2minus lnOD

1) divide (1199052minus 1199051)] divide 120583CDM (1)

where 120583 is the relative growth rate (hminus1) ln is the symbol fornatural logarithm and OD

1and OD

2are the corrected OD

Journal of Food Quality 3

Table 1 Composition of CDM and SDMmedium

Constituent ContentCDM SDM

Amino acids (g Lminus1)L-Asparagine 100 100L-Aspartic acid 100 mdashL-Glutamic acid 100 100L -Glutamine 100 mdashL-Cys 100 100L-Alanine 100 mdashL-Arginine 100 100Glycine 100 100L-Histidine 100 100L-Isoleucine 100 100L-Leucine 100 100L-Lysine 100 100L-Methionine 100 100L-Phenylalanine 100 100L-Proline 100 mdashL-Serine 100 100L-Threonine 100 100L-Tryptophan 100 100L-Tyrosine 100 mdashL-Valine 100 mdash

Nucleic acid bases (g Lminus1)AdemomeSO

4002 002

Guanine 002 mdashInosine 002 mdashXanthine 002 mdashUracil 002 002Thymine 002 mdashOrotic acid 002 mdash

B vitamins (mgsdotLminus1)Biotin 2000 2000Para-aminobenzoic acid 1000 mdashNicotinic acid 200 200Ca-pantothenic acid 2000 2000Riboflavin 200 200Folic acid 200 200Cyanocobalamin 200 mdashThiamine 1000 mdashPyridoxal 2000 mdash

Minerals (gsdotLminus1)Manganese sulfate 005 005Magnesium sulfate 01 010Ferrous sulfate7H

2O 002 mdash

CaCl2

mdash mdashSodium citrate 500 500Potassium dihydrogen phosphate 200 200Dipotassium hydrogen phosphate 700 700

Table 1 Continued

Constituent ContentCDM SDM

Carbon source (gsdotLminus1)Glucose 1500 1500

Others (gsdotLminus1)Tween 80 100 100Glycerol mdash mdashNaCl mdash 500

27 Effects of NaCl CaCl2 and Glycerol on the Growth of Efaecium Y31 and Enterocin Y31 Production To determine theeffects of these components 5 gL 10 gL 15 gL and 20 gLNaCl 10 gL CaCl

2 and 50 gL glycerol were individually

added to 1000mLCDM andCDMmediumwith no addtionswas used as a control wherein the inoculum size was 2fermentation temperature was 37∘C and inoculum time was24 h The culturing liquid was then centrifuged for 20minat 10000timesg and then the CFSs were used to determineEnterocin Y31 activity and ODmax (24 h)

28 Effects of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth ofE faecium Y31 and Enterocin Y31 Production According tothe Leave One Out (LOO) technique each amino acid Bvitamin mineral and nucleic acid base was sequentially andindividually omitted from 1000mLCDMmedium andCDMwithout additions was used as a control The inoculum sizewas 2 fermentation temperature was 37∘C and inoculationtime was 24 h The culture liquid was then centrifugedfor 20min at 10000timesg and then the CFSs were used todetermine Enterocin Y31 activity and ODmax (24 h)

The following terms were used to describe the rela-tionship between each medium component and growth asdetermined by the single omission technique A constituentwas considered essential if its omission resulted in less thanhalf the maximum strain growth rate and production ofbacteriocin of the positive control stimulatory when itsabsence resulted in the fact that the growth rate and thebacteriocin production was between 50 and 80 of thatobserved in complete CDM and nonessential if the growthrate and Enterocin Y31 production was 80 (or more) of thatobtained in the complete CDM

29 Purification of Enterocin Y31 E faecium Y31 was allowedto grow in the SDM (Table 1) for 24 h The cells were thenremoved by centrifugation (11800timesg 25min) The CFSswere then filtered through a 022 120583m filter (low-protein-binding HVLP filter Millipore Corp) to remove any remain-ing cells These filtered CFSs were referred to as crude bacte-riocin The crude bacteriocin was subjected to ultrafiltrationof 1 kDa and 30 kDa The retentate from the 1 kDa step wasthen subjected to Tricine-SDS-PAGE

210 Statistical Analyses All experiments were preformedseparately three times and mean plusmn standard deviation (SD)values were calculated from triplicate determinations All

4 Journal of Food Quality

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 320002

0604

081012141618202224

ODpHInhibition zone diameter (mm)

Time (h)

OD

35404550556065707580

pH

0

2

4

6

8

10

12

14

Inhi

bitio

n zo

ne (

mm

)

Figure 1 Relationship between the growth of the bacteriocinogenicstrain and Enterocin Y31 production

data were subjected to one-way analysis of variance (one-way ANOVA) Comparison of means was performed withDuncanrsquos multiple range tests Statistical significance was setat 119875 lt 005

3 Results and Discussion

31 Relationship between the Growth of the Strain andEnterocin Y31 Activity The growth of E faecium Y31 wasunrelated to EnterocinY31 activity inMRSmedium as shownin Figure 1 The result was consistent with the result ofBacterocin J23 produced by Lactobacillus paracasei J23 asdescribed by Huaxi Yi in our research group (not published)whichwas inconsistentwith the result of Salivaricin producedby L salivarius CRL 1328 [19] thus the growth rate of EfaeciumY31 and Enterocin Y31 activity were used as detectionindexes for developing a novel chemical defined mediumEnterocin Y31 activity could be detected at the exponentialphase of the producing strain (9 h) and reached its highestvalue of 1126 plusmn 036mm at stationary phase of producingstrain (24 h) ODmax remained stable at 16 h of fermentationof strain Y31 thus ODmax (16 h) was used as an index of thestrain growth status

32 Effect of NaCl Concentration on the Growth of E faeciumY31 and Enterocin Y31 Production Theeffect of NaCl at 5 gL10 gL 15 gL and 20 gL was determined in CDMwith CDMwith no additives as the control The results indicated thatthe growth of E faecium Y31 and production of EnterocinY31 were not significant difference when adding 5 gL or10 gL NaCl and 0 gL and 15 gL NaCl had no effect onthe growth of strain Y31 and production of Enterocin Y31When the concentration of NaCl was 20 the growth of Efaecium Y31 and production of Enterocin Y31 reduced whichshowed the significant difference when compared to 0 gLand 15 gL NaCl We can conclude that 20 gL NaCl have anegative effect on the growth of strain Y31 and the productionof Enterocin Y31 When the adding concentration of NaClwas 5 gL the ODmax (16 h) of E faecium Y31 was highest

150

155

160

165

170

175

180

Enterocin Y31 production (AUmg protein)

CDM

(con

trol)

bc c

bc

ab

a

b b bab

a

GR

(16B

)

ODmax (16 B)

10A

L N

aCl

15A

L N

aCl

20A

L N

aCl

5A

L N

aCl 0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 2 Effect of NaCl concentration on the growth of Enterococ-cus faecium Y31 and Enterocin Y31 production Means not sharing acommon superscript letter are significantly different fromeach other(119875 lt 005)

172 plusmn 001 and the antibacterial activity also reached themaximum value 128364 plusmn 4140AUmg protein Based thesignificant difference analysis we could conclude that 5 gLNaCl stimulated the growth of strain Y31 (119875 lt 005) andhad no effect on the production of Enterocin Y31 (Figure 2)Similar results have been reported in a study of nutritionalrequirements of L salivarius CRL 1328 producing Salivaricin[19] Considering that the condition for the growth of Efaecium Y31 was crucial 5 gL NaCl was added to the novelchemically defined medium SDM (the medium ingredientsof SDM were listed in Table 1)

33 Effect of CaCl2 and Glycerol on the Growth of E faeciumY31 and Enterocin Y31 Production The results shown inTable 2 indicated that adding 10 gL CaCl

2to CDM had no

effect on the growth of E faecium Y31 but had a negativeeffect on the production of Enterocin Y31 (119875 lt 005) whereasadding 50 gL glycerol had a slight negative effect on thegrowth of E faecium Y31 (119875 lt 005) and a negative influenceon Enterocin Y31 production (119875 lt 005)

34 Effect of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth of Efaecium Y31 and Enterocin Y31 Production According to theLeaveOneOut (LOO) technique each amino acid B vitaminmineral and nucleic acid base was sequentially omitted ina series of prepared formulations along with CDM as acontrol The results shown in Table 3 indicated that L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser and L-Cys areessential amino acids which had an effect on the growth ofE faecium Y31 and Enterocin Y31 production and the stim-ulatory amino acids mainly included L-Asn L-Glu L-Iso L-Lys and L-Try Omitting the stimulatory amino acids resultedin the slow growth of E faecium Y31 and low production

Journal of Food Quality 5

Table 2 Effects of CaCl2and glycerol on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Added components ODmax (600 nm) after 16 h Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003b 124224 plusmn 4141c

10 gL CaCl2

170 plusmn 002b 28986 plusmn 4141a

50 gL glycerol 153 plusmn 003a 56591 plusmn 4181b

Note CDM is explained in Table 1 and means in the same row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

Table 3 Effect of omitting a single amino acid on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Omitted amino acid ODmax (16 h) Relative growth rate Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003h 100 124224 plusmn 4141cd

L-Ala 150 plusmn 005g 90 122843 plusmn 6325cd

L-Arg 076 plusmn 002c ng mdasha

L-Asp 143 plusmn 004g 93 117322 plusmn 6325cd

L-Asn 091 plusmn 003d 60 122843 plusmn 8225cd

L-Cys 100 plusmn 004de 44 mdasha

L-Glu 152 plusmn 004g 72 110420 plusmn 2391c

L-Gln 171 plusmn 004h 84 124224 plusmn 5686d

L-Gly 061 plusmn 003ab ng mdasha

L-His 066 plusmn 003bc ng mdasha

L-Iso 106 plusmn 004ef 79 66252 plusmn 8251b

L-Leu 071 plusmn 003bc ng mdasha

L-Lys 116 plusmn 004f 80 62111 plusmn 4140b

L-Met 053 plusmn 002a ng mdasha

L-Phe 077 plusmn 002c ng mdasha

L-Pro 181 plusmn 003h 71 110420 plusmn 6545cd

L-Ser 049 plusmn 003a ng mdasha

L-Thr 068 plusmn 002bc ng mdasha

L-Try 112 plusmn 003ef 80 57322 plusmn 2391b

L-Tyr 170 plusmn 007h 100 120082 plusmn 3487cd

L-Val 196 plusmn 008i 98 122843 plusmn 6582cd

Note ldquongrdquo represents that the strain did not grow and ldquomdashrdquo represents that there was no inhibition activity CDM is explained in Table 1 and means in thesame row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

of Enterocin Y31 Therefore the essential amino acids andstimulatory amino acids were included in the SDM (listedin Table 1) A previous study reported the similar results asZhang et al found that six amino acids (arginine histidineisoleucine leucine methionine and valine) were necessaryfor the lactococci enterococci and streptococci [20]

Pyridoxal and pantothenic acid are essential B vitaminswhich had an effect on the growth of E faeciumY31 and Ente-rocin Y31 production and the stimulatory B vitamins mainlyincluded niacin and riboflavin Wherein the stimulatory Bvitamins could not result in the growth arrest of E faeciumY31 and the biosynthesis arrest of Enterocin Y31 they couldcause low growth rate and low biosynthesis volume There-fore the essential and stimulatory B vitamins were neededin the SDM Omitting folic acid would cause a reduction of80 in the ODmax (16 h) of E faecium Y31 therefore folicacid is also needed for the growth of E faecium Y31 and theproduction of Enterocin Y31 (Figure 3) It has been reported

that nutritional requirements of L delbrueckii ssp lactis CRL581 growthwere nicotinic acid and pyridoxal and pantothenicacid whereas the growth of L delbrueckii ssp lactis CRL654 requires niacin and pantothenic acid and riboflavinand cyanocobalamin were found to be stimulatory for bothstrains [21] Research results about S thermophilus strains(ST1 ST7 ST8 ST11 ST18 and ST21) indicated that riboflavinwas essential for the growth of all strains whereas Ca-pantothenic acid and nicotinic acid were also required [22]

In the present study MgSO4sdot7H2O was an essential min-

eral andMnSO4sdot4H2OKH

2PO4 K

2HPO4 andCH

3COONa

were stimulatory minerals which had an effect on the growthof E faecium Y31 and Enterocin Y31 production (Figure 4)The necessity of magnesium and phosphate has previouslybeen reported by other researchers for various LAB species[20 23 24]

Adenine and uracil are stimulatory nucleic acids whichhad an effect on the growth of E faecium Y31 and Enterocin

6 Journal of Food Quality

Non

e (CD

M)

Pyrid

oxal

Thia

min

e

Nia

cin

D-B

iotin

Ribo

flavi

n

Cyan

ocob

alam

in

Folic

acid

p-A

min

oben

zoic

acid

Pant

othe

nic a

cid

02040608101214161820

Omitted vitamins

f

b

f

c

f

d

e ef

a

d

b

d

b

ccd

cdcd

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 3 Effect of individually omitting each B vitamin on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Y31 production (Figure 5) No nucleic acid was essential forthe growth of E faecium Y31 and Enterocin Y31 production

35 Comparison of Enterocin Y31 Production onMRSMediumand SDM A novel chemical defined medium (SDM) wasdeveloped (Table 1 and Figures 3 4 and 5) and SDMcontainedNaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

and uracil Strain Y31 grew better on SDM than on MRSmedium (Figure 6) As shown in Figure 7 Enterocin Y31production on SDM was 16 times than that on MRS

36 Purification and Characterization of Enterocin Y31 Afterthe removal of cells from the defined medium the cell-free supernatant was subjected to ultrafiltration through a30 kDa ultrafiltration membrane The active permeate liquorwas then subjected to a second ultrafiltration step using a1 kDa NMWL The antimicrobial activity was again foundin the retentate (10240AUL) Enterocin Y31 was purified byTricine-SDS-PAGE and its molecular weight was 674 kDa(showed in Figure 8)

4 Conclusion

When culturing E faecium Y31 using novel chemical definedmedium (SDM) Enterocin Y31 production increased 16times than that on MRS The ingredients were composedof NaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-ThrL-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

Non

e (CD

M)

Am

mon

ium

citr

ate d

ibas

ic

MnS

O4 middot 4

H2O

MgS

O4 middot 7

H2O

KH2P

O4

K2H

PO4

Sodi

um ac

etat

e

0204060810121416182022

Omitted minerals

d d

b

a

b

c ce e

b

a

c

d d

Enterocin Y31 production (AUmg protein)$

GR

(16B

)$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

Figure 4 Effect of individually omitting each a mineral on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Non

e (CD

M)

Aden

ine

Gua

nine

Inos

ine

Xant

hine

Oro

tic ac

id

Ura

cil

Thym

ine

14

15

16

17

18

19

20

Omitted nucleic acid bases

d

a

c

d d d

b

d

d

abbc

d d d

a

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

Figure 5 Effect of individually omitting each a nucleic acid baseon the growth of Enterococcus faecium Y31 and Enterocin Y31production Means not sharing a common superscript letter aresignificantly different from each other (119875 lt 005)

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

uracil and glucose which were the macro- and micronu-trients needed by biosynthesis of Enterocin Y31 SDM washelpful to the growth of E faecium Y31 and EnterocinY31 production improvement In addition SDM avoided aseries of chromatography steps and the loss of Enterocin Y31

Journal of Food Quality 7

0 5 10 15 20 25 30 3500020406081012141618202224

Time (h)

SDMMRS

GR

(16B

)

Figure 6 Growth of Enterococcus faecium Y31 on MRS and SDM

0 5 10 15 20 25 30 3502468

10121416182022

Time (h)

Inhi

bitio

n zo

ne d

iam

eter

(mm

)

SDMMRS

Figure 7 Enterocin Y31 productions on MRS and SDM

Enterocin Y31

M 140 +$

30+$

20 +$

10 +$

46 +$

17 +$

Figure 8 Tricine-SDS-PAGE of Enterocin Y31 M protein marker1 Enterocin Y31

activity only two steps of ultrafiltration and Tricine-SDS-PAGE were needed to separate and purify Enterocin Y31Therefore chemically defined medium has better potentialfor improving the bacteriocin production and reducing thesteps of separation and purification Chemically definedmedia is useful for purification of not only large bacteriocinssuch as Enterocin Y31 but also small peptide bacteriocinsThe alternative use of a chemically defined medium meetsthe nutritional requirements of strains producing bacteri-ocins and therefore is an excellent alternative to reduce theload of contaminating peptides from the medium therebydecreasing the purification steps To our knowledge no suchstudies have been conducted to improve class IIa bacteriocinEnterocin Y31 production and purify Enterocin Y31

Ethical Approval

This study complies with the research ethics guidelines and itdoes not contain any studies with human or animal subjects

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article

Acknowledgments

This work was financially supported by the 60th Finan-cial Grant from China Postdoctoral Science Foundation(Grant no 2016M602534) the Youth Innovation TalentsProject of General Higher School in Guangdong Province(2016KQNCX144) and theNationalNatural Science Founda-tion of China (Grants nos 31571850 31771988 and 31701621)

References

[1] R C R Martinez M Wachsman N I Torres J G LeBlancS D Todorov and B D G D M Franco ldquoBiochemical anti-microbial and molecular characterization of a noncytotoxicbacteriocin produced by Lactobacillus plantarum ST71KSrdquo FoodMicrobiology vol 34 no 2 pp 376ndash381 2013

[2] I M Aasen T Moslashretroslash T Katla L Axelsson and I StorroslashldquoInfluence of complex nutrients temperature and pH on bacte-riocin production by Lactobacillus sakei CCUG 42687rdquo AppliedMicrobiology andBiotechnology vol 53 no 2 pp 159ndash166 2000

[3] P Alvarez-Sieiro M Montalban-Lopez D Mu and O PKuipers ldquoBacteriocins of lactic acid bacteria extending thefamilyrdquo Applied microbiology and biotechnology vol 100 no 7pp 2939ndash2951 2016

[4] F A C Martinez E M Balciunas A Converti P D Cotterand R P De Souza Oliveira ldquoBacteriocin production by Bifido-bacterium spp A reviewrdquo Biotechnology Advances vol 31 no 4pp 482ndash488 2013

[5] E F OrsquoShea P D Cotter R P Ross and C Hill ldquoStrategiesto improve the bacteriocin protection provided by lactic acidbacteriardquo Current Opinion in Biotechnology vol 24 no 2 pp130ndash134 2013

[6] A-M Zouhir E Kheadr I Tahiri J Ben Hamida and IFliss ldquoCombination with plant extracts improves the inhibitoryaction of divergicin m35 against Listeria monocytogenesrdquo Jour-nal of Food Quality vol 31 no 1 pp 13ndash33 2008

8 Journal of Food Quality

[7] J Pei Y Yuan and T Yue ldquoPrimary characterization of bacteri-ocin paracin C - A novel bacteriocin produced by Lactobacillusparacaseirdquo Food Control vol 34 no 1 pp 168ndash176 2013

[8] D Drider and S Rebuffat ldquoClassification of Bacteriocins fromGram-Positive Bacteriardquo in Prokaryotic Antimicrobial Peptidespp 29ndash53 Springer New York NY USA 2011

[9] T Aymerich H Holo L S Havarstein M Hugas M Garrigaand I F Nes ldquoBiochemical and genetic characterization of ente-rocin A from Enterococcus faecium a new antilisterial bac-teriocin in the pediocin family of bacteriocinsrdquo Applied andEnvironmental Microbiology vol 62 no 5 pp 1676ndash1682 1996

[10] W Liu L Zhang H Yi et al ldquoQualitative detection of class IIabacteriocinogenic lactic acid bacteria from traditional Chinesefermented food using a YGNGV-motif-based assayrdquo Journal ofMicrobiological Methods vol 100 no 1 pp 121ndash127 2014

[11] W Liu L Zhang J Shi et al ldquoAssessment of the safety and appli-cations of bacteriocinogenic Enterococcus faecium Y31 as anadjunct culture in North-eastern Chinese traditional fermen-tation paocairdquo Food Control vol 50 pp 637ndash644 2015

[12] H Khan S H Flint and P-L Yu ldquoDevelopment of a chemicallydefined medium for the production of enterolysin A fromEnterococcus faecalis B9510rdquo Journal of Applied Microbiologyvol 114 no 4 pp 1092ndash1102 2013

[13] M Silva d M Andrade d S A Bauermeister et al ldquoA SimpleDefined Medium for the Production of True Diketopiperazinesin Xylella Fastidiosa and Their Identification by Ultra-FastLiquidChromatography-Electrospray Ionization IonTrapMassSpectrometryrdquoMolecules vol 22 no 6 p 985 2017

[14] E Texeira J Checa A Rıal et al ldquoA New Chemically DefinedMedium for Cultivation of Streptococcus Pneumoniae SerotyperdquoJournal of Biotech Research vol 6 p 54 2015

[15] A Ricciardi R G Ianniello E Parente and T Zotta ldquoModifiedchemically definedmedium for enhanced respiratory growth ofLactobacillus casei and Lactobacillus plantarum groupsrdquo Journalof Applied Microbiology vol 119 no 3 pp 776ndash785 2015

[16] U Schillinger and K Lucke F ldquoAntibacterial activity of Lacto-bacillus sake isolated from meatrdquo Applied and EnvironmentalMicrobiology vol 55 no 8 pp 1901ndash1906 1989

[17] P K Smith R I Krohn G Hermanson et al ldquoMeasurement ofprotein using bicinchoninic acidrdquo Analytical biochemistry vol150 no 1 pp 76ndash85 1985

[18] J Monod ldquoThe Growth of Bacterial Culturesrdquo Annual Reviewsin Microbiology vol 3 no 1 pp 371ndash394 1949

[19] E V Pingitore EMHebert F Sesma andM E Nader-MacıasldquoInfluence of vitamins and osmolites on growth and bacteriocinproduction by Lactobacillus salivarius CRL 1328 in a chemicallydefinedmediumrdquoCanadian Journal of Microbiology vol 55 no3 pp 304ndash310 2009

[20] G Zhang D AMills and D E Block ldquoDevelopment of chemi-cally defined media supporting high-cell-density growth ofLactococci Enterococci and Streptococcirdquo Applied and Environ-mental Microbiology vol 75 no 4 pp 1080ndash1087 2009

[21] E M Hebert R R Raya and G S De Giori ldquoNutritionalrequirements of Lactobacillus delbrueckii subsp lactis in achemically defined mediumrdquo Current Microbiology vol 49 no5 pp 341ndash345 2004

[22] C Letort and V Juillard ldquoDevelopment of a minimal chemi-cally-defined medium for the exponential growth of Streptococ-cus thermophilusrdquo Journal of AppliedMicrobiology vol 91 no 6pp 1023ndash1029 2001

[23] N Terrade and R Mira de Orduna ldquoDetermination of theessential nutrient requirements of wine-related bacteria fromthe genera Oenococcus and Lactobacillusrdquo International Journalof Food Microbiology vol 133 no 1-2 pp 8ndash13 2009

[24] F M Saguir and M C M De Nadra ldquoImprovement of a chem-ically definedmedium for the sustained growth of Lactobacillusplantarum nutritional requirementsrdquo Current Microbiologyvol 54 no 6 pp 414ndash418 2007

Research ArticleLipid Oxidation Color Changes and MicrobiologicalQuality of Frozen Beef Burgers Incorporated with ShiraziThyme Cinnamon and Rosemary Extracts

Hadi Hashemi Gahruie Seyed Mohammad HashemHosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan Shad

Department of Food Science and Technology School of Agriculture Shiraz University Shiraz Iran

Correspondence should be addressed to Mohammad Hadi Eskandari eskandarshirazuacir

Received 3 January 2017 Revised 17 March 2017 Accepted 11 April 2017 Published 21 May 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Hadi Hashemi Gahruie et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In this study the oxidative stability of beef burgers incorporated with Shirazi thyme cinnamon and rosemary extracts wascompared with that of BHT-incorporated and antioxidant-free samples The chemical composition TBARS metmyoglobin pHcolor and microbial and sensory characteristics were evaluated during storage at minus18∘C for 2 months The results indicated thatShirazi thyme and cinnamon extracts did not change the colorimetric properties significantly (119875 lt 005) Incorporating naturalantioxidants led to a significant (119875 lt 005) reduction in TBARS (3658ndash4634) and metmyoglobin (1625ndash1847) as compared tocontrol Except for the control sample total microbial counts of burgers were lower than the maximum allowed limit Burgersformulated with Shirazi thyme revealed the lowest amount of total count Regarding the sensory characteristics the overallacceptability of different samples decreased in the order of cinnamon gt BHT gt Shirazi thyme gt rosemary gt control Finally theresults showed that these plant extracts can be utilized as an alternative to synthetic antioxidants in formulation of burgers

1 Introduction

Meat and meat products are among the most importantprotein sources in the daily diet of people living in developedcountries Beef burger is almost the most popular meatproduct consumed by millions of people from all over theworld The common processes (such as mincing cookingand salt addition) applied in the production of burgersenhance the formation of reactive oxygen species thereforethe resultant product is highly vulnerable to oxidation [1]Lipid and protein oxidations have been reported as theprincipal reason for the decreased quality of burgers duringstorage resulting in decreasing the shelf life [2ndash4]

Application of antioxidants is the best strategy to pre-vent oxidation reactions [5] Synthetic antioxidants such asBHT TBHQ and BHA have various adverse human healtheffects including allergy headache asthma and dermatitis

Therefore the application of natural antioxidants (such asherbal essential oils and extracts) is of interest and canbe observed in a growing number of research works [6ndash8](Aliakbarlu et al 2016)Moreover consumers are increasinglydemanding for green-labeled food products such as thosecontaining natural antioxidant Natural compounds can beobtained from natural sources such as plants fruits vegeta-bles oil seeds spices team honey bee pollen and cereals[9] A lot of extracts have been approved as GRAS (GenerallyRecognized as Safe) that is the addition of these chemicals orsubstances into food is considered safe by experts and theirapplication is exempted from the usual Federal Food Drugand Cosmetic Act (FFDCA) [10]

The potential of natural antioxidants in preventing thelipid oxidation in different food products has been evaluatedby many researchers around the world [11] It has beenreported that the extracts of kinnow rind pomegranate rind

HindawiJournal of Food QualityVolume 2017 Article ID 6350156 9 pageshttpsdoiorg10115520176350156

2 Journal of Food Quality

Hamburger ingredients Extracts (20 g herb + 500 ml water)

Preparation of base batter

Formula 1without additives

(control)

Formula 2with BHT(100 ppm)

Formula 3with Shirazi thyme

(22 mlkg)

Formula 4with rosemary

(28 mlkg)

Formula 5with cinnamon

(73 mlkg)

Analysis (0 15 30 45 and 60 days)

Chemical analysis

Chemical compotation(i) Moisture

(ii) Protein(iii) Fat(iv) Carbohydrate(v) Ash

Deterioration criteria(i) TBARS

(ii) pH(iii) Metmyoglobin

Microbiological analysis(i) Total aerobic bacterial count

Sensory analysis(i) Appearance

(ii) Texture(iii) Taste(iv) Odor(v) Overall acceptance

Color analysis(i) Llowast

(ii) alowast

(iii) blowast

(iv) ΔE

Production and storage at minus18∘C

Figure 1 Schematic diagram of experimental design

and seed powders were significantly able to decrease the lipidoxidation in goat meat patties [12] The effects of natural(sage and rosemary) and synthetic (BHT) antioxidants onprotein oxidation discoloration and texture of refrigeratedpatties produced from pig liver have been studied by Estevezet al [13] Authors reported that the antioxidant propertiesof natural and synthetic antioxidants were similar In treatedsamples the increase in the carbonyl content as a result ofoxidation was significantly (P lt 005) lower than controlsamples Moreover antioxidants could successfully protectheme molecules from degradation Among different naturalantioxidants it has been reported that the extracts of Shirazithyme cinnamon and rosemary reveal substantial antioxi-dant capacity [14]

The main objective of the current study was to comparethe effects of Shirazi thyme cinnamon and rosemary extracts(denoted as natural antioxidants) with those of BHT on pro-tein and lipid oxidations and physicochemicalmicrobial andsensory characteristics of frozen beef burgers during storageThe results of this study may have potential implications

in substituting the synthetic antioxidants with nature-madeones

2 Materials and Methods

A schematic representation of beef burger production isshown in Figure 1

21 Materials Beef flanks (18 fat) from freshly slaughteredanimals (24 hours post slaughter)were purchased froma localmarket (Shiraz Iran) and transported to the laboratory ininsulated polystyrene ice-boxes The meat was ground (MeatGrinder Philips HR2743 AmsterdamNetherlands) througha perforated plate with a hole diameter of 5mm Thiobar-bituric acid (Sigma-Aldrich St Louis MO USA) 1133-tetraethoxypropane (Sigma-Aldrich St Louis MO USA)and diphenyl-2-picrylhydrazyl (DPPH∙) (Sigma-Aldrich StLouisMOUSA) soy protein isolate (SPI 90 protein SonicCo India) onions salt spices and ruskwere also used in thisstudy

Journal of Food Quality 3

22 Plant Extracts Shirazi thyme (Zatariamultiflora) cinna-mon (Cinnamomum zeylanicum) and rosemary (Rosmarinusofficinalis) were purchased from a local grocery The genusand species were certified by experts from the Herbariumof Biology Department (Shiraz University Shiraz Iran)Dried plants were powdered with a mill and then kept inpolyethylene bags at room temperature before extraction

221 Extract Preparation Plant powder (20 g) was thor-oughly mixed with boiling distilled water (500mL) for5min followed by filtration through Whatman grade No 1filter papers and concentration in rotary evaporator (BuchiRotavapor R Switzerland) at 50∘C [15]

222 DPPH Radical Scavenging Activity Antioxidant activ-ity of natural extracts and BHT was calculated using DPPHfree radicalmethod described by Cam et al [16]The amountsof extracts required to replace BHT were calculated basedon the IC50 of BHTThe required amounts of natural extractsshould have equal antioxidant activity to BHT

23 Beef Burger

231 Burger Preparation and Storage The formulation ofbeef burger used in this study was composed of beef (70)onions (134) rusk (4) water (8) SPI (3) salt (1)black (03) and red (02) peppers Ground meat saltwater and minced onion were mixed together After thatSPI was added and then mixed for 15min to obtain ahomogenousmixture Rusk and spices were added in the nextstep Finally natural extracts andor BHT were incorporatedinto the homogenate and thenmixing process was continuedThe concentration of BHT was 100 ppm A burger maker(9 cm internal diameter) was used to shape the mixture intopatties of approximately 90 g and 5mm thickness Burgers(15 patties per treatment) were then packed in light-resistantpolyethylene containers and frozen at minus18∘C Analyses wereperformed during 15-day intervals for two months Beforeanalysis the samples were thawed at +4∘C and then hand-mixed for 30 s

232 Chemical Analysis Moisture protein fat and ashcontents of burgers were determined according to the AOACmethods [17] Carbohydrate content was estimated by sub-tracting the total amounts of moisture protein fat and ashfrom 100

233 pH Measurement Meat sample (10 g) was homog-enized with 50mL deionized water for 1min pH wasmeasured at room temperature using a digital pH meter(Suntex TS-1 Taiwan) equipped with a probe-type combinedelectrode (Ingold) through direct immersion of electrode intothe mixture [17]

234 Instrumental Color Evaluation Color attributes of beefburgers were measured by 119871lowast119886lowast119887lowast method described byYam and Papadakis [18] The values of 119871lowast (brightness) 119886lowast(redness-greenness) and 119887lowast (yellowness-blueness) weremea-sured on the whole outer surfaces of beef burger A wooden

box (50 times 50 times 60 cm3) equipped with a natural daylightsource (6500K) and a digital camera (CanonPowershotA540of six megapixels resolution) in a vertical position and adistance of 25 cm from the samples was used for takingphotos Adobe PhotoshopCS6 was applied to determine theaverage surface color

235 Determination of Lipid Oxidation Lipid oxidationwas monitored by measuring thiobarbituric acid reactivesubstances (TBARS) Meat sample (4 g) was homogenizedwith 20mL trichloroacetic acid solution (20 wv) and thencentrifuged at 3000119892 for 10min The supernatant (2mL) wasmixed with 2mL thiobarbituric acid solution (01 wv indouble distillated water) followed by heating in a water bathat 100∘C for 30min and then cooling to room temperatureTherefore TBARS were extracted in chilled atmosphere Theabsorbance of each extract was measured at 520 nm in aspectrophotometer (spec 1650PC Shimadzu Japan) 1133-tetraethoxypropane was used to develop the standard curvefor TBARS assay TBARS values were reported as mg ofmalonaldehyde per kg of beef burger [7]

236 Metmyoglobin Measurement A modified method ofAn et al [19] was used to measure the metmyoglobincontent in raw beef burgers The sample (4 g) was mixedin a homogenizer with 20mL of phosphate buffer (004MpH 68) and then stored at 1∘C for 1 h The mixture wasthen centrifuged at 3500119892 and 4∘C for 30min Finally thesupernatant was filtered through Whatman grade No 1filter paper The absorbance of the solution was measuredat 525 572 and 700 nm Metmyoglobin () was calculatedaccording to the following equation

Metmyoglobin () = [1395 minus [(119860572 minus 119860700)(119860525 minus 119860700)]]times 100

(1)

Total Aerobic Bacterial Count Total aerobic bacteria werequantified every 15 days using the method described byAliakbarlu et al (2016) Beef burgers (10 g) were asepti-cally transferred into individual stomaching bags containing90mL of sterile saline (09) and homogenized for 2minSerial 10-fold dilutions were prepared in saline and 100 120583Lfrom appropriate dilutions was spread on the surface of platecount agar for total aerobic count (TMC) and then incubatedat 35∘C for 24 h

237 Sensory Evaluation Sensory analyses have been per-formed by 20 trained panelists from the Department of FoodScience and Technology (Shiraz University) Panelists wereboth male and female in the age range of 23ndash28 years oldPanelists were selected based on their previous experiences inconsuming traditional beef burgers Moreover they receivea preparatory session before the sensory test to train themhow to describe all evaluated factors completely Burgers werefried at 150∘C in a forced draft oven to a core temperatureof 72∘C and kept warm in the oven for 3ndash8min until thesensory testing [20] Rectangular pieces of approximately

4 Journal of Food Quality

2 cm were cut from the center of each burger and then servedat room temperature Each panelist randomly evaluated threepieces of all formulations and asked to give a numericalvalue between 1 and 9 for the following attributes taste 1(imperceptible) to 9 (extremely intense) texture attributesand juiciness 1 (extremely dry) to 9 (extremely moist)appearance 1 (extremely soft) to 9 (extremely tough) andodor 1 (imperceptible) to 9 (extremely intense) Tap waterwas provided for panelists to rinse their mouth betweendifferent samples At the end of evaluation each panelist wasasked to give an overall score from 1 (dislike very much) to9 (like very much) for the overall acceptability of differentformulations

24 Statistical Analysis A completely randomized blockdesign with five treatments (including antioxidant-free (con-trol) treatment and those incorporated with BHT cinnamonrosemary and Shirazi thyme extracts) was used in this studyExperiments were performed during a 60-day storage periodat 15-day intervals (0 15 30 45 and 60) Independent blocks(developed from three different batches) were replicatedthree times at each sampling point A two-way analysisof variance (ANOVA) and Duncanrsquos multiple range tests(SAS 80 software SAS Institute Inc Cary NC USA) wereperformed to analyze the effect of treatments storage periodand their interaction on the physicochemical microbial andsensory characteristics of beef burgers at a confidence levelof 005 In the analysis models the treatments storage timesand their interaction were assigned as fixed effects and thereplications as random effects

The given scores of different sensory attributes werecompared between the treatments using general linear model(GLM) Duncanrsquos multiple range tests were used for compar-ison of means at a confidence level of 005 Treatments andassessors were considered as main effects and the replicationsas random effects Data was reported as mean plusmn standarderror (SE)

3 Results and Discussion

31 Antioxidant Activity of Extracts The IC50 values (definedas the concentration of an antioxidant required to reduce theinitial DPPH concentration by 50 using DPPH free radicalmethod described by Cam et al [16]) of natural extracts(including Shirazi thyme cinnamon and rosemary) andsynthetic BHT were 0022 0373 0062 and 0107mgmLrespectively Therefore the amounts of Shirazi thyme cinna-mon and rosemary concentrated extracts required to replace100 ppm BHT in formulation were 22 73 and 28mL per kgof beef burger respectively Cinnamon is a source of bioactivecompounds such as cinnamaldehyde eugenol and coumarin[21] The effect of cinnamon extract as direct scavengersof free radicals has been studied by Roussel et al [22]Carnosic acid and carnosol are the main bioactive com-pounds present in the rosemary extract [23] According toSharififar et al [24] the major chemical compounds presentin Shirazi thyme were carvacrol (3365) thymol (3759) p-cymene (772) 120574-terpinene (388) and 120573-caryophyllene(206)

40

45

50

55

60

65

70

75

80

Met

myo

glob

in (

)

15 30 45 600Storage period (days)

ControlBHTCinnamon extract

Rosemary extractShirazi thyme extract

Figure 2 Effect of incorporating Shirazi thyme cinnamon androsemary extracts on the metmyoglobin () developed in raw beefburgers during frozen storage at minus18∘C

32 Physicochemical Properties of Beef Burger The resultsindicated that the samples contained 5913 moisture 19protein 12 fat 772 carbohydrate and 2 ash

33 Color Stability When assessing meat a consumer paysa great attention to its color which as a visual impressionis induced mainly by the presence of pigments but it alsodepends on tissue composition and meat structure Hencethe color of fresh meat is an important quality parameterthat determines a consumerrsquos response and decision to buyor not to buy that product at retail Changes in 119871lowast 119886lowast and119887lowast values of beef burgers during frozen storage are shown inTable 1 No significant difference (119875 gt 005) was observedbetween the samples incorporated with natural antioxidantsand those incorporated with BHT at production time (day 0)resulting in low Δ119864 values at early stages of storage All of theformulations showed significant decrease in 119886lowast during frozenstorage Formulation incorporated with rosemary extractshowed lower amounts of 119886lowast at the end of storage timeThe significant decrease in 119886lowast values indicated the red colorreduction of products during storage this is despite the factthat BHT- and extract-incorporated treatment significantlyreduced the Met-mb development ratio in comparison tocontrol one (Figure 2) During the first 30 days of storage119871lowast values increased significantly (119875 lt 005) then remainedconstant During frozen storage changes in the amountsof 119871lowast in cinnamon- (642) or Shirazi thyme-incorporatedsamples (597) were less than those in other formulationsSamples incorporated with rosemary extract showed the leastredness (433)

A significant decrease in 119886lowast values of raw pork pat-ties containing grape seed extract and bearberry has beenreported over a 12-day storage by Carpenter et al [25]however 119887lowast values (particularly of control samples) increasedsignificantly (119875 lt 005) Similarly Nunez de Gonzalez et al[26] reported that 119886lowast value of beefs stored under refrigeration

Journal of Food Quality 5

Table 1 Effect of addition of Shirazi thyme cinnamon and rosemary extracts and BHT on 119871lowast 119886lowast 119887lowastand Δ119864 values of raw beef burgersduring frozen storage at minus18∘CParameter Sample Storage period (days)

0 15 30 45 60

119871lowastControl 6033 plusmn 088 glowastlowast 5800 plusmn 058 hi 7133 plusmn 034 abc 7167 plusmn 034 ab 7267 plusmn 067 aBHT 5867 plusmn 088 ghi 5733 plusmn 034 i 6833 plusmn 034 de 6933 plusmn 034 cd 7067 plusmn 067 abc

Cinnamon extract 6033 plusmn 067 g 5433 plusmn 034 j 5967 plusmn 067 gh 6533 plusmn 067 f 6800 plusmn 058 deRosemary extract 5733 plusmn 034 i 5433 plusmn 082 i 6967 plusmn 088 bcd 7133 plusmn 088 abc 7167 plusmn 034 ab

Shirazi thyme extract 5733 plusmn 146 i 5667 plusmn 067 i 5700 plusmn 058 i 6700 plusmn 058 ef 6833 plusmn 067 de

119886lowastControl 1133 plusmn 034 a 833 plusmn 034 de 833 plusmn 034 de 767 plusmn 034 ef 667 plusmn 034 fghBHT 1100 plusmn 058 ab 667 plusmn 034 fgh 767 plusmn 067 ef 700 plusmn 058 fg 667 plusmn 034 fgh

Cinnamon extract 933 plusmn 034 cd 733 plusmn 034 efg 667 plusmn 034 fgh 567 plusmn 034 hij 533 plusmn 034 ijkRosemary extract 1167 plusmn 034 a 533 plusmn 034 ijk 533 plusmn 034 ijk 467 plusmn 034 jk 433 plusmn 034 k

Shirazi thyme extract 1000 plusmn 058 667 plusmn 034 fgh 633 plusmn 034 ghi 567 plusmn 034 hij 533 plusmn 034 ijk

119887lowastControl 2333 plusmn 034 kl 2500 plusmn 058 ij 3233 plusmn 034 bc 3267 plusmn 067 b 3400 plusmn 058 aBHT 2233 plusmn 034 lmn 2333 plusmn 034 kl 3100 plusmn 058 cd 3133 plusmn 067 bcd 3167 plusmn 067 bcd

Cinnamon extract 2167 plusmn 034 mno 2267 plusmn 034 lm 2533 plusmn 034 ij 2600 plusmn 058 i 2767 plusmn 034 hRosemary extract 2033 plusmn 0340 2100 plusmn 058 no 2900 plusmn 058 fgh 3067 plusmn 034 de 3133 plusmn 067 bcd

Shirazi thyme extract 2300 plusmn 000 klm 2433 plusmn 034 jk 2833 plusmn 034 gh 2933 plusmn 034 efg 3033 plusmn 034 def

Δ119864lowastlowastlowastControl 000 plusmn 000 f 1700 plusmn 025 aBHT 272 plusmn 069 e 1409 plusmn 018 bc

Cinnamon extract 282 plusmn 072 e 1078 plusmn 095 dRosemary extract 442 plusmn 104 e 1559 plusmn 102 ab

Shirazi thyme extract 354 plusmn 030 e 1229 plusmn 080 cdlowastlowastData represent averages of three independent repeats plusmn standard errorslowastlowastMeans with different letters are significantly different (119875 le 005)lowastlowastlowastFor each storage time the color difference (Δ119864) was calculated by comparing the color attributes of different formulations with those of control sample

for 10 weeks decreased significantly (119875 lt 005) The resultsof the current study showed that high antioxidant activity ofnatural extracts can be potentially used to develop naturalcolor stabilizers particularly for controlling 119871lowast and 119887lowast valuesin frozen beef burger

As mentioned already samples incorporated with BHTand natural extracts did not show any significant differencein Δ119864 value at the beginning of the storage time However atthe end of storage the lowest and highest changes in Δ119864wereobserved in cinnamon-incorporated and control samplesRedmeat color is an important property of visual appearanceand could influence meat purchasing decisions more thanany other quality parametersThe color of meat products andmeat is influenced by metmyoglobin percentage in muscleInitially the myoglobin was changed into oxymyoglobin(light pink color) which could result in brighter redmeat andthen oxymyoglobin was oxidized into metmyoglobin duringstorage [7]

34 Metmyoglobin Content Assay The amount of metmyo-globin has been positively linked to the extent of proteinoxidation in meat products The heme complex of heme(in) proteins consists of iron in the ferrous state (Fe+2)which turns into the ferric state (Fe+3) via a process calledautoxidation [27] The effects of natural extracts on thechanges of metmyoglobin content are shown in Figure 2Themaximum amount of metmyoglobin (7426) was measuredin antioxidant-free samples The presence of antioxidantsresulted in a significant decrease (1625ndash1847) in the

amounts of metmyoglobin developed during storage whichwas attributed to the strong antioxidant activity An etal [19] evaluated the percent metmyoglobin of the porkjerky samples incorporated with different kimchi powderconcentrations It has been reported that the metmyoglobincontents () of the samples prepared with various kimchipowder levels (ranged from 81 to 83) were significantly(119875 lt 005) lower than that of control sample (85) [19]There was no significant difference between the amounts ofmetmyoglobin under the influence of natural extracts or BHTindicating that these natural extracts can be utilized as asubstitute for BHT to prevent discoloration

The myoglobin reactions with peroxides result in theformation of lipid oxidation promoting compounds [28]The lowest amount of metmyoglobin was measured in thesamples formulated with cinnamon extract indicating thatit was more effective than the other antioxidants (eithernatural or synthetic) in preventing metmyoglobin formationA reverse relationship between the metmyoglobin level and119886lowast value was observed in this study A decrease in 119886lowast valuescorresponding to the decreased redness of lamb meat as aresult of myoglobin oxidation (metmyoglobin formation) hasbeen reported previously [29 30]

Metmyoglobin content increased during storage Thelowest increasing rate was observed in the samples incor-porated with rosemary extract The highest amount of met-myoglobin was observed in the control sample at the endof storage Changes in the metmyoglobin content of controlsample became significant after 15 days

6 Journal of Food Quality

Table 2 Thiobarbituric acid reactive substances (TBARS) values (mg malonaldehyde per kg) of beef burger during frozen storage at minus18∘CSample Storage period (days)

0 15 30 45 60Control 012 plusmn 001lowast 015 plusmn 002 020 plusmn 002 023 plusmn 001 041 plusmn 004BHT 010 plusmn 001 013 plusmn 001 015 plusmn 002 018 plusmn 001 023 plusmn 002Cinnamon extract 011 plusmn 001 013 plusmn 001 016 plusmn 001 017 plusmn 002 024 plusmn 002Rosemary extract 011 plusmn 001 013 plusmn 002 017 plusmn 002 019 plusmn 002 022 plusmn 002Shirazi thyme extract 012 plusmn 001 014 plusmn 002 017 plusmn 002 018 plusmn 001 026 plusmn 002lowastData represent averages of three independent repeats plusmn standard errors

35 Oxidative Stability Initiation is the step in which afatty acid radical is produced Two notable initiators inoxidative stability are OH∙ and HOO∙ which combines witha hydrogen atom to make water and a fatty acid radical Thefatty acid radical is not a very stable molecule so it reactsreadily with molecular oxygen thereby creating a peroxyl-fatty acid radical This radical is also an unstable species thatreacts with another free fatty acid producing a different fattyacid radical and a lipid peroxide or a cyclic peroxide if ithad reacted with itself This cycle continues as the new fattyacid radical reacts in the same wayThe radical reaction stopswhen two radicals react and produce a nonradical speciesThe lipid oxidation leads to produce of some componentscausing off-flavors and reduced nutritional quality such asmalondialdehyde and 4-hydroxynonenal

Thiobarbituric acid test can be used to determine thesecondary products of lipid oxidation in different foods suchas meat and its products [31] Thiobarbituric acid reactivesubstances (TBARS) values of different formulations (as afunction of storage time) are shown in Table 2 Exceptfor control sample the variations in TBARS values of theother formulations revealed a similar pattern Due to theabsence of antioxidant in formulation the observed changesin TBARS values of control were significantly (119875 lt 005)higher than others (8636 higher than rosemary) Natu-ral extracts were as effective as BHT for preventing lipidoxidation in beef burgers This observation indicated thatnatural herbal extracts are suitable replacers for syntheticantioxidant It has been reported that rosemary oleoresin(7704) and a mixture of BHT and BHA (7869) wasequally efficient in inhibiting the lipid oxidation of breakfastsausage containing 25 turkey meat [32] These findings arealso in good agreement with those of Mielnik et al [33] whoreported lower TBARS values after cooking of mechanicallydeboned turkey meat already stored in dark cold and treatedwith rosemary (8834) and grape seed extracts (8383)Sanchez-Escalante et al [34] reported that incorporatingrosemary essential oil into beef patties led to a significant(119875 lt 005) decrease (6400) in TBARS values during coldstorage The essential oil of rosemary was also effective inpreventing (7243) the rancidity of heat-treated turkeymeatproducts [35] It has also been reported that rosemary extractaddition into deboned poultry meat can protect (9820) theproduct from cooking-induced oxidation [36]

Regardless of sample type examined TBARS valuesincreased significantly during the frozen storage and reached

43

45

47

49

51

53

55

57

59

Tota

l aer

obic

bac

teria

l cou

nt (l

og cf

ug)

15 30 45 600Storage period (Days)

52

53

54

55

56

57

58

59

6

61

pH

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

Figure 3 Total aerobic bacterial count (log cfug) (solid symbols)and pH value (open symbols) of different beef burger formulationsas a function of storage time

to a maximum amount of 041mg malonaldehyde per kg inantioxidant-free (control) sample after 60 days At TBARSvalues of 20 off-flavors are definitely detectable and themeatis considered to be unacceptable [37]

36 Changes in pH Values Changes in pH values of beefburgers during frozen storage are shown in Figure 3 Allformulations revealed relatively similar pH values just afterproduction ranging from 588 to 593 coinciding with theISIRI 2008 Mohamed and Mansour [38] similarly reportedthat no significant differences (119875 gt 005) were observed in thepH values of beef patties after incorporating natural herbalextracts

A downward pattern of different rates was observed in thepH values of all formulations during frozen storage As nomicrobial growth was expected during storage the decreasein the pH values could be attributed to the microbial growthduring thawing (by consuming sugar and producing organicacids) Control sample had the lowest pH (551) at the end ofstorage Emiroglu et al [39] reported that the pH values of

Journal of Food Quality 7

all fresh ground beef patty samples treated with thyme andoregano generally decreased after sixth day of storage (119875 gt005)

Also the result showed that to decrease pH amount oflipid oxidation and metmyoglobin significantly increasedLapidot et al (2005) evaluated lipid peroxidation of grilledred turkey muscle (Donor Kabab) as affected by pH In thisstudy they show indeed that lipid peroxidation and myo-globin of a real fast food (turkey Doner Kebab shawarma) issignificantly more rapidly oxidized at pH 30 than at pH 50

37 Microbial Growth As shown in Figure 3 total aerobicbacterial counts of antioxidants-incorporated formulationswere not significantly (119875 lt 005) different The highestamount of total count was observed in control sample(Figure 3) Shirazi thyme-incorporated beef burgers had thelowest microbial count which could be attributed to thehigh antimicrobial properties resulting from thymol and car-vacrol The antibacterial mechanism of thymol and carvacrolis the disruption of the cytoplasmic membrane which raisesits permeability and depolarizes its potential Total countof frozen raw beef burger should be lower than 6 log cfug[40] Except for the control sample the microbial counts ofbeef burgers were lower than the maximum allowed countA relatively good correlation was observed between the pHvalues and total aerobic counts For example control samplehad the lowest pH and the highestmicrobial count Rosemaryextract (1000 ppm) inhibitory effect on the microbial growthof surface-applied beef steaks has been reported by Djenaneet al [41] However Sanchez-Escalante et al [34] reportedthat rosemary did not affect the microbial counts of beefpatties during storage (3 logCFUg)

An increase in the microbial counts was observed duringstorage but not beyond the standard range As a rule ofthumb in good manufacturing and hygienic practices duringpreparation of beef burger and its related products rapidand proper storage is important for decreasing the microbialgrowth and enhancing the shelf life

Vieira et al [42] studied the effect of frozen storage condi-tions (temperature and length of storage) on microbiologicaland sensory quality of rustic crossbred beef at different statesof ageing The result showed that psychrotrophic bacteriaincreased (138 logCFUg) significantly during 90-day storage38 Sensory Properties Color flavor and texture are themostimportant sensory attributes which influence the acceptabil-ity of meat products by consumers [43] Sensory evaluationresults of cooked beef burgers are shown in Figure 4 Gener-ally incorporating Shirazi thyme cinnamon and rosemaryextracts into beef burger formulations had no significantinfluence on the sensory properties Although samples for-mulated with Shirazi thyme and cinnamon extracts with6944 and 7167 acceptability obtained the highest tastescores by panelists (119875 lt 005) The antioxidant prop-erties of natural extracts were the main reason for theincreased sensory scores of natural extract-incorporatedformulations through preventing the formation of oxidation-mediated off-flavors and off-odors (short-chain aldehydes

4

45

5

55

6

65

7Appearance

Taste

OdorTexture

Overall

ControlBHTRosemary extract

Shirazi thyme extractCinnamon extract

Figure 4 Sensory evaluation of different beef burger formulationsa 9-point descriptive scale (1 = extremely poor and 9 = highlyacceptable) was used during evaluation

and ketones) during storage Moreover the presence ofpleasant volatile constituents in natural extracts (particu-larly in cinnamon and Shirazi thyme) led to an increasedsensory score in comparison to the BHT-incorporatedformulation

A significant increase in the flavor scores of beef pattiesincorporated with antioxidant mechanically deboned poul-try meat during frozen storage was similarly reported byMohamed and Mansour [38]

4 Conclusion

This work aimed to study the possible replacement ofsynthetic antioxidant BHT with natural extracts (includingShirazi thyme cinnamon and rosemary extracts) in beefburger formulation Different samples were prepared thendifferent characteristics such as protein and lipid oxidationand physicochemical microbial and sensory properties wereevaluated during frozen storage Herbal extracts could inhibitthe lipid oxidation in formulated burgers Moreover it wasdemonstrated that natural herbal extracts were generallybetter than BHT in preventing the lipid and protein oxi-dations as well as improving the sensory attributes of beefburgersTherefore it can be concluded that natural extracts ofShirazi thyme (0022mgmL) cinnamon (0373mgmL) androsemary (0062mgmL) can be used as natural substitutesfor BHT (0107mgmL)This substitutionmay have potentialimplication for developing green-labeled meat product Infuture studies it would be informative to study the effect ofmixed extracts and their possible synergistic or antagonisticeffects in extending the shelf life of meat products

8 Journal of Food Quality

Additional Points

Practical Applications Beef burger containing natural antiox-idant is one of themost important functional food for humanconsumption attributable to its nutritional properties andhealth effects However the nutraceutical properties of thisfood have improved due to alternative BHT with extractsThe present investigation demonstrated the effects of addingvarious natural antioxidants to the beef burger so as tomonitor the changes that occur to the physicochemicalantimicrobial and sensorial properties of the beef burger

Conflicts of Interest

The authors declare that they have no conflicts of interest

Acknowledgments

This research project was financially supported by ScientificAffairs Shiraz University and Department of Food Scienceand Technology Shiraz University Shiraz Iran

References

[1] D Ladikos and V Lougovois ldquoLipid oxidation in muscle foodsa reviewrdquo Food Chemistry vol 35 no 4 pp 295ndash314 1990

[2] C JMussinan andM JMorello ldquoFlavor analysis developmentsin isolation and characterizationrdquo American Chemical Societypp 343ndash358 1998

[3] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWTmdashFoodScience and Technology vol 68 pp 385ndash390 2016

[4] G Comi E Tirloni D Andyanto M Manzano and LIacumin ldquoUse of bio-protective cultures to improve the shelf-life and the sensorial characteristics of commercial hamburg-ersrdquo LWTmdashFood Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[5] F Shahidi ldquoAntioxidants in food and food antioxidantsrdquoFoodNahrung vol 44 pp 158ndash163 2000

[6] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[7] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[8] H H Hashemi Gahruie M H Eskandari G Mesbahi andM A Hanifpour ldquoScientific and technical aspects of yogurtfortification a reviewrdquo Food Science and Human Wellness vol4 no 1 pp 1ndash8 2015

[9] K Yamazaki S Kawamorita H Ohmiya and M SawamuraldquoDirected ortho borylation of phenol derivatives catalyzed by asilica-supported iridium complexrdquo Organic Letters vol 12 no18 pp 3978ndash3981 2010

[10] A Roberts and L A Haighton ldquoA hard look at FDArsquos review ofGRAS noticesrdquo Regulatory Toxicology and Pharmacology vol79 pp S124-S128 2016

[11] H H Hashemi Gahruie E Ziaee M H Eskandari andS M Hosseini ldquoCharacterization of basil seed gum-basededible films incorporated with Zataria multiflora essential oilnanoemulsionrdquo Carbohydrate Polymers vol 166 pp 93ndash1032017

[12] S K Devatkal K Narsaiah and A Borah ldquoAnti-oxidant effectof extracts of kinnow rind pomegranate rind and seed powdersin cooked goatmeat pattiesrdquoMeat Science vol 85 no 1 pp 155ndash159 2010

[13] M Estevez R Ramırez S Ventanas and R Cava ldquoSage androsemary essential oils versus BHT for the inhibition of lipidoxidative reactions in liver paterdquo LWTmdashFood Science andTechnology vol 40 no 1 pp 58ndash65 2007

[14] E Abdollahzadeh M Rezaei and H Hosseini ldquoAntibacterialactivity of plant essential oils and extracts the role of thymeessential oil nisin and their combination to control listeriamonocytogenes inoculated in minced fish meatrdquo Food Controlvol 35 no 1 pp 177ndash183 2014

[15] A Alaklabi I A Arif A Ahamed R Surendra Kumar andA Idhayadhulla ldquoEvaluation of antioxidant and anticanceractivities of chemical constituents of the saururus chinensis rootextractsrdquo Saudi Journal of Biological Sciences 2017

[16] M Cam Y Hısıl and G Durmaz ldquoClassification of eightpomegranate juices based on antioxidant capacity measured byfourmethodsrdquo FoodChemistry vol 112 no 3 pp 721ndash726 2009

[17] AOAC Association of Official Agricultural Chemists ldquoOfficialmethods of analysis of AOAC Internationalrdquo in AgricultureChemicals Contaminants Drugs vol 1 AOAC InternationalArlington VA USA 16th edition 1995

[18] K L Yam and S E Papadakis ldquoA simple digital imagingmethodfor measuring and analyzing color of food surfacesrdquo Journal ofFood Engineering vol 61 no 1 pp 137ndash142 2004

[19] K-I An J-H Choi Y-S Choi et al ldquoEffects of kimchi powderon quality characteristics of semi-dried pork jerkyrdquo KoreanJournal for Food Science of Animal Resources vol 30 no 2 pp198ndash205 2010

[20] B Kodal Coskun E Calikoglu Z Karagoz Emiroglu and KCandogan ldquoAntioxidant active packaging with soy edible filmsand oregano or thyme essential oils for oxidative stability ofground beef pattiesrdquo Journal of Food Quality vol 37 no 3 pp203ndash212 2014

[21] B Shan Y Z Cai M Sun and H Corke ldquoAntioxidant capacityof 26 spice extracts and characterization of their phenolicconstituentsrdquo Journal of Agricultural and Food Chemistry vol53 no 20 pp 7749ndash7759 2005

[22] A-M Roussel I Hininger R Benaraba T N Ziegenfuss andR A Anderson ldquoAntioxidant effects of a cinnamon extract inpeople with impaired fasting glucose that are overweight orobeserdquo Journal of the American College of Nutrition vol 28 no1 pp 16ndash21 2009

[23] S Moreno T Scheyer C S Romano and A A VojnovldquoAntioxidant and antimicrobial activities of rosemary extractslinked to their polyphenol compositionrdquo Free Radical Researchvol 40 no 2 pp 223ndash231 2006

[24] F Sharififar M H Moshafi S H Mansouri M Khodashenasand M Khoshnoodi ldquoIn vitro evaluation of antibacterial andantioxidant activities of the essential oil and methanol extractof endemic Zataria multiflora Boissrdquo Food Control vol 18 no7 pp 800ndash805 2007

[25] R Carpenter M N OrsquoGrady Y C OrsquoCallaghan N M OrsquoBrienand J P Kerry ldquoEvaluation of the antioxidant potential of grape

Journal of Food Quality 9

seed and bearberry extracts in raw and cooked porkrdquo MeatScience vol 76 no 4 pp 604ndash610 2007

[26] M T Nunez de Gonzalez B S Hafley R M Boleman R KMiller K S Rhee and J T Keeton ldquoAntioxidant propertiesof plum concentrates and powder in precooked roast beef toreduce lipid oxidationrdquo Meat Science vol 80 no 4 pp 997ndash1004 2008

[27] M P Richards and M A Dettmann ldquoComparative analysisof different hemoglobins autoxidation reaction with peroxideand lipid oxidationrdquo Journal of Agricultural and FoodChemistryvol 51 no 13 pp 3886ndash3891 2003

[28] J Everse and N Hsia ldquoThe toxicities of native and modifiedhemoglobinsrdquo Free Radical Biology and Medicine vol 22 no6 pp 1075ndash1099 1997

[29] C Kennedy D J Buckley and J P Kerry ldquoInfluence of differentgas compositions on the short-term storage stability of mother-packaged retail-ready lamb packsrdquo Meat Science vol 69 no 1pp 27ndash33 2005

[30] J P Kerry M G OrsquoSullivan D J Buckley P B Lynch andP A Morrissey ldquoThe effects of dietary 120572-tocopheryl acetatesupplementation and modified atmosphere packaging (MAP)on the quality of lamb pattiesrdquo Meat Science vol 56 no 1 pp61ndash66 2000

[31] J Fernandez J A Perez-Alvarez and J A Fernandez-LopezldquoThiobarbituric acid test for monitoring lipid oxidation inmeatrdquo Food Chemistry vol 59 no 3 pp 345ndash353 1997

[32] S Barbut D B Josephson and A J Maurer ldquoAntioxidantproperties of rosemary oleoresin in Turkey sausagerdquo Journal ofFood Science vol 50 no 5 pp 1356ndash1359 1985

[33] M B Mielnik K Aaby and G Skrede ldquoCommercial antioxi-dants control lipid oxidation in mechanically deboned turkeymeatrdquoMeat Science vol 65 no 3 pp 1147ndash1155 2003

[34] A Sanchez-Escalante D Djenane G Torrescano J A Beltranand P Roncales ldquoThe effects of ascorbic acid taurine carnosineand rosemary powder on colour and lipid stability of beef pattiespackaged in modified atmosphererdquoMeat Science vol 58 no 4pp 421ndash429 2001

[35] M B Mielnik S Sem B Egelandsdal and G Skrede ldquoBy-products from herbs essential oil production as ingredient inmarinade for Turkey thighsrdquo LWTmdashFood Science and Technol-ogy vol 41 no 1 pp 93ndash100 2008

[36] J H Macneil P S Dimick and M G Mast ldquoUse of chemicalcompounds and a rosemary spice extract in quality mainte-nance of deboned poultry meatrdquo Journal of Food Science vol38 no 6 pp 1080-1081 1973

[37] E TEC ldquoMeat technology update 1-6 2009rdquo[38] H M H Mohamed and H A Mansour ldquoIncorporating

essential oils of marjoram and rosemary in the formulation ofbeef patties manufactured with mechanically deboned poultrymeat to improve the lipid stability and sensory attributesrdquoLWTmdashFood Science and Technology vol 45 no 1 pp 79ndash872012

[39] Z K Emiroglu G P Yemis B K Coskun and K CandoganldquoAntimicrobial activity of soy edible films incorporated withthyme and oregano essential oils on fresh ground beef pattiesrdquoMeat Science vol 86 no 2 pp 283ndash288 2010

[40] ISIR Raw frozen hamburgermdashSpecifications vol 2304 Instituteof standards and industrial research of Iran Karaj Iran 3rdedition 2008

[41] DDjenane A Sanchez-Escalante J A Beltran andP RoncalesldquoAbility of 120572-tocopherol taurine and rosemary in combination

with vitamin C to increase the oxidative stability of beef steakspackaged in modified atmosphererdquo Food Chemistry vol 76 no4 pp 407ndash415 2002

[42] C Vieira M T Diaz B Martınez and M D Garcıa-CachanldquoEffect of frozen storage conditions (temperature and lengthof storage) on microbiological and sensory quality of rusticcrossbred beef at different states of ageingrdquo Meat Science vol83 no 3 pp 398ndash404 2009

[43] J Aliakbarlu and S Khalili Sadaghiani ldquoEffect of avishaneshirazi (zataria multiflora) and clove (syzygium aromaticum)essential oils on microbiological chemical and sensory proper-ties of ground sheep meat during refrigerated storagerdquo Journalof Food Quality vol 38 no 4 pp 240ndash247 2015

Research ArticleOptimization of Ultrasound Extraction of Cactus Pear(Opuntia ficus indica) Seed Oil Based on AntioxidantActivity and Evaluation of Its Antimicrobial Activity

Mariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-CansinoErnesto Alaniacutes-Garciacutea Luis Delgado-Olivares Joseacute Alberto Ariza-OrtegaEsther Ramiacuterez-Moreno and Joseacute de Jesuacutes Manriacutequez-Torres

Centro de Investigacion Interdisciplinario Area Academica de Nutricion Instituto de Ciencias de la Salud Universidad Autonoma delEstado de Hidalgo Circuito Actopan-Tilcuautla SN Ex Hacienda La Concepcion 42160 San Agustın Tlaxiaca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 20 February 2017 Accepted 9 April 2017 Published 27 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Marıa de los Angeles Ortega-Ortega et alThis is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The purpose of the present study was to determine the optimal ultrasound conditions (amplitude level and time) for the extractionof cactus pear seed oil with the highest antioxidant activity using a closed system Seed oil was analyzed for yield antioxidant activityby ABTS and DPPH and antimicrobial activity Conventional extraction methods were assessed for comparison Amplitude levelsignificantly affected antioxidant activity in linear terms (p lt 00001 DPPH and p lt 0001 ABTS resp) so at lower amplitudes thehigher antioxidant activity was achieved The optimum ultrasound extraction conditions were of 78 amplitude for 10min andyielded antioxidant activity values of 6625mg AAE100 g and 289120583mol TE100 g for ABTS and DPPH respectively Comparedwith conventional extraction methods ultrasound exhibited lower oil yield and antioxidant activity but had the potential toachieve comparable results if multiple ultrasound extractions are performed in the time needed by conventional methods Seed oilsshowed similar antimicrobial activity despite the extraction method and were more effective against Escherichia coli The resultsdemonstrated that ultrasound can be an alternative extraction method of seed oils from fruits such as cactus pear

1 Introduction

Cactus pear fruit (Opuntia ficus indica) is common in aridand semiarid regions around the world [1] This fruit that ismainly consumed fresh in Mexico [2] is composed by pulppeel and seeds [3] According to several studies cactus pearfruit has bioactive compounds [4 5] with high antioxidantand antimicrobial activity [6 7] Some of these compoundsare found in the seeds [8] which comprise 3 to 15 of thecactus pear pulp [9] and are usually considered waste afterpulp processing [7] Seeds also have a high content of oil(988 gkg) [10] characterized by high levels of linoleic andoleic acids [7] and other components as phenols [11] all whichmay contribute to humanhealth [12] Currently seed oils havebeen used as natural agents for food preservation [13] andmany have exhibited antimicrobial and antioxidant activity

some of these oils are from pumpkin [14] apple [15] blackcumin [16] and basil [17] among other seeds Cactus pearseeds fromOpuntia dillenii also have a high antioxidant activ-ity derived from bioactive compounds such as polyphenolsand polyunsaturated fatty acids [18] Some polyunsaturatedfatty acids have also been identified in seeds from Opuntiaficus indica [19 20] implying that these seeds may also havehigh antioxidant activity

Seed oil is usually extracted by means of conventionalmethods such as Soxhlet and maceration using heat agita-tion or long extraction times [21] Microwave supercriticalfluids and ultrasonic assisted extraction are unconventionalmethods that exert a physical effect on the sample [22]Ultrasound has been used to extract antioxidants frommanyfood materials including seeds Ultrasound and ultrasound-assisted extractions use sound waves to produce cavitation

HindawiJournal of Food QualityVolume 2017 Article ID 9315360 9 pageshttpsdoiorg10115520179315360

2 Journal of Food Quality

microbubbles that collapse violently in the sample and facili-tate the release and extraction of several compounds [23ndash25]Some researchers had evaluated ultrasound-assisted extrac-tion in an open system using a sonicator probe directly onthe liquid sample to obtain seed oil fromflaxseed [26] Koreanpine [27] and pomegranate [28] The purpose of the presentstudy was to optimize the extraction conditions of cactuspear seed oil using ultrasound in a closed system based onantioxidant activity and using response surfacemethodologyYield extraction and antioxidant and antimicrobial activitywere compared with conventional methods

2 Materials and Methods

21 Sample Green cactus pear (Opuntia ficus indica) Reynavariety was provided by the Mexican Association CoMeN-Tuna (Consejo Mexicano del Nopal y la Tuna AC ofActopanHidalgoMexico) in spring of 2012Thegreen cactuspear seeds were obtained after several washes with water thatremoved the pulp and residues The seeds were leaved todry at ambient temperature until they reached a moisture of643 After the seeds were crushed using an industrial mill(Cyclotec 1093 Tecator Hoganas AB Sweden) the powderwas passed through a mesh sieve to obtain a particle size ofapproximate 05mm and then stored in sealed plastic bags atroom temperature and dark conditions

22 Ultrasound Extraction Ultrasound (VCX-1500 Sonic ampMaterials Inc Newtown CTUSA) at 1500Wwith a constantfrequency of 20 kHz and a probe of 25mm was used forthe extraction of green cactus pear seeds oil Extractionfrom milled and sieved seeds (20 g) was carried out at anamplitude and time ranges of 80 to 90 and 5 to 15minrespectively and a fixed outlet temperature of 25∘C A sampleof 400mL was introduced in a jacketed vessel with waterat 4∘C circulating through the secondary layer [29] Afterextraction the aqueous and solid phases were separatedby filtration using a vacuum pump (DOA-P704-AA GASTManufacturing Inc BentonHarbor MI USA) Both phasesaqueous and solid (this last was dried) (Weston 74-1001-wWeston Products LLC Strongsville OH USA) were mixedwith hexane for 30min and then separated from the solventby filtration The aqueous phase was centrifuged (Allegra25R Beckman Couler CA USA) at 10000 rpm for 30minat 4∘C and was stored in plastic containers and kept frozenuntil analysis The solid phase was stored in hermeticallysealed bags in the dark The solvent obtained from the twophaseswas evaporated (BUCHILabortechnikAG Flawil SGSwitzerland) at 40∘C to obtain the oil

23 Soxhlet Extraction Soxhlet extraction was performedaccording to the AOAC [30] Milled and sieved seeds (5 g)hexane (120mL) and a universal fat extraction system (BuchiLabortechnik AG Flawil SG Switzerland) were used

24 Maceration Extraction Milled and sieved seeds (10 g)were introduced in a previously defatted cotton bag andthen immersed in 200mL of hexane in a closed glass at atemperature of asymp25∘C After the sample was stored in a dark

place for 24 hrs the oil was obtained after solvent evaporationusing a rotary evaporator (BUCHI Labortechnik AG FlawilSG Switzerland) at 40∘C

25 Yield Oil yield was determined according to Chouguiet al [31] using the following equation

Oil () = (1198721 minus11987201198722 ) times 100 (1)

where1198720 is the weight of the empty Eppendorf tube (g)1198721is the weight of the Eppendorf tube after evaporation (g) and1198722 is the weight of the milled seeds (g)

The oil was stored in 2mL amber Eppendorf tubes atminus32∘C until analysis

26 Determination of Antioxidant Activity

261 ABTS Assay Antiradical capacity by ABTS was mea-sured according to Kuskoski et al [32] The radical cation221015840azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) diam-monium salt (ABTS∙+) was produced by reacting 7mMABTSstock solution with 245mM potassium persulfate in thedark at room temperature for 16 hrs before being used TheABTS∙+ solution was diluted with deionized water to anabsorbance of 070 plusmn 010 at 754 nm An aliquot of 20120583L ofsample was added to 980120583L of the diluted ABTS∙+ solutionand absorbance readings were taken after 7min incubationat room temperature The absorbance of the mixture wasmeasured at 754 nm in themicroplate reader (PowerWaveXSUV-Biotek software KC Junior VT USA) and antioxidantcapacity was expressed as mg ascorbic acid equivalent per100 g of oil (mg AAE100 g)

262 DPPH Assay Antiradical activity was measured using11-diphenyl-2-picrylhydrazyl (DPPH∙) radical as describedby Morales and Jimenez-Perez [33] A methanol-acetatesolution (74mg100mL) of the stable DPPH∙ radical wasprepared A sample aliquot of 100120583Lwas placed into vials and500 120583L of DPPH∙ solution was added before the mixture wasleft to sit at room temperature for 1 hr Finally absorbancewasmeasured at 520 nm in the microplate reader (Power WaveXS UV-Biotek software KC JuniorWinooski VT USA) andantioxidant activity was expressed as 120583mol of Trolox equiva-lents per 100 g of oil (120583mol TE100 g)

27 Experimental Design

271 Optimization The optimization of the ultrasoundextraction conditions was performed using the responsesurface methodology (RSM) with a central composite rotat-able design for two independent extraction variables at fivelevelsThe independent extraction variables (amplitude level80ndash90 time 5ndash15min) were determined based on prelimi-nary experiments where higher antioxidant activity by ABTSand DPPH was observed Design consisted in thirteen com-binations with five central points replicates (Table 1) Exper-imental data were subjected to multiple nonlinear regression

Journal of Food Quality 3

Table 1 Experimental design matrix

Numbera Pattern Amplitude level () Time (min)119883119894 119883119895

(1) 00 85 10(2) +minus 90 5(3) ++ 90 15(4) 00 85 10(5) A0 92 10(6) minusminus 80 5(7) 00 85 10(8) a0 78 10(9) 0A 85 17(10) minus+ 80 15(11) 00 85 10(12) 00 85 10(13) 0a 85 3aNonrandomized

analysis (JMP 702 SAS Institute Inc Cary NC USA) fittedto a second-order polynomial model

119884 = 1205730 +2

sum119894=1

120573119894119883119894 +2

sum119894=1

1205731198941198941198832119894 +sum119894

sum119895=119894+1

120573119894119895119883119894119883119895 (2)

where 119884 is the predicted response 1205730 is the constant coeffi-cient120573119894 is the lineal coefficient120573119894119894 is the quadratic coefficientand120573119894119895 is the interaction coefficients In thismodel119883119894 and119883119895are the independent extraction variables amplitude level ()and time (min) respectively

The adequacy of themathematicalmodel was determinedusing the coefficient 1198772The significance of the model regres-sion coefficients was evaluated using an analysis of varianceThree-dimensional curves from the response surface plotswere obtained to interpret the effects of the interactionbetween independent variables on the response variablesContour plots were generated to represent the extrapolationand interpret the optimization of the extraction variablesusing the Sigma Plot 123 graphing software (SYTAT softwareInc Richmond CA USA)

272 Treatment Comparison Comparison between extrac-tion methods (ultrasound-optimized Soxhlet and macera-tion) was carried out by a one-way analysis of variance(ANOVA) All determinations were performed in triplicateand significant differences between means were determinedby Duncan test (p le 005) using the SPSS program (150 SPSSInc Chicago IL USA)

28 Scanning Electron Microscopy Scanning electron micro-scopy (SEM) was used to examine the morphological alter-ations caused to the cactus pear seeds before and after theultrasound extraction Samples deposited on the siliconwaferwere coated with a thin layer of gold (Denton VacuumDesk V Moorestown NJ USA) applying 20 millitorr and

20mA during 4min Samples were observed in a scanningelectronic microcopy (JEOL JSM-6300 Peabody MA USA)at 1000 and 500 amplifications and micrographs were takento establish the structural comparison between both samples

29 Antimicrobial Activity The green cactus pear seed oilwas tested against one Gram-positive bacteria Staphylococ-cus aureus (ATCC 1654) and two Gram-negative bacteriaEscherichia coli (ATCC 25922) and Pseudomonas aeruginosa(ATCC 27853) All microorganisms were obtained from theMexicanMicrobial Culture Collection of CINVESTAV of theNational Polytechnic Institute (Mexico) For each microor-ganism bacterial suspensions were made in a soybean-casein digest medium to a concentration of approximately108 CFUmL

To evaluate the antimicrobial activity and the mini-mum inhibitory concentration (MIC) the disk diffusionmethod was used Each bacterial suspension (100 120583L fromthe 108 CFUmL) was spread on prepared agar plates (sterileStandardMethodsAgar for bacteria) Filter sterile paper discs(6mm in diameter) were impregnated with 6667 50 3333and 1667 120583L of the undiluted oil and were placed on theinoculated plates The negative control was hexane whileampicillin (10 120583g) and streptomycin (10 120583g) were used aspositive controls The plates where incubated at 37∘C (ArsaAR-130 Felisa Jalisco Mexico) for 24 hrs The diameters ofthe inhibition zones were measured in millimeters and theresults of MIC were expressed as 120583g120583L

3 Results and Discussion

31 Extraction Yield Table 2 shows the oil yields achievedby the ultrasound treatments The extraction yield variedfrom 375 to 6 and the maximum yield was obtained at thehighest amplitude level of 92 Oil yield strongly dependedon amplitude level probably because at high amplitudes thecavitation effect increases [21] and induces physical changeson the structure of the seed such as disruption of the cell wallsreduction of the particle size and increase of exposure areaThese conditions may facilitate the penetration of the solventand thus the extraction of oil [26 28 34] The maximumyield was achieved after 10min of treatment and longertimes (15min) at high amplitudes (90) did not increase oilextraction (Table 2) Albeit time is an important variable afteryield reaches a peak a longer treatment does not maximizeextraction the same was described by Zhang et al [27] forKorean pine seed who demonstrated that oil yield increasedwith time but when it reached amaximum yield equilibratedand then decreased gradually This may be attributed to aninitial complete fracture of the cell walls during the firstminutes of the cavitation effect [26 28 34]

32 Antioxidant Activity of Green Cactus Pear Seed OilExtracted by Ultrasound Due to the complexity of theoxidation processes it is advisable to performmore than onemethod to obtain the antioxidant profile of a sample [35]In order to determine the antioxidant activity of the green

4 Journal of Food Quality

Table 2 Extraction yield and antioxidant activity of green cactus pear seed oil extracted by ultrasound under different conditions

Extraction conditions Antioxidant activity

Amplitude level () Time (min) Oil yield () ABTS DPPHmg AAE100 g 120583mol TE100 g

85 10 575 plusmn 003 6615 plusmn 407 24610 plusmn 09290 5 415 plusmn 001 5598 plusmn 313 14176 plusmn 39090 15 485 plusmn 002 5993 plusmn 445 16702 plusmn 11485 10 525 plusmn 001 6812 plusmn 659 23601 plusmn 32292 10 600 plusmn 006 5584 plusmn 236 10163 plusmn 46880 5 525 plusmn 001 6607 plusmn 217 26707 plusmn 73785 10 375 plusmn 000 6837 plusmn 392 24505 plusmn 23778 10 540 plusmn 010 6599 plusmn 501 28926 plusmn 02685 17 560 plusmn 006 6578 plusmn 037 26009 plusmn 13380 15 540 plusmn 000 6691 plusmn 320 28496 plusmn 09385 10 575 plusmn 000 6773 plusmn 040 27755 plusmn 17185 10 530 plusmn 010 6744 plusmn 389 24508 plusmn 29285 3 550 plusmn 010 6763 plusmn 000 25005 plusmn 199plusmn standard deviation

Table 3 Antioxidant activity regression coefficients of the ultra-sound extraction conditions

Coefficient ABTS DPPH1205730 67562964a 24996199a

120573119894 minus3927762b minus6357459a120573119895 02724311 71702572120573119894119895 077572 18421052120573119894119894 minus3719624b minus2977102b120573119895119895 minus0826106 004258041198772adj 093 096120573119894 amplitude level 120573119895 time significance levels a119901 lt 00001 b119901 lt 0001

cactus pear seed oil two parameters were evaluated antiox-idant and scavenging capacity by ABTS and DPPH respec-tively The results and experimental design are described inTable 2 Antioxidant activity ranged from 5584 to 6837mgAAE100 g for ABTS and 10163 to 28926120583mol TE100 g forDPPH A 1198772 value closest to one or at least of 080 indicates agood fit of themodel [36]The1198772 values for ABTS andDPPHwere 093 and 096 respectively (Table 3) indicating thatthe averages obtained adjusted to the mathematical responsesurface model

33 Effect of Ultrasound Extraction Conditions on the Antiox-idant Activity of Cactus Pear Seed Oil In this study asecond-order polynomial model for predicting the antiox-idant activity of green cactus pear seed oil was obtainedby multiple linear regression analysis of the experimentaldata Table 3 shows the regression coefficients and significantprobabilities of the linear quadratic and interaction effects ofthe ultrasound conditions on the seed oil antioxidant activityBoth ABTS and DPPH values were significantly affected byamplitude level in linear term (120573119894) at 119901 lt 00001 DPPH and119901 lt 0001 ABTS respectively as well as in its quadratic term

(120573119894119894) at 119901 lt 0001 DPPH and ABTS The three-dimensionalsurface plots constructed to observe the effect of ultrasoundprocessing (Figure 1) demonstrated that antioxidant activitywas higher when the applied amplitude decreased

34 Optimization of the Ultrasound Extraction Conditions ofCactus Pear Seed Oil Optimal extraction conditions wereselected from the overlapped contour plots inwhich the effectof amplitude level and time on the antioxidant activity ofgreen cactus pear seed oil was considered

Figure 2 shows the optimal zone where the highestantioxidant activity by ABTS and DPPH was achieved Theconditions corresponded to amplitude of 78 applied for10min In this zone the values for antioxidant activity wereof 6625mg AAE100 g and 289 120583mol TE100 g for ABTS andDPPH respectively

35 Comparison between Methods

Extraction Yield and Antioxidant Activity Figure 3 comparesthe oil yields obtained by the three extraction methodsThe results revealed that the yield obtained using the opti-mized ultrasound extraction was significantly lower than theobtained with the Soxhlet and maceration procedures Thehigher oil yield obtained by Soxhlet could be attributed to theconstant and extended contact (4 to 6 hrs) of the sample withthe solvent at high temperatures in addition to the repeatedwashing cycles [37] The ultrasound yield was closer to thatof maceration method but this last one required longer time(24 hrs) as compared to 10min ultrasound treatment

The results of antioxidant activity by ABTS andDPPH areshown in Figure 4 Both parameters were significantly higherin the oil extracted by Soxhlet (5433 plusmn 084mg AAE100 gand 26660 plusmn 197 120583mol TE100 g resp) compared to theother extraction methods The ultrasound and macerationextractions exhibited similar antioxidant activity by ABTSwhile DPPH was significantly higher for the ultrasound seed

Journal of Food Quality 5

45

50

55

60

65

70

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(mg

AA

E100

g)A

ntio

xida

nt ac

tivity

(a)

50

100

150

200

250

300

350

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(120583m

ol T

E100

g)A

ntio

xida

nt ac

tivity

(b)

Figure 1 Effect of the ultrasound extraction on the antioxidant activity of green cactus pear seed oil (a) ABTS (b) DPPH

121

109

133145

157

169181

157

169

193

169

181

205

193

205

217

217

205

229

217

229

241

229

241

253

241

253

253

265

265

265

265

277

277

277

265

289

DPPH

5650

5650

557555005425

572558005875

5950

6025

6100

6175

6250

5950

6025

63256400

6175

6250

6250

6325

6475

6325

64006475

6400

6550

6475

6550

6550

6625

6625

6625

6700

6700

6700

6775

6775

6775

6700

6700

6625

6550

6475

6625

ABTS

Optimun condition

4

6

8

10

12

14

16

Tim

e (m

in)

80 82 84 86 88 90 9278Amplitude level ()

Figure 2 Optimal ultrasound extraction conditions of green cactuspear seed oil based on the highest antioxidant activity

oil Albeit the oil extracted by the Soxhlet method presentedhigher yield and antioxidant activity the ultrasound-assistedextraction may be enhanced if multiple extractions arecarried out in a time comparable to the required by theSoxhlet procedure (4ndash6 hrs)

36 Antimicrobial Activity Escherichia coli and Staphylo-coccus aureus are distributed in nature (water soil andvegetation) and are also part of the human intestinal

c

a

b

Ultrasound Soxhlet Maceration0

1

2

3

4

5

6

7

8Yi

eld

()

Figure 3 Cactus pear seed oil yield achieved by different extractionmethods abcDifferent letters mean significant differences betweenmethods (p lt 005)

b a b

b

a

c

Ultrasound Soxhlet Maceration0

255075

100125150175200225250275300

DPPH (120583mol TE100 g)ABTS (mg AAE100 g)

Figure 4 Antioxidant activity by ABTS and DPPH of cactus pearseed oil extracted by different methods abcDifferent letters meansignificant differences between methods (p lt 005)

6 Journal of Food Quality

Table 4 Antimicrobial activity of cactus pear seed oil extracted by different methods

Diameter of inhibition zone (mm)Oillowast (+) control (minus) control

Staphylococcus aureus (Gram-positive)Ultrasound 917 plusmn 029a 1889 plusmn 154 NDSoxhlet 950 plusmn 087a 1878 plusmn 164 NDMaceration 978 plusmn 069a 1811 plusmn 117 NDEscherichia coli (Gram-negative)Ultrasound 778 plusmn 019a 1556 plusmn 212 NDSoxhlet 756 plusmn 019a 1533 plusmn 265 NDMaceration 756 plusmn 038a 1400 plusmn 233 NDPseudomonas aeruginosa (Gram-negative)Ultrasound ND 1256 plusmn 038 NDSoxhlet ND 1222 plusmn 038 NDMaceration ND 1278 plusmn 038 NDlowastSeed oil 6667120583L (+) control ampicillin (disc 10 120583g Staphylococcus aureus and Escherichia coli) and streptomycin (disc 10 120583g Pseudomonas aeruginosa) (minus)control hexane ND not detected plusmn standard deviation a Same superscripts indicates that there is no significant difference (p gt 005)

microbiota [38] Pseudomonas aeruginosa besides beingpresent in the intestinalmicrobiota [39] is a bacteria found inthe soil fertilizers and water used for food production [40]and thus it can contaminate fresh or processed food whichis an indicator of inadequate sanitation or improper han-dling during food production [41] Table 4 summarizes theantimicrobial activity of green cactus pear seed oil Extractionmethod did not have a significant effect on the antimicrobialactivity against Staphylococcus aureus and Escherichia colibut the effect was lower than the positive controls Theseresults may be explained by the similar seed oil concentrationand combined action of compounds on the structure ofmicrobial cells [42 43] despite the extraction method Seedoil did not exhibit antimicrobial activity against Pseudomonasaeruginosa probably due to the oil chemical composition thetype of microorganism and the own characteristics of thebacteria [42ndash44]The antimicrobial activity of oils is generallymore effective against Gram-positive bacteria in comparisonto Gram-negative bacteria which are more resistant mainlybecause their outer membrane is less permeable [42 4345 46] The results suggest that Pseudomonas aeruginosawas more resistant than Escherichia coli probably due tothe lipopolysaccharides present in the outer membrane thatrestrict the diffusion of compounds making it less permeable[45]The resistance can also be caused by systems of exclusionpumps that eject antimicrobial compounds from the inside ofthe bacteria before they can cause damage [39 44]

37 Effect of Ultrasound on the Physical Structure Scanningelectron micrographs of the green cactus pear seeds powderbefore and after the ultrasound treatment at magnificationsfactors of 1000x and 500x are shown in Figure 5 Beforethe ultrasound treatment and despite the previous millingprocess in the control sample it was possible to identify intactstructures of the seeds cell as well as some starch granules

(Figure 5(a)) After the ultrasound treatment the cell struc-tural damage and the variations in the shape and size of theparticles were observed (Figure 5(b)) For instance starchgranules were not observed because sonication fragmentedthese particles while cavitation phenomenon disrupted thecell structures of the seeds [47 48]

4 Conclusions

This study demonstrated that response surface methodologyand a second-order polynomial model were effective tools todetermine the optimumprocessing conditions of ultrasound-assisted extraction based on the maximum values of antiox-idant activity The results demonstrated that cactus pearseed oil has good antioxidant and antimicrobial propertiesUltrasound-assisted extraction was comparable to macera-tion but a single ultrasound process yielded less oil andlower antioxidant activity than solvent extraction (Soxhlet)Ultrasound can be considered an alternative technology forthe extraction of seed oil but further research is required todetermine the uses of the seed oil and the technology withinthe food industry and the potential of several ultrasoundcycles at the optimized conditions

Conflicts of Interest

The authors declare that there are no conflicts of interest

Acknowledgments

This work was financially supported by Programa Integral deFortalecimiento Institucional (PIFI 2014-2015) The authorsacknowledge Mexican Association CoMeNTuna (HidalgoMexico) for providing the plant materials Marıa de losAngeles Ortega-Ortega participated in this research and she

Journal of Food Quality 7

(i) (ii)

A A

(a)

(i) (ii)

(b)

Figure 5 Scanning electron micrographs of green cactus pear seed powder before (a) and after (b) ultrasound treatment (i) 1000x (ii) 500xA The black circle shows a starch granule

received her Bachelorrsquos degree in nutrition in the Universi-dad Autonoma del Estado de Hidalgo Mexico (Act no 12872016)

References

[1] L Lozano ldquoEcofisiologıa de la tuna (Opuntia ficusmdashindica (L)Mill)rdquo Horticultura Argentina vol 30 no 72 pp 37ndash52 2011

[2] LMedina-Torres J A Gallegos-Infante R F Gonzalez-Laredoand N E Rocha-Guzman ldquoDrying kinetics of nopal (Opuntiaficusmdashindica) using three different methods and their effect ontheir mechanical propertiesrdquo LWTmdashFood Science and Technol-ogy vol 41 no 7 pp 1183ndash1188 2008

[3] J A Reyes-Aguero J R Aguirre-Rivera and H M HernandezldquoSystematic notes and a detailed description of Opuntia ficusindica (L)Mill (Cactaceae)rdquoAgrociencia vol 39 no 4 pp 395ndash408 2005

[4] H I Jun M N Cha E I Yang D G Choi and Y S KimldquoPhysicochemical properties and antioxidant activity of Koreancactus (Opuntia humifusa) cladodesrdquoHorticulture Environmentand Biotechnology vol 54 no 3 pp 288ndash295 2013

[5] A Rabhi H Falleh F Limam R Ksouri C Abdelly and ARaies ldquoUpshot of the ripening time on biological activitiesphenol content and fatty acid composition of Tunisian Opuntiaficus-indica fruitrdquo African Journal of Biotechnology vol 12 no40 pp 5875ndash5885 2013

[6] M Kaur A Kaur and R Sharma ldquoPharmacological actions ofOpuntia ficus indica a reviewrdquo Journal of Applied Pharmaceuti-cal Science vol 2 no 7 pp 15ndash18 2012

[7] M R Bhatt and P S Nagar ldquoEvaluation of physicochemicalproperty and fatty acid composition ofOpuntia elatior seed oilrdquoJournal of the Professional Association for Cactus Developmentvol 15 pp 13ndash19 2013

[8] M Ennouri H Fetoui E Bourret N Zeghal F Guermazi andH Attia ldquoEvaluation of some biological parameters of Opuntiaficus indica 2 Influence of seed supplemented diet on ratsrdquo Bio-resource Technology vol 97 no 16 pp 2136ndash2140 2006

[9] SAGARPA Secretarıa de Agricultura Ganaderıa DesarrolloRural Pesca y Alimentacion Pliegos de condiciones para eluso de la marca oficial Mexico calidad suprema en tuna 2005httpwwwmexicocalidadsupremaorgassetsgaleriaPC 0462005 Tunapdf

[10] M F Ramadan and J-TMorsel ldquoOil cactus pear (Opuntia ficus-indica L)rdquo Food Chemistry vol 82 no 3 pp 339ndash345 2003

[11] K El-Mostafa Y Kharrassi A Badreddine et al ldquoNopal Cactus(Opuntia ficus-indica) as a source of bioactive compounds fornutrition health and diseaserdquo Molecules vol 19 no 9 pp14879ndash14901 2014

[12] Z Ghazi M Ramdai M L Fauconnier B El Mahi and RCheikh ldquoFatty acids sterols and Vitamin E composition of seedoil of Opuntia ficus indica and Opuntia dilenii from MoroccordquoJournal of Materials and Environmental Science vol 4 no 6 pp967ndash972 2013

[13] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extrac of Laururs nobillis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

8 Journal of Food Quality

[14] A Nawirska-Olszanska A Kita A Biesiada A Sokol-Łętowska and A Z Kucharska ldquoCharacteristics of antioxidantactivity and composition of pumpkin seed oils in 12 cultivarsrdquoFood Chemistry vol 139 no 1ndash4 pp 155ndash161 2013

[15] V Cervantes-Cardoza N E Rocha-Guzman J A Gallego-Infante M Rosales-Castro L Medina-Torres and R FGonzalez-Laredo ldquoActividad antioxidante de extractos desemilla de tres variedades de manzana (Malus domestica Borkh-Rosaceae-)rdquo Boletın Latinoamericano y del Caribe de PlantasMedicinales y Aromaticas vol 9 no 6 pp 446ndash456 2010

[16] M K M Nair P Vasudevan and K Venkitanarayanan ldquoAnti-bacterial effect of black seed oil onListeriamonocytogenesrdquoFoodControl vol 16 no 5 pp 395ndash398 2005

[17] A I Hussain F Anwar S T H Sherazi and R PrzybylskildquoChemical composition antioxidant and antimicrobial activi-ties of basil (Ocimum basilicum) essential oils depends on sea-sonal variationsrdquo Food Chemistry vol 108 no 3 pp 986ndash9952008

[18] W Liu Y J Fu Y G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[19] M T Labuschagne and A Hugo ldquoOil content and fatty acidcomposition of cactus pear seed compared with cotton andgrape seedrdquo Journal of Food Biochemistry vol 34 no 1 pp 93ndash100 2010

[20] S Zine S Gharby and M El Hadek ldquoPhysicochemical char-acterization of Opuntia ficus-indica seed oil from MoroccordquoBiosciences Biotechnology Research Asia vol 10 no 1 pp 99ndash105 2013

[21] R Azuola and P Vargas ldquoExtraccion de sustancias asistida porultrasonido (EUA)rdquoTecnologıa enMarcha vol 20 no 4 pp 30ndash40 2007

[22] M Gao and C Z Liu ldquoComparison of techniques for theextraction of flavonoids fromcultured cells of SaussureamedusaMaximrdquo World Journal of Microbiology and Biotechnology vol21 no 8-9 pp 1461ndash1463 2005

[23] B Karki B P Lamsal S Jung et al ldquoEnhancing protein andsugar release from defatted soy flakes using ultrasound tech-nologyrdquo Journal of Food Engineering vol 96 no 2 pp 270ndash2782010

[24] F Adam M Abert-Vian G Peltier and F Chemat ldquolsquoSolvent-freersquo ultrasound-assisted extraction of lipids from freshmicroal-gae cells a green clean and scalable processrdquo BioresourceTechnology vol 114 pp 457ndash465 2012

[25] T Allaf V Tomao K Ruiz and F Chemat ldquoInstant controlledpressure drop technology and ultrasound assisted extraction forsequential extraction of essential oil and antioxidantsrdquo Ultra-sonics Sonochemistry vol 20 no 1 pp 239ndash246 2013

[26] Z S Zhang L J Wang D Li S S Jiao X D Chen and ZH Mao ldquoUltrasound-assisted extraction of oil from flaxseedrdquoSeparation and Purification Technology vol 62 no 1 pp 192ndash198 2008

[27] T Zhang Z Wang and X Chen ldquoUltrasound-associatedextraction of seed oil of Korean pinerdquo Journal of Forest Researchvol 16 no 2 pp 140ndash142 2005

[28] A M Goula ldquoUltrasound-assisted extraction of pomegranateseed oilmdashkinetic modelingrdquo Journal of Food Engineering vol117 no 4 pp 492ndash498 2013

[29] Q Y Zafra-Rojas N S Cruz-Cansino A Quintero-Lira etal ldquoApplication of ultrasound in a closed system optimum

condition for antioxidants extraction of blackberry (Rubusfructicosus) residuesrdquoMolecules vol 21 no 7 p 950 2016

[30] AOAC Official Methods of Analysis AOAC InternationalGaithersburg Md USA 18th edition 2005

[31] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[32] EM Kuskoski A G Asuero AM Troncoso J Mancini-Filhoand R Fett ldquoAplicacion de diversos metodos quımicos paradeterminar actividad antioxidante en pulpa de frutosrdquo Cienciae Tecnologia de Alimentos vol 25 no 4 pp 726ndash732 2005

[33] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[34] Y Tian Z Xu B Zheng and Y Martin Lo ldquoOptimization ofultrasonic-assisted extraction of pomegranate (Punica grana-tum L) seed oilrdquo Ultrasonics Sonochemistry vol 20 no 1 pp202ndash208 2013

[35] M L Agudo ldquoTecnicas para la determinacion de compuestosantioxidantes en alimentosrdquo 2010 httpwwwanpebadajozesautodidactaautodidacta archivosnumero 9 archivosl amedinapdf

[36] S K Ho C P Tan Y Y Thoo F Abas and C W HoldquoUltrasound-assisted extraction of antioxidants inMisai Kucing(Orthosiphon stamineus)rdquo Molecules vol 19 no 8 pp 12640ndash12659 2014

[37] S R Kirk R Sawyer and H Egan ldquoMetodos quımicos gen-eralesrdquo inComposicion y Analisis de Alimentos pp 25ndash29 Com-panıa editorial continental Ciudad de Mexico Mexico 2002

[38] S Vazquez S OrsquoNeill and M Legnani ldquoImportancia de loscoliformes en los alimentosrdquo 2013 httpwwwmontevideogubuysitesdefaultfilesimportancia de los coliformes en losalimentospdf

[39] C A Gomez-Alvarez A L Leal-Castro M J Perez de Gonza-lez and M L Navarrete-Jimenez ldquoMecanismos de resistenciaen Pseudomonas aeruginosa entendiendo a un peligroso ene-migordquo Revista de la Facultad de Medicina de la UniversidadNacional de Colombia vol 53 no 1 pp 27ndash34 2005

[40] S D Kominos C E Copeland B Grosiak and B Postic ldquoIntro-duction of Pseudomonas aeruginosa in to a hospital via vegeta-blesrdquo Applied Microbiology vol 24 no 4 pp 567ndash570 1972

[41] NOM Norma Oficial Mexicana NOM-210-SSA1-2014 Pro-ductos y servicios Metodos de prueba microbiologicosDeterminacion de microorganismos indicadores Determina-cion de microorganismos patogenos 2014 httpdofgobmxnota detallephpcodigo=539868ampfecha=26062015

[42] F Reyes-Jurado E Palou and A Lopez-Malo ldquoMetodos deevaluacion de la actividad antimicrobiana y de determinacionde los componentes quımicas de los aceites esencialesrdquo TemasSelectos de Ingenierıa de Alimentos vol 8 pp 68ndash78 2014

[43] D Zekaria ldquoLos aceites esenciales una alternativa a los antimi-crobianosrdquo 2015 httpwwwwpsa-aecaesaeca imgs docswpsa1182855355apdf

[44] DM Livermore ldquoMultiplemechanisms of antimicrobial resist-ance in Pseudomonas aeruginosa our worst nightmarerdquo Clini-cal Infectious Diseases vol 34 no 5 pp 634ndash640 2002

[45] M Viuda-Martos M A Mohamady J Fernandez-Lopez et alldquoIn vitro antioxidant and antibacterial activities of essentials oilsobtained from Egyptian aromatic plantsrdquo Food Control vol 22no 11 pp 1715ndash1722 2011

Journal of Food Quality 9

[46] X Feas L M Estevinho C Salinero et al ldquoTriacylglyc-eride antioxidant and antimicrobial features of virgin camelliaoleiferaC reticulata andC sasanqua oilsrdquoMolecules vol 18 no4 pp 4573ndash4587 2013

[47] R G Earnshaw ldquoUltrasound a new opportunity for foodpreservationrdquo in Ultrasound in Food Processing M J W PoveyandT JMason Eds pp 183ndash192 Editorial BlackAcademic andProfessional New York NY USA 1998

[48] M Vinatoru ldquoAn overview of the ultrasonically assisted extrac-tion of bioactive principles from herbsrdquo Ultrasonics Sonochem-istry vol 8 no 3 pp 303ndash313 2001

Research ArticleAntioxidant and Antimicrobial Properties of CactusPear (Opuntia) Seed Oils

Esther Ramiacuterez-Moreno1 Raquel Carintildeo-Corteacutes2 Nelly del Socorro Cruz-Cansino1

Luis Delgado-Olivares1 Joseacute Alberto Ariza-Ortega1 Vanessa Yelina Montantildeez-Izquierdo3

Mariacutea Manuela Hernaacutendez-Herrero3 and Tomaacutes Filardo-Kerstupp4

1Academic Area of Nutrition Health Sciences Institute Autonomous University of Hidalgo State 42160 Pachuca HGO Mexico2Academic Area of Medicine Autonomous University of Hidalgo State Eliseo Ramırez Ulloa 400 42090 Pachuca HGO Mexico3Department of Food Hygiene Faculty of Veterinary Autonomous University of Barcelona 08193 Bellaterra Spain4Academic Area of Chemistry Basic Science and Engineering Institute Autonomous University of Hidalgo StateCarretera Pachuca-Tulancingo Km 45 Mineral de la Reforma 42183 Pachuca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 23 January 2017 Accepted 5 April 2017 Published 26 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Esther Ramırez-Moreno et alThis is an open access article distributed under the Creative CommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Seed oils from two Mexican varieties of cactus pear (green Opuntia albicarpa and red Opuntia ficus indica) were extracted withdifferent solvents (hexane ethanol and ethyl acetate) to evaluate their antioxidant activity The seed oil with higher antioxidantactivitywas selected to evaluate antimicrobial activityThe fatty acid profilewas analyzed by gas chromatography-mass spectrometry(GC-MS) Oil from green cactus pear seeds obtained with ethanol and ethyl acetate exhibited higher antioxidant activity (119901 lt 005)of 323 and 316 120583mol TE20mg (p lt 005) respectively compared to red cactus pear seed oil (asymp274 and 247 120583mol TE20mgwith ethyl acetate and ethanol resp) The oil obtained with ethanol and higher antioxidant activity was used to determine theantimicrobial activity Both cactus pear oils produced a microbial inhibition zone in most of the microorganisms evaluatedparticularly Saccharomyces cerevisiae which had similar diameter (38ndash40mm) The oil fatty acids profiles of both varieties weresimilar and exhibited a high content of linoleic acid while two fatty acids (linolenic and behenic) found in red cactus pear were notobserved in the green variety

1 Introduction

A relatively untapped source of lipid and protein rawmaterialis the by-product of fruit-processing plants Millions ofpounds of fruit seeds are discarded yearly causing disposalproblems while proper utilization of these waste productscould lead to an important new source of oil and meal [1]Seeds of fruits collect at least some cytoplasmic lipid bodies asmajor storage reserve for lipid accumulation [2] Fruit seedsoils are of great interest because they are edible oils with highdegree of unsaturation antioxidant radical scavenging prop-erties [3ndash8] and a broad spectrum of antimicrobial activity[9ndash15] Therefore the oil from plants can be potentially usedby the food industry for the manufacturing of ldquonaturalrdquo orldquogreenrdquo safe foods [16] and extend shelf-life [17 18]

The oil from cactus pear seed has been found to havean appreciable amount of oil with high levels of unsaturatedfatty acids [19] with antioxidant [20 21] and antimicrobialactivity [22] as well as cardioprotective antithrombotic anti-inflammatory antiarrhythmic hypolipidemic and antihy-perglycemic effect [23 24] These properties are of interestfor the pharmaceutical and food industry However theconcentration and effectiveness of these oils may vary amongcultivars or varieties crop environmental factors (eg lighttemperature and type of soil nutrients) or methods andsolvents used for their extraction Therefore the purpose ofthis research was to determine the antioxidant and antimi-crobial activity and fatty acid profile of the oil obtained fromtwo Mexican varieties of cactus pear (Opuntia albicarpa andOpuntia ficus indica) seeds extracted with different solvents

HindawiJournal of Food QualityVolume 2017 Article ID 3075907 8 pageshttpsdoiorg10115520173075907

2 Journal of Food Quality

2 Materials and Methods

21 Plant Material Two Mexican varieties of cactus pear(Opuntia albicarpa and Opuntia ficus indica) fruit green (cvReyna) and red (cv Rojo Pelon) respectively were providedby theMexican association CoMeNTuna (ConsejoMexicanodel Nopal y la Tuna AC Actopan Hidalgo Mexico) Fruitsfree of external injuries were selected washed and manuallypeeled Cactus pear seeds were obtained after juice wasextracted stirring the pulpwith an industrial blender (38BL52LBC10 Waring Comercial USA) and passing it through aconventional strainer The seeds retained were washed in thestrainer with water until pulp residues were removed

22 Powder Seed and Oil Extraction Green cactus pear seeds(GCPS) and red cactus pear seeds (RCPS)were sun-dried andthen grounded (Cyclotec 1093 Tecator Sweden) to a 1mmdiameter mesh and stored at minus32∘C until further analysisTheseed oil was extracted as follows 25 g of powdered seeds wasmixed with 500mL of solvents with varying polarities (hex-ane ethanol and ethyl acetate) and the obtained residue wasreextracted until extraction solvents become colourless Allthe extracts were filtered through filtration paper Whatmannumber 1 and the filtered extracts were collected for furtherdrying and removal of the remaining solvent at 50∘C using arotary evaporator (BUCHI R-200 Switzerland) All extractswere placed in plastic bottles and then stored at minus20∘C untilused The oils obtained were used to further analysis

23 Free Radical Scavenging Assay The free radical scaven-ging activity was measured using 11-diphenyl-2-picrylhy-drazyl (DPPH∙) radical as described byMorales and Jimenez-Perez [25] A volume of 500 120583L of ethanolic DPPH∙ solution(74mg100mL) was added to a sample aliquot of 100 120583Lplaced in vialsThemixturewas left to sit at room temperaturefor 1 h and then was vortexed and centrifuged at 3000 rpm for10 minutesThe absorbance of the supernatant was measuredat 520 nm in amicroplate reader (PowerWave XSUV-Bioteksoftware KC Junior USA) and 120583mol of Trolox equivalentsper 20 milligram (120583mol TE20mg) of sample was obtainedOil samples with best antioxidant capacity obtained from thedifferent solvents were used for the antimicrobial analysis

24 Antimicrobial Activity Eight standard freeze-dried cul-tures of bacteria Candida albicans (ATCC 10231) Escherichiacoli O58H21 (ATCC 10536) Escherichia coli O157H7(CCUG 44857) Staphylococcus aureus (ATCC 13565) Liste-ria monocytogenes (CCUG 15526) Pseudomonas aeruginosa(ATCC 15442) Saccharomyces cerevisiae (CECT 1942) andSalmonella Typhi (CCUG 29478) were obtained in ther-mosealed vials from the Spanish Type Culture Collection(Autonomous University of Barcelona Barcelona Spain)Freeze-dried cultures were rehydrated in tryptone soy brothat 37∘C for 18 h and then were used to inoculate tryptone soyagar and malt extract agar plates all microorganisms wereincubated at 37∘CexceptCandida albicans and Saccharomycescerevisiae which were incubated at 25∘C Individual colonies

were maintained on specific agar slants stored at 4∘C andsubcultured every 15 days

Disc Diffusion Assay Antimicrobial activity of oil extractedfromGCPS andRCPSwas carried out using the disc diffusionmethod [26] Petri plates were filled with sim20mL of steriletryptone soy agar for bacteria and malt extract agar for fungiThe test cultures were swabbed on the top of the solidifiedmedia and allowed to dry for 10 minutes Serial dilutions(10ndash50 120583gmL) of the seed oil from a stock solution (1mgmL)were prepared in 20 DMSO and 10 120583L loaded onto thesterile blank discs (BBL Sensi-Disc) of 6 millimetersof diameter On the media surface the loaded disks wereplaced and left for 30 minutes at room temperature toallow compound diffusion The seed oil was serially dilutedin MuellerndashHinton broth medium and duplicate tubes ofeach dilution (10ndash100 120583gmL) were inoculated with 5 times106 cells of the test bacteria strain and culturesThe antibioticagents Sensi-Disc streptomycin ampicillin and sulfamethox-azoletrimethoprim (BBL Sensi-Disc) were used as positivecontrols at the same concentration level After plates wereincubated at 37∘C for 24 h the diameters of the inhibitionzones were recorded in millimeters Three independentrepetitions were performed and tests were made in triplicate

25 GC-MS Analysis The GC-MS analysis was performedwith a GC-MS HP-5890 (Hewlett-Packard Company PaloAlto California USA) equipped with a Flame IonizationDetector (FID) and a ZB-WAX fused silica capillary column(60m times 025mm id times 025mm film thickness) packedwith 5 phenylmethylpolysiloxane (Phenomenex TorranceCA) To obtain the methyl esters the cactus pear seed oilswere saponified and derivatized using KOH 1N (IUPAC1969) Changes in the fatty acids of the oils samples werecompared against a standard mixture of 37 components offatty acids methyl esters (FAMEs) (Food Industry FAMEsMix Restek) comprised by methyl esters with chains C40C60 C80 C100 C110 C120 C130 C140 C141 C150C151 C160 C161 C170 C171 C180 C181n9c C181n9tC182n6c C182n6t C183n6 C183n3 C200 C201n9 C202C203n6 C203n3 C204n6 C205n3 C210 C220 C221n9C222 C226n3 C230 C240 and C241n9 The samplevolume injected was of 2 120583L (split ratio 20 2) at an injectorand detector temperatures of 225 and 225∘C respectively N2was used as carrier gas at a flow rate of 12mLsdotminminus1 Fattyacids were calculated as percentage of total FAMEs

26 Statistical Analysis All values were obtained by triplicateand expressed as means plusmn standard deviations (SD) Datawere analyzed using the SPSS V15 software (SPSS InstituteInc Cary NC) An ANOVA was carried out to determinedifferences between oils extracted as well as its antimicrobialactivity that were significant at the 5 level of probability anda Tukey test was used for comparison of data

3 Results and Discussion

31 Yield Comparison between Extraction Solvents Hexaneethanol and ethyl acetate were used to extract the oil from

Journal of Food Quality 3

1183

669

1013

511

106

381

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

2

4

6

8

10

12

14

Oil

yiel

d (

)

Figure 1 Oil yields () extracted from GCPS and RCPS withhexane ethanol and ethyl acetate

cactus pear seeds The extraction yields are compared inFigure 1 which shows that the higher amount of oil () wasobtained from the green cultivar and that yield depended onthe solvent used Oil extraction with hexane was higher forboth fruit varieties (1183 for GCPS and 689 for RCPS)followed by ethanol which reached the same yield as ethylacetate for GCPS (asymp10) Ethyl acetate was the least effectivesolvent for RCPS The extraction yields were similar to thosereported (asymp7 to 11) for several varieties of Opuntia ficusindica [27ndash29] This extraction yields will vary depending onseveral factors as fruit variety harvest period maturationgeographic region percentage of oil in the seed and chemicalcompounds found in the source and by the extractionmethod[30] Researchers have determined that solvent extractioncombinedwith othermethods could increase oil yield as highpressure or supercritical fluid combined with solvent reacheda yield of 933 from tobacco seeds (Nicotiana tabacum L)while sonication and Soxhlet reached a 775 and 1372respectively [31]

32 Free Radical Scavenging Activity Solvent extraction isusually used for isolation of antioxidants the extractiondepends on the solvent selected based on the different antiox-idant compounds with varying polarity [32 33] DPPH is astable free radical that accepts an electron or hydrogen radicalto become a stable diamagnetic molecule [34 35]The DPPHassay has also been used to predict the oxidative stability ofedible oils [36 37] The antioxidant activity determined byDPPH of the oil extracted from RCPS and GCPS is shownin Figure 2 Oil from the GCPS extracted with ethanol andethyl acetate exhibited the higher antioxidant activity (119901 lt005) of 323 and 316 120583mol TE20mg extract respectivelyfollowed by RCPS oil extracted with ethyl acetate (274120583molTE20mg extract) and ethanol (247 120583mol TE20mg extract)These results demonstrate that the extraction solvent hada significant effect on the free radical scavenging capacityof the oil where the hexane had the lower values In ourstudy the green variety exhibited a higher antioxidant activityregardless of solvent Different results may depend mainly

e

d

a

c

ab

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

50

100

150

200

250

300

350

휇m

ol T

E20

mg

extr

act

Figure 2 Antioxidant activity of GCPS and RCPS oils extractedwith different solvents andashdDifferent letters above bars indicate thatsamples are significantly different (119901 lt 005)

on the content and concentration of bioactive compounds inthe oil but other factors such as solvent polarity solubilityof the extracts in different testing systems stereoselectivityof the radicals [38] and strong synergism between fattyacids [6] may affect antioxidant activities Other studies havealso reported diverse antioxidant activity among oils fromdifferent Opuntia varieties [20 39 40]

33 Antibacterial and Antifungal Activity The most recom-mended way to prevent or inhibit microbial growth in foodsis the use of food preservatives Essential oils are secondarymetabolites of plants that have wide applications in thefood flavoring and preservative industry [41] Six differentbacterium and two fungi species were used to screen theantimicrobial potential of the oils extracted from the twovarieties of cactus pear seeds Oil extracted with ethanolexhibited the highest antioxidant activity and therefore itwas used to evaluate the antibacterial and antifungal activityFigure 3 shows the results from the microbial assay wheremost microorganisms showed an inhibition zone whenexposed to GCPS and RCPS oils except Salmonella Typhiand Escherichia coli O157H7 (image not shown) From thesetwo microorganisms the first showed an inhibition zonein the presence of antibiotic agents streptomycin (S) ampi-cillin (AMP) and sulfamethoxazoletrimethoprim (STX) indiameters of 146 113 and 273mm respectively (Table 1)while Escherichia coli O157H7 was only inhibited by SXT(253mm) which agrees with other reports of multiantibi-otic resistance of E coli O157H7 due to the presence ofthe gene cluster AMR-SSuT [42] and production of beta-lactamase [43] On the other hand Saccharomyces cerevisiaewas highly inhibited (38ndash40mm) by the extracted oils butgrew in presence of the antimicrobial agents (Figure 3)Similar results were observed for Candida albicans althoughinhibition zones were smaller and similar for both oilsThese observations demonstrate that certain compounds inthe cactus pear seed oil have antimicrobial activity Otherresearchers also reported similar observations for cactus

4 Journal of Food Quality

Table 1 Diameters of growth inhibition zones (mm) in the presence of oil extracted from cactus pear seeds and conventional antimicrobialsA

Microbial cultures Extract Antimicrobial agentGCPS RCPS S AMP SXT

Saccharomyces cerevisiae (CECT1942) 383 plusmn 42a 403 plusmn 45a ND ND NDEscherichia coli O58H21 (ATCC 10536) 119 plusmn 07d 114 plusmn 09d 195 plusmn 14b 178 plusmn 15c 299 plusmn 09a

Escherichia coli O157H7 (CCUG 44857) NDB ND ND ND 253 plusmn 10Staphylococcus aureus (ATCC 13565) 121 plusmn 10c 111 plusmn 11c 183 plusmn 09b 281 plusmn 15a 333 plusmn 19a

Listeria monocytogenes (CCUG15526) 133 plusmn 15c 114 plusmn 09d 213 plusmn 12a 173 plusmn 08c 376 plusmn 18a

Pseudomonas aeruginosa (ATCC15442) 164 plusmn 21c 151 plusmn 20c 201 plusmn 15b 241 plusmn 25a 366 plusmn 29a

Salmonella typhi (CCUG29478) ND ND 146 plusmn 04b 113 plusmn 18c 273 plusmn 08a

Candida albicans (ATCC 10231) 111 plusmn 10a 110 plusmn 18a ND ND NDAInhibition zone diameters for oil and reference antibiotics are means plusmn SE of three replicas GCPS green cactus pear seed oil extract RCPS red cactus pearseed oil extract S streptomycin (10120583gdisc) AMP ampicillin (10 120583gdisc) and SXT sulfamethoxazoletrimethoprim (10120583gdisc) BND not detected activityandashdDifferent letters in the same row indicate significant differences

RG

SXT

S

AMP

(a)

RG

SXT

S

AMP

(b)

R G

SXTS

AMP

(c)

RG

SXTS

AMP

(d)

RG

SXT

S

AMP

(e)

R G

SXT

S

AMP

(f)

Figure 3 Antimicrobial activity of oil extracted from green cactus pear (G) oil extracted from red cactus pear seeds (R) streptomycin(S) ampicillin (AMP) and sulfamethoxazoletrimethoprim (SXT) Candida albicans (ATCC 10231) (a) Escherichia coli O58H21 (ATCC10536) (b) Staphylococcus aureus (ATCC 13565) (c) Listeria monocytogenes (CCUG15526) (d) Pseudomonas aeruginosa (ATCC15442) (e)Saccharomyces cerevisiae (CECT1942) (f)

pear fruit cv Opuntia stricta [44] and for other plants asfennel (Foeniculum vulgare L) and chamomile (Matricariachamomilla L) [5] Differences in the levels of antimicrobialactivity may be partially attributed to variable chemicalcomposition of the oils [45] Mnayer et al [46] suggestedthat oil compounds can act on different bacterial structureswhile Gill et al [47] mentioned that whole oils have a greater

antibacterial activity than the major component mixed sothat minor components are critical for the activity and exerta synergistic effect [16 48 49]

In the present study the antimicrobial activity of cactuspear seed oil was more effective against fungi comparedto bacteria cultures These interesting results suggest thatthere is a link between the oil chemical contents and the

Journal of Food Quality 5

Table 2 Percentages of FAMEs in crude cactus pear seed oil extracts

FAMEs Green cactus pear seed oil extract Red cactus pear seed oil extractC140 0078 plusmn 000 0066 plusmn 001C160 12327 plusmn 009 12887 plusmn 002C161 0429 plusmn 002 0570 plusmn 001C162 0073 plusmn 000 0540 plusmn 000C170 0060 plusmn 001 0075 plusmn 000C180 3436 plusmn 001 3389 plusmn 007C181 16215 plusmn 003 17061 plusmn 001C182 67448 plusmn 008 65407 plusmn 001C183 Ni 0372 plusmn 001C220 Ni 0160 plusmn 001Means of 3 replicates plusmn SE Ni not identified

140

160

181

182

18017

016

116

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(a)14

0 161

162

170

180

181

182

183

220

160

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(b)

Figure 4 Chromatograms of FAMEs of cactus pear seed oil extract (a) Green cactus pear seed oil extract (b) red cactus pear seed oil extractIn both oils extracts were identified myristic (C140) palmitic (C160) palmitoleic (C161 cis-9) hexadecadienoic (C162 cis-9 12) margaric(C170) stearic (C180) oleic (C181 cis-9) linoleic (C182 cis-9 12) except linolenic (C183 cis-6 9 12) and behenic (C220) fatty acids thatwere identified only in red cactus pear seed

antimicrobial activity The membrane disruption could beone mechanism of action by inactivating microbial adhesionenzymes and proteins transport [15 46] RCPS and GCPSextracts inhibited most of the evaluated bacterial and fungispecies (Table 1) however antimicrobial activity was notdetected for Salmonella Typhi which is a gram-negative bac-terium In general gram-negative bacteria have an effectiveoutermembrane that restricts the penetration of amphipathiccompounds and has a mechanism to extrude toxins across[50]Thismay explain the apparent antimicrobial ineffective-ness of the oils against the permeability barrier in addition tothe presence of multidrug resistance encoding plasmids [51]

34 Fatty Acid Profile FAMEs chromatograms and percent-ages are shown in Figure 4 and Table 2 Cactus pear seed oilscontained saturated and unsaturated fatty acids the linoleicfatty acid being the predominant (674 and 654 in GCPSand RCPS oils resp) Minimal amounts of myristic (C140)palmitoleic (C161) hexadecadienoic (C162) and margaric(C170) fatty acids in both oils were also identified The fattyacids profiles of the two cactus pear varieties were similarhowever theGCPS had a slightly higher content of the linoleicacid (C182)while the fatty acids linolenic (C183) and behenic(C220) were in minimal amounts only in the RCPS

Different studies have established that factors as cultivartype temperature and harvest time have a strong influence inparameter as pH Brix vitamin C sugars and fat content [5253] Oumato et al [52] found differences in linoleic fatty acid(C182) content among cactus pear cultivars In other studythe oleic acid (C181) content was significantly influenced bythe cultivar and location interaction [53] providing uniquecharacteristics to the oil

In comparison with other plants oils the linoleic acid(C182) content of the cactus pear fruit was similar to thelevels reported for sunflower oil (62) [54] and higher thanwheat germ oil (5505) [55] and soybean oil (5270)[56] The contents of other FAMEs in cactus pear varietiessuch as palmitic (C160) oleic (C181) and stearic (C180)were similar to those reported for Castilla blackberry (Rubusglaucus Benth) with 1124 passion fruit (Passiflora edulis)with 1547 [57] and grape (Vitis vinifera) with 35 [58]

Other researchers have reported similar fatty acidsprofile to our findings for different plant materials andhave analyzed the antimicrobial effectiveness against dif-ferent microorganisms For instance fatty acids found inAllium cepa were found to effectively inhibit Staphylococcusaureus Bacillus subtilis Enterococcus faecalis Escherichia coliand Klebsiella pneumoniae [59] Oil extracted from SwieteniaMacrophylla king seed oil inhibited growth of S aureus

6 Journal of Food Quality

S Typhimurium and P aeruginosa [60] These studies de-monstrate that seed oil can inhibit fungi and bacteria buttheir efficacy would depend on their concentration levels andspecific pathogen [15]

4 Conclusions

Oil yield from the green cactus pearwas higher in comparisonto the red cultivar andwas also influenced by the solvent usedHexane exhibited high extraction yield while oils extractedwith ethanol had the better antioxidant activity The resultsdemonstrated that oil extracts from both varieties have anoticeable antimicrobial activity against gram-positive andgram-negative bacteria comparable to antimicrobial com-pounds such as ampicillin streptomycin and sulfamethoxa-zoletrimethoprimThis research provides further incentivesto develop additives for the food cosmetic and pharmaceu-tical sectors seeking natural compounds with antimicrobialactivity Further studies are needed to determine the specificcomponent responsible for the antimicrobial activity in cac-tus pear seeds oil and determine the optimum levels of oilextract and the antimicrobial effectiveness in the foodmatrix

Additional Points

Practical Application Our results suggest that the oilsextracted from cactus pear seeds have the potential to be usedas a natural antioxidant and antimicrobial agents by the foodcosmetic and pharmaceutical sectors

Conflicts of Interest

The authors have declared that no conflicts of interest exist

Acknowledgments

This study was possible thanks to the financial supportfrom the Programa Integral de Fortalecimiento Institucional(PIFI 2013ndash2015) Mexico This research project was partiallysupported by the Food Hygiene Department Faculty ofVeterinary from the Autonomous University of BarcelonaSpain The authors acknowledge the Mexican associationCoMeNTuna (Consejo Mexicano del Nopal y la TunaHidalgo Mexico) for providing the plant materials

References

[1] B S Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Acids in Foods and Their Health Implications pp 263ndash301 CRC Press 3rd edition 2007

[2] D J Murphy I Hernandez-Pinzon and K Patel ldquoRole oflipid bodies and lipid-body proteins in seeds and other tissuesrdquoJournal of Plant Physiology vol 158 no 4 pp 471ndash478 2001

[3] A Kedia B Prakash P KMishra andN K Dubey ldquoAntifungaland antiaflatoxigenic properties of Cuminum cyminum (L)seed essential oil and its efficacy as a preservative in storedcommoditiesrdquo International Journal of Food Microbiology vol168-169 pp 1ndash7 2014

[4] S Singh S S Das G Singh C SchuffM P de Lampasona andC A Catalan ldquoComposition in vitro antioxidant and antimi-crobial activities of essential oil and oleoresins obtained fromblack cumin seeds (Nigella sativa L)rdquo BioMed Research Inter-national vol 2014 Article ID 918209 10 pages 2014

[5] M H H Roby M A Sarhan K A-H Selim and K I KhalelldquoAntioxidant and antimicrobial activities of essential oil andextracts of fennel (Foeniculum vulgare L) and chamomile(Matricaria chamomilla L)rdquo Industrial Crops and Products vol44 pp 437ndash445 2013

[6] G Kavoosi A Tafsiry A A Ebdam and V Rowshan ldquoEvalua-tion of antioxidant and antimicrobial activities of essential oilsfrom carum copticum seed and ferula assafoetida latexrdquo Journalof Food Science vol 78 no 2 pp T356ndashT361 2013

[7] S Lalas O Gortzi V Athanasiadis J Tsaknis and I ChinouldquoDetermination of antimicrobial activity and resistance tooxidation of Moringa peregrina seed oilrdquoMolecules vol 17 no3 pp 2330ndash2334 2012

[8] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extract of Laurus nobilis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

[9] R S Bhat and S Al-daihan ldquoAntimicrobial activity of Litchichinensis and Nephelium lappaceum aqueous seed extractsagainst some pathogenic bacterial strainsrdquo Journal of King SaudUniversitymdashScience vol 26 no 1 pp 79ndash82 2014

[10] J M Silvan E Mingo M Hidalgo S de Pascual-Teresa A VCarrascosa and A J Martinez-Rodriguez ldquoAntibacterial activ-ity of a grape seed extract and its fractions against Campylobac-ter spprdquo Food Control vol 29 no 1 pp 25ndash31 2013

[11] K Rakholiya M Kaneria D Desai and S Chanda ldquoAntimi-crobial activity of decoction extracts of residual parts (seedand peels) ofMangifera indica L var Kesar against pathogenicand food spoilage microorganismrdquo in Microbial pathogens andstrategies for combating them science technology and educationA Mendez-Vilas Ed vol 2 pp 850ndash856 2013

[12] N A Hasan M Z Nawahwi and H Ab Malek ldquoAntimicrobialactivity ofNigella sativa seed extractrdquo Sains Malaysiana vol 42no 2 pp 143ndash147 2013

[13] Z I Sajid F Anwar G Shabir G Rasul KM Alkharfy and A-H Gilani ldquoAntioxidant antimicrobial properties and phenolicsof different solvent extracts from bark leaves and seeds ofPongamia pinnata (L) pierrerdquoMolecules vol 17 no 4 pp 3917ndash3932 2012

[14] M Khoobchandani B K Ojeswi N Ganesh et al ldquoAntimicro-bial properties and analytical profile of traditional Eruca sativaseed oil comparisonwith various aerial and root plant extractsrdquoFood Chemistry vol 120 no 1 pp 217ndash224 2010

[15] V Kesari A Das and L Rangan ldquoPhysico-chemical charac-terization and antimicrobial activity from seed oil of Pongamiapinnata a potential biofuel croprdquo Biomass and Bioenergy vol34 no 1 pp 108ndash115 2010

[16] K Carovic-Stanko S Orlic O Politeo et al ldquoComposition andantibacterial activities of essential oils of seven Ocimum taxardquoFood Chemistry vol 119 no 1 pp 196ndash201 2010

[17] MM Tajkarimi S A Ibrahim andDO Cliver ldquoAntimicrobialherb and spice compounds in foodrdquo Food Control vol 21 no 9pp 1199ndash1218 2010

[18] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

Journal of Food Quality 7

[19] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[20] W Liu Y-J Fu Y-G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[21] B Matthaus and M M Ozcan ldquoHabitat effects on yield fattyacid composition and tocopherol contents of prickly pear(Opuntia ficus-indica L) seed oilsrdquo Scientia Horticulturae vol131 pp 95ndash98 2011

[22] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research vol 27 no 14 pp 1305ndash1314 2013

[23] KMobraten TMHaug C R Kleiveland and T Lea ldquoOmega-3 and omega-6 PUFAs induce the same GPR120-mediatedsignalling events but with different kinetics and intensity inCaco-2 cellsrdquo Lipids in Health and Disease vol 12 no 1 ArticleID 101 2013

[24] A BerraaouanA ZiyyatHMekhfi et al ldquoEvaluation of antidi-abetic properties of cactus pear seed oil in ratsrdquo PharmaceuticalBiology vol 52 no 10 pp 1286ndash1290 2014

[25] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[26] P R Murray E J Baron M A Pfaller F C Tenover and R HYolkeManual of Clinical Microbiology 1995 Washington DCUSA

[27] M Ennouri H Fetoui E Bourret N Zeghal and H AttialdquoEvaluation of some biological parameters of Opuntia ficusindica 1 Influence of a seed oil supplemented diet on ratsrdquoBioresource Technology vol 97 no 12 pp 1382ndash1386 2006

[28] Y Habibi L Heux M Mahrouz and M R Vignon ldquoMorpho-logical and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruitsrdquo Carbohydrate Polymers vol 72 no 1pp 102ndash112 2008

[29] MMoudenM Boujnah S Salmaoui S Zantar and A DouiraldquoEffect of two extraction methods and harvest period andperformance there statement of fatty oils of figs pear seedrdquoInternational Journal of Pure amp Applied Bioscience vol 4 no1 pp 1ndash8 2016

[30] A El Finti M Belayadi R El Boullani F Msanda and A ElMousadik ldquoAssessment of some agro-technological parametersof cactus pear fruit (Opuntia ficus-indica Mill) in Moroccocultivarsrdquo Journal of Medicinal Plants Research no 7 pp 2574ndash2583 2013

[31] S Majdi M Barzegar A Jabbari and M Agha AlikhanildquoSupercritical fluid extraction of tobacco seed oil and itscomparison with solvent extraction methodsrdquo Journal of Agri-cultural Science and Technology vol 14 no 5 pp 1043ndash10512012

[32] E M Marinova and N V Yanishlieva ldquoAntioxidative activity ofextracts from selected species of the family Lamiaceae insunflower oilrdquo Food Chemistry vol 58 no 3 pp 245ndash248 1997

[33] Y-Y Soong and P J Barlow ldquoAntioxidant activity and phenoliccontent of selected fruit seedsrdquo Food Chemistry vol 88 no 3pp 411ndash417 2004

[34] J R Soares T C P Dinis A P Cunha and L M AlmeidaldquoAntioxidant activities of some extracts of Thymus zygisrdquo FreeRadical Research vol 26 no 5 pp 469ndash478 1997

[35] I GulcinMOktay E Kirecci and O I Kufrevioglu ldquoScreeningof antioxidant and antimicrobial activities of anise (Pimpinellaanisum L) seed extractsrdquo Food Chemistry vol 83 pp 371ndash3822003

[36] J Lee H Chung P-S Chang and J Lee ldquoDevelopment of amethod predicting the oxidative stability of edible oils using 22-diphenyl-1-picrylhydrazyl (DPPH)rdquo Food Chemistry vol 103no 2 pp 662ndash669 2007

[37] A Fazio P Plastina J Meijerink R F Witkamp and BGabriele ldquoComparative analyses of seeds of wild fruits ofRubus and Sambucus species from Southern Italy fatty acidcomposition of the oil total phenolic content antioxidant andanti-inflammatory properties of the methanolic extractsrdquo FoodChemistry vol 140 no 4 pp 817ndash824 2013

[38] R L Prior X Wu and K Schaich ldquoStandardized methods forthe determination of antioxidant capacity and phenolics infoods and dietary supplementsrdquo Journal of Agricultural andFood Chemistry vol 53 no 10 pp 4290ndash4302 2005

[39] A Cardador-Martınez C Jimenez-Martınez and G SandovalldquoRevalorization of cactus pear (Opuntia spp) wastes as a sourceof antioxidantsrdquo Ciencia e Tecnologia de Alimentos vol 31 no3 pp 782ndash788 2011

[40] Z Ghazi M Ramdani M Tahri et al ldquoChemical compositionand antioxidant activity of seeds oils and fruit juicerdquo Journalof Materials and Environmental Science vol 6 no 8 pp 2338ndash2345 2015

[41] V K Bajpai K-H Baek and S C Kang ldquoControl of Salmonellain foods by using essential oils a reviewrdquo Food ResearchInternational vol 45 no 2 pp 722ndash734 2012

[42] K Ziebell R P Johnson A M Kropinski et al ldquoGenecluster conferring streptomycin sulfonamide and tetracyclineresistance in Escherichia coli O157H7 phage types 23 45 and67rdquo Applied and Environmental Microbiology vol 77 no 5 pp1900ndash1903 2011

[43] O Chandra K J Putra and I Wayan ldquoAntibiotic resistanceprofiles of Escherichia coli O157H7 in cattle at Suth-KutaBadung Regency Bali Indonesiardquo Global Veterinaria vol 15no 5 pp 480ndash484 2015

[44] E Moosazadeh M R Akhgar and A Kariminik ldquoChemicalcomposition and antimicrobial activity of Opuntia stricta Fessential oilrdquo Journal of Biodiversity and Environmental Sciencesvol 4 pp 94ndash101 2014

[45] S Burt ldquoEssential oils their antibacterial properties and poten-tial applications in foods - a reviewrdquo International Journal ofFood Microbiology vol 94 no 3 pp 223ndash253 2004

[46] D Mnayer A-S Fabiano-Tixier E Petitcolas et al ldquoChemicalcomposition antibacterial and antioxidant activities of sixessentials oils from the Alliaceae familyrdquo Molecules vol 19 no12 pp 20034ndash20053 2014

[47] A O Gill P Delaquis P Russo and R A Holley ldquoEvaluationof antilisterial action of cilantro oil on vacuum packed hamrdquoInternational Journal of FoodMicrobiology vol 73 no 1 pp 83ndash92 2002

[48] M Turgis K D Vu C Dupont and M Lacroix ldquoCombinedantimicrobial effect of essential oils and bacteriocins againstfoodborne pathogens and food spoilage bacteriardquoFoodResearchInternational vol 48 no 2 pp 696ndash702 2012

[49] H Zengin and A H Baysal ldquoAntibacterial and antioxi-dant activity of essential oil terpenes against pathogenic andspoilage-forming bacteria and cell structure-activity relation-ships evaluated by SEM microscopyrdquo Molecules vol 19 no 11pp 17773ndash17798 2014

8 Journal of Food Quality

[50] G Tegos F R Stermitz O Lomovskaya and K Lewis ldquoMul-tidrug pump inhibitors uncover remarkable activity of plantantimicrobialsrdquo Antimicrobial Agents and Chemotherapy vol46 no 10 pp 3133ndash3141 2002

[51] M Baltazar A Ngandjio K E Holt et al ldquoMultidrug-resistantSalmonella enterica serotype typhi Gulf of Guinea RegionAfricardquo Emerging Infectious Diseases vol 21 no 4 pp 655ndash6592015

[52] J Oumato S ZriraM Boujnah andB Saidi ldquoEffect ofmaturitystage onmorphological and chemical characteristics ofOpuntiaficus indica from Moroccordquo International Journal of Innovationand Applied Studies vol 20 no 1 pp 400ndash410 2017

[53] M deWit A Hugo N Shongwe and R van derMerwe ldquoEffectof cultivar season and locality on lipid content and fatty acidcomposition of cactus pear seed oilrdquo South African Journal ofPlant and Soil no 33 pp 279ndash288 2016

[54] Australian Oilseeds Federation Incorporated 2015 Section 1ldquoQuality standards technical information amp typical analysisrdquono 14 pp 31ndash40 2016 (Accessed 1 November 2015)

[55] A Awad A Adel A A M Nady and AAE ldquoWheat germ anoverview on nutritional value antioxidant potential andantibacterial characteristicsrdquo Food and Nutrition Sciences vol6 no 2 pp 265ndash277 2015

[56] P Pumrojana S Terapuntuwat and P Pakdee ldquoInfluence offatty acid composition of soybean oil vs beef tallow on egg yolkfatty acid profiles of laying hensrdquo Pakistan Journal of Nutritionvol 14 no 7 pp 383ndash387 2015

[57] A F Ceron M O Osorio and B A Hurtado ldquoIdentificacionde acidos grasos contenidos en los aceites extraıdos a partir desemillas de tres diferentes especies de frutasrdquo Acta Agronomicavol 61 no 2 pp 126ndash132 2012

[58] J Orsavova L Misurcova J Vavra Ambrozova R Vicha andJ Mlcek ldquoFatty acids composition of vegetable oils and itscontribution to dietary energy intake and dependence of car-diovascular mortality on dietary intake of fatty acidsrdquo Interna-tional Journal of Molecular Sciences vol 16 no 6 pp 12871ndash12890 2015

[59] M Derbali A Elaissi I Cheraief and M Aouni ldquoFatty acidcomposition and antimicrobial activity against sensitive andmulti-drug resistant bacteria of Tunisian Allium cepa seedextractrdquo Research amp Reviews Journal of Hospital and ClinicalPharmacy vol 2 no 2 pp 30ndash34 2016

[60] M B Suliman A H Nour M M Yusoff P Kuppusamy A RYuvaraj and S A Mazza ldquoFatty acid composition and antibac-terial activity of Swietenia macrophylla king seed oilrdquo AfricanJournal of Plant Science vol 7 no 7 pp 300ndash303 2013

Page 5: Natural Preservatives to Improve Food Quality and Safety

Editorial Board

Encarna Aguayo SpainRiccarda Antiochia ItalyJorge Barros-Velaacutezquez SpainJoseacute A Beltraacuten SpainAacute A Carbonell-Barrachina SpainMarina Carcea ItalyMaria Rosaria Corbo ItalyEgidio De Benedetto ItalyAlessandra Del Caro ItalyAntimo Di Maro Italy

Rossella Di Monaco ItalyHuumlseyin Erten TurkeySusana Fiszman SpainAndrea Galimberti ItalyEfstathios Giaouris GreeceVicente M Goacutemez-Loacutepez SpainElena Gonzaacutelez-Fandos SpainAlejandro Hernaacutendez SpainJesuacutes Lozano SpainSara Panseri Italy

Mariacutea B Peacuterez-Gago SpainWitoon Prinyawiwatkul USAEduardo Pueacutertolas SpainJuan E Rivera MexicoFlora V Romeo ItalyJordi Rovira SpainAmy Simonne USAGiuseppe Zeppa Italy

Contents

Natural Preservatives to Improve Food Quality and SafetyMoreno Bondi Andrea Laukovaacute Simona de Niederhausern Patrizia Messi and Chrissanthy PapadopoulouVolume 2017 Article ID 1090932 3 pages

Natural Food Additives and Preservatives for Fish-Paste Products A Review of the Past Present andFuture States of ResearchKhawaja Muhammad Imran Bashir Jin-Soo Kim Jeong Hyeon An Jae Hak Sohn and Jae-Suk ChoiVolume 2017 Article ID 9675469 31 pages

Development of a Chemically Defined Medium for Better Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31Wenli Liu Lanwei Zhang and Huaxi YiVolume 2017 Article ID 9017452 8 pages

Lipid Oxidation Color Changes and Microbiological Quality of Frozen Beef Burgers Incorporatedwith ShiraziThyme Cinnamon and Rosemary ExtractsHadi Hashemi Gahruie Seyed Mohammad Hashem HosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan ShadVolume 2017 Article ID 6350156 9 pages

Optimization of Ultrasound Extraction of Cactus Pear (Opuntia ficus indica) Seed Oil Based onAntioxidant Activity and Evaluation of Its Antimicrobial ActivityMariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-Cansino Ernesto Alaniacutes-GarciacuteaLuis Delgado-Olivares Joseacute Alberto Ariza-Ortega Esther Ramiacuterez-Morenoand Joseacute de Jesuacutes Manriacutequez-TorresVolume 2017 Article ID 9315360 9 pages

Antioxidant and Antimicrobial Properties of Cactus Pear (Opuntia) Seed OilsEsther Ramiacuterez-Moreno Raquel Carintildeo-Corteacutes Nelly del Socorro Cruz-Cansino Luis Delgado-OlivaresJoseacute Alberto Ariza-Ortega Vanessa Yelina Montantildeez-Izquierdo Mariacutea Manuela Hernaacutendez-Herreroand Tomaacutes Filardo-KerstuppVolume 2017 Article ID 3075907 8 pages

EditorialNatural Preservatives to Improve Food Quality and Safety

Moreno Bondi1 Andrea Laukovaacute2 Simona de Niederhausern1

Patrizia Messi1 and Chrissanthy Papadopoulou3

1Department of Life Sciences University of Modena and Reggio Emilia Via G Campi 287 Modena Italy2Institute of Animal Physiology Slovak Academy of Sciences Soltesovej 4-6 040 01 Kosice Slovakia3Microbiology Department Faculty of Medicine School of Health Sciences University of Ioannina Ioannina Greece

Correspondence should be addressed to Moreno Bondi morenobondiunimoreit

Received 12 October 2017 Accepted 12 October 2017 Published 12 December 2017

Copyright copy 2017 Moreno Bondi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Food products can be contaminated by a variety of path-ogenic and spoilage microbiota the former causing food-borne diseases and the latter causing significant economiclosses for the food industry due to undesirable effects onthe food properties According to the Centers for DiseaseControl and Prevention (CDC) each year in the UnitedStates 48 million people get sick 128000 are hospitalizedand 3000 die because of foodborne infections Howeveralthough foodborne outbreaks are well recorded sporadiccases are not because not all patients visit the doctor orenter the hospital and the causative agent is not alwaysidentified A considerable number of foodborne pathogens ofgreat public health importance (eg VTEC E coli serotypesCampylobacter jejuni Listeria monocytogenes and Yersiniaenterocolitica) have emerged during the recent two decadescausing severe illness and foodborne outbreaks worldwide

Microbial food spoilage is also an area of immenseconcern for the food industry It is estimated that as much as25 of all food produced is lost after harvest due to microbialactivity While the growth of spoilage microbiota in foodsis not harmful for the human health it has negative impacton the shelf-life textural characteristics and overall qualityof the finished products affects the consumer choices andresults in significant commercial losses Thus prevention orinhibition of microbial growth in foods is of outmost impor-tance for the current globalized food production Hencethere is still the need for new processing methods to be usedeither alone or in combination with the already existing onesable to reduce or eliminate foodborne pathogens and spoilagebacteria

Chemical additives have been extensively used to preventthe survival and proliferation of microorganisms but their

safety and impact on human health are under discussionSince the reduction or elimination of pathogens and spoilagemicroorganisms in food is the foremost priority the currenttrends in food processing are focusing on the use of naturalcompounds which are considered as safe alternatives andsatisfy the consumer preferences for more ldquogreen foodsrdquoHence the increased awareness on the safety of food additivesand preservatives and the consumerrsquos trend to avoid foodscontaining chemicals which in the long-term may haveadverse impact on their health have generated a significantnumber of studies and publications on the potential useof various natural substances recognized as GRAS (Gener-ally Recognized as Safe) to be used as food preservativesChemical compounds added to foods as antioxidant agentsare also of concern particularly when important proteinsources (eg burgers steaks) are involved in the daily diet ofwesternized consumer living in the developed countries [1 2]Synthetic antioxidants such as BHT TBHQ and BHA havedemonstrated various adverse effects on the human healthincluding allergy headache asthma and dermatitis Recentstudies on the utilization of natural antioxidants (eg herbalessential oils and extracts) indicate their capacity and safety[3 4] Also the antimicrobial properties of natural substancessuch as plant essential oils and extracts have been extensivelystudied with promising results [5] The proper recycling anduse of fruit-processing plants by-products like fruit seedsor skins discarded and piling up in huge amounts everyyear are of great interest for the food industry particularlytheir potential to be a useful source of oil and meal [6]Additionally the oil from plant seeds can be used by thefood industry for manufacturing more ldquonaturalrdquo or ldquogreenrdquofoods and also can sufficiently extend the shelf-life of the

HindawiJournal of Food QualityVolume 2017 Article ID 1090932 3 pageshttpsdoiorg10115520171090932

2 Journal of Food Quality

food product [7] The oils derived from fruit seeds oils mayalso have some more useful properties beyond being justldquoediblerdquoThe oil derived from the seed extract of twoMexicanvarieties of cactus pear (Opuntia albicarpa and Opuntia ficusindica) has been found to have sufficient antioxidant andantimicrobial properties [8] Furthermore some biologicalactive compounds produced by microorganisms are widelyused in the food industry as well A good alternative toconventional chemically synthesized food preservatives is theuse of natural antimicrobials such as bacteriocins producedby lactic acid bacteria (LAB) with Nisin being officiallyemployed by the food industry and thus the most widelyused Bacteriocins are peptides actually microbial toxinsproduced from various microorganisms and so far someof them (eg enterocins produced mostly by enterococci)have shown remarkable antimicrobial potential and theirapplication as a natural barrier against pathogens and foodspoilage has been proven to be very efficient when used inthe form of purified or semipurified extracts or as protectivecultures [9 10] Therefore as the developments in foodpreservation are focusing on the implementation of naturalantimicrobials and antioxidants this special issue exploresthe potential of alternatives to currently used preserva-tives through the publication of five high-quality articleswhich aim to address recent advancements in the field ofnatural food preservatives and antioxidants The prospectto replace synthetic preservatives with natural substanceshas been demonstrated by comparing the effects of Shirazithyme cinnamon and rosemary extracts (denoted as naturalantioxidants) with those of the synthetic antioxidant BHT onprotein and lipid oxidations physicochemical microbial andsensory characteristics of frozen beef burgers during storageSpecifically the oxidative stability of the beef burgers contain-ing Shirazi thyme cinnamon and rosemary extracts was welldemonstrated and the antibacterial activitywas documentedas the total microbial counts of the tested burgers were wellbelow the maximum allowed limit Besides the evaluationof the antimicrobial and antioxidant properties of naturalsubstances it is important to optimize their recovery Withregard to bacteriocins to enhance Enterocin Y31 productionand simplify the steps of separation and purification a propersimplified and defined medium (SDM) has been developedfor the Enterococcus faecium Y31 growth and enhancementof the Enterocin Y31 production The bacterial growth didnot result in Enterocin Y31 production in MRS medium andtherefore both the growth rate and the EnterocinY31 produc-tion were set as the goal for the investigation Single omissionexperiments revealed that 5 gL NaCl five vitamins twonucleic acid bases MgSO4sdot7H2O MnSO4sdot4H2O KH2PO4K2HPO4 CH3COONa fourteen amino acids and glucosewere essential for the adequate strain growth and EnterocinY31 production As a result a novel simplified and definedmedium (SDM) was formulated containing 30 ingredientsin which the Enterocin Y31 production yield was higherwhen compared to either MRS or CDM The developmentof the SDM improved the Enterocin Y31 production andsimplified the steps of purification (only two steps) whichis very promising and increases its potential applicationsReferring to seedsrsquo oils the optimization of the extraction

conditions of cactus pear seed oil has been obtained usingultrasound in a closed system based on the antioxidantactivity and using response surface methodology The yieldextraction and antioxidant and antimicrobial activity werecompared with those obtained using both conventional andunconventional methods such as Soxhlet and macerationusing heat agitation or long extraction times microwavesupercritical fluids and ultrasound-assisted extraction inan open and in a closed system The results have shownthat ultrasound exhibited lower oil yield and antioxidantactivity but had the potential to achieve comparable resultsif multiple ultrasound extractions are performed in the timeneeded by conventional methods Seed oils showed similarantimicrobial activity despite the extraction method and canbe an alternative extraction method of seed oils from fruitssuch as cactus pear Lastly the replacement of chemicaladditives with natural compounds has been addressed for fishfoods as well Fish-paste products also known as fish cakes orsurimi-based products are worldwide favorites Surimi a wetprotein concentrate of fish muscle is used as an intermediateraw material to produce surimi seafood The flavor texturetaste shelf-life and market value of surimi-based productsdepend on several factors including the additives used toprepare the surimi While preparing surimi with chemicaladditives several problems have been observed such as alack of unique characteristics inferior acceptability and poorfunctionality In this context a systematic review of fish-paste products prepared using natural food additives (eganimal seafood and plant source additives herbs and orientalmedicines grains and roots and functional food materials)has been performed which summarizes the existing relevantknowledge in the production of new value-added foodstuffsof interest for the surimi industry

In conclusion this special issue offers to the readers thechance to be informed on the recent advancements relatedto the antimicrobial and antioxidant properties of naturalsubstances that are of interest for the contemporary foodindustry Their prospective use in the food production hasthe potential to lead towards the production of safer andhealthier foods not excluding their contribution to a moreefficient preservation of the environment when chemicalswill be replaced with natural substances

Moreno BondiAndrea Laukova

Simona de NiederhausernPatrizia Messi

Chrissanthy Papadopoulou

References

[1] G Comi E Tirloni D AndyantoMManzano and L IacuminldquoUse of bio-protective cultures to improve the shelf-life andthe sensorial characteristics of commercial hamburgersrdquo LWT -Food Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[2] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWT - FoodScience and Technology vol 68 pp 385ndash390 2016

Journal of Food Quality 3

[3] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[4] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[5] H Sakkas P Gousia V Economou V Sakkas S Petsios and CPapadopoulou ldquoIn vitro antimicrobial activity of five essentialoils on multidrug resistant Gram-negative clinical isolatesrdquoJournal of Intercultural Ethnopharmacology vol 5 no 3 pp212ndash218 2016

[6] B Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Fatty Acids in Foods and their Health ImplicationsThirdEdition vol 20073230 of Food Science and Technology pp 263ndash301 CRC Press 3rd Edition edition 2007

[7] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

[8] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research (Formerly Natural Product Letters)vol 27 no 14 pp 1305ndash1314 2013

[9] R Iseppi F Pilati M Marini et al ldquoAnti-listerial activity of apolymeric film coated with hybrid coatings doped with Ente-rocin 416K1 for use as bioactive food packagingrdquo InternationalJournal of Food Microbiology vol 123 no 3 pp 281ndash287 2008

[10] A Laukova and P Turek ldquoEffect of enterocin 4231 in Slovak fer-mented salami puchov after its experimental inoculation withListeria Innocua Lirdquo ACTA Scientiarum Polonorum TechnologiaAlimentaria vol 10 no 4 pp 423ndash431 2011

Review ArticleNatural Food Additives and Preservatives forFish-Paste Products A Review of the Past Present andFuture States of Research

Khawaja Muhammad Imran Bashir1 Jin-Soo Kim2 Jeong Hyeon An1

Jae Hak Sohn13 and Jae-Suk Choi13

1Seafood Research Center IACF Silla University 606 Advanced Seafood Processing Complex Wonyang-roAmnam-dong Seo-gu Busan 49277 Republic of Korea2Department of Seafood and Aquaculture Science Gyeongsang National University 38 Cheondaegukchi-gilTongyeong-si Gyeongsangnam-do 53064 Republic of Korea3Food Biotechnology Division of Bioindustry College of Medical and Life Sciences Silla University 140 Baegyang-daero700 beon-gil Sasang-gu Busan 46958 Republic of Korea

Correspondence should be addressed to Jae-Suk Choi jsc1008sillaackr

Received 9 June 2017 Revised 15 August 2017 Accepted 17 September 2017 Published 27 November 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Khawaja Muhammad Imran Bashir et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Fish-paste products also known as fish cakes or surimi-based products are worldwide favorites Surimi a wet protein concentrateof fish muscle is used as an intermediate raw material to produce surimi seafood The flavor texture taste shelf-life and marketvalue of surimi-based products depend on the source of the fish meat type of applied heat treatment and additives used toprepare the surimi While preparing surimi with chemical additives several problems have been observed such as a lack of uniquecharacteristics inferior acceptability and poor functionality Various types of fish-paste products have been developed by usingdifferent ingredients (eg vegetables seafood herbs and oriental medicines grains and roots including carrots and functionalfood materials) However a systematic review of fish-paste products prepared using natural food additives has not yet beenperformedTherefore the quality characteristics of fish-paste products and their functionalities were elucidated in this study Withthe increasing demand for surimi seafood products the functional properties physiochemical properties and shelf-life of surimi-based products need to be improved This review will aid the preparation of new value-added products in the surimi industry

1 Introduction

Fish-paste products popularly known as fish cakes areproduced from frozen surimi (ie they are a kind of surimi-based product) and are popular in Korea and Japan [1] Inthe Korean Food Standards Codex fish cakes are known asa processed marine product comprising salt-soluble proteinsisolated from fish meat [2] Fish muscle is mechanicallydeboned washed with water and blended with cryoprotec-tants to prepare a wet concentrate of proteins called surimiSurimi is a Japanese term that is also known as washed fishmince It is a refined fish myofibrillar protein manufacturedthrough numerous step-by-step processes including headinggutting filleting deboning (mincing) washing dewatering

refining mixing with cryoprotectants freezing and metaldetection for HACCP [3] The myofibrillar proteins make itan excellent ingredient for developing food products It hasexcellent gelling properties and forms strong and elastic gelsupon heating [4]

The setting and deformation are important to preparesurimi and surimi-based products Setting also known asldquosuwarirdquo in Japanese is a very important process which hasa significant influence on the physiological and rheologicalproperties of surimi-based products Setting is a vital processin the quality estimation of surimi because it helps to improvethe water-holding capacity as well as the gel texture of surimi-based productsWhen fishmince paste (sol) is heated at a lowtemperature (up to 50∘C) a loose network (suwari) is formed

HindawiJournal of Food QualityVolume 2017 Article ID 9675469 31 pageshttpsdoiorg10115520179675469

2 Journal of Food Quality

from myosin and actomyosin molecules this process isreferred to as setting Setting is species dependent and occursover a range of temperatures (up to 50∘C) and to a varyingextent As the temperature is increased to around 70∘Csuwari is partially disrupted to form a broken net structure(modori) a phenomenon attributed to the dissociation ofmyosin from actin and the possible fragmentation of the actinfilament [5ndash7]

Most of the surimi-based products are different types offish-paste products while less than 10 include fish burgersfish ham and fish sausages [3] Surimi-based products areprepared by mixing the raw or frozen surimi with saltsand other ingredients molded and heated to form the finalproduct in the specified shape and texture and pasteurizedbefore packaging The kind of heat treatment depends on theflavor texture and appearance of the desired final productand may include broiling steaming deep-fat frying andboiling [8] while fish-paste products in South Korea aremostly prepared by frying [9] Textural characteristics suchas gel strength are the major determinant of surimi priceand quality [10] Several studies have attempted to enhancethe textural quality of surimi or surimi-based products usingvarious protein additives [11ndash14]

Surimi quality and gelling property are mainly affectedby both intrinsic factors (effect of fish species seasonalitysexual maturity and freshness or rigor) and extrinsic fac-tors (harvesting handling water characteristics processingtime and temperature solubilization of myofibrillar proteinsduring processing the activity of the endogenous or addedprotein oxidants and proteolytic enzymes washing cyclessalinity and pH) [3 134] Surimi forms thermoirreversiblegels upon heating which do not deform with further changein the temperature This phenomenon of surimi and surimi-based products is similar to that observed in other proteinssuch as egg white milk-lactoglobulin and wheat glutenAdditionally surimi produces gels of very high deformabilityand strength This heat-induced gelation property of surimimakes it a very valuable food ingredient [134]

The gel-forming ability and capacity of surimi areadversely affected by the proteolytic degradation of myofib-rillar proteinsThe presence of indigenous proteinases causedgel softening in surimi made from fish species for examplethreadfin bream [135] arrow tooth flounder [136] Pacificwhiting [137] and lizard fish and bigeye snapper [20 59]Various active proteinases in fish muscle are responsible forsoftening of the surimi gels Nakamura and Ogawa and Anet al testified that cathepsins L and B were the most activecysteine proteinases in Pacific whiting surimi and fish filletsrespectively [7 138] The myofibril-associated proteinasesobserved in lizardfish surimi were serine proteinases andcysteine while a serine proteinase was reported in the bigeyesnapper surimi [20 59]

Seasonal analysis of the compositional properties ofAlaska pollock and Pacific whiting showed higher proteincontents in winter while the moisture contents were higherin summer [139 140] Surimi prepared from cold-water fishspecies with low thermostability of myofibrillar proteinsmakes setting easier Normally a myofibrillar protein withlow thermostability is optimum to do setting because its

reactivity is increased due to the loose internal structure bysodium chloride addition and heat denaturation In contrastthe myofibrillar protein of tropical fish species with high heatstability is difficult to denature and form the myofibrillarprotein network structure in surimi [3]

Several research groups have studied ways to enhance thequality of surimi-based products by investigating the changesin microbial content enzyme activity nutrient content andacceptability characteristics the use of raw materials thestandardization of the manufacturing process storage andmarketing Natural and chemical food-grade additives suchas konjac flour proteinase inhibitors egg white and hydro-colloids have been used to enhance the gelling properties ofsurimi [12 17 20 23 34 141ndash143] The trypsin inhibitor inegg white plays a major role in improving the gel strengthof surimi The addition of egg white inhibits the proteolyticactivity of the modori-inducing enzyme in fish meat andsuppresses the decrease of elasticity in surimi Serum pro-teins have strong inhibiting abilities against the action ofvarious proteases with different active centers such as SHgroups and serine groups In addition they also containtransglutaminases that accelerate the setting Egg white andserum proteins also play an important role in inhibiting theenzymatic activity of the parasites Apart from the use ofadditives gel strengthening can be achieved by treating thegels at low temperatures (0ndash40∘C) before cooking [144 145]Furthermore the gel quality of surimi and surimi-basedproducts can also be enhanced by using alternate fish speciesor by acid and alkali washing to increase the myofibrillarprotein concentrations [7 146 147]

Surimi production worldwide reached around800000MT by 2011-2012 [3] while South Korea alonecontributed approx 156000MT in 2013 Over the yearsthe size of the market for Korean fish-paste products hasgradually increased reaching sim350 million US dollars in2013 (based on the amount produced) [148] Howevermanufacturers have had several problems in producingsurimi-based products such as a lack of unique character-istics and inferior acceptability and functionality Thereforethere have been several attempts to develop new fish-pasteproducts with excellent acceptability and functionalityTo this end numerous types of fish-paste products havebeen developed using various natural ingredients such asvegetables seafood animals plants herbs and orientalmedicines seaweed and functional food materials It is ofworldwide interest to use these natural food preservativesinstead of chemical or synthetic ones However to date nosystematic review of fish-paste products supplemented withvarious food raw materials has been performed Thereforethe quality characteristics of fish-paste products and theirfunctionalities were elucidated in this study

2 Improvement of the Gel Properties ofFish-Paste Products

Various food additives derived from animals (eg beefswine and chicken) seafood (eg fish invertebrates) plants(eg legumes cereals) sugars polyols and functional mate-rials used in fish-paste products to improve their gelling

Journal of Food Quality 3

capabilities and strength are listed in Table 1 and describedbelow

21 Animal Source Additives Various food-grade proteaseinhibitors from animal sources are used to enhance thephysical properties of surimi-based products as well to pre-vent the protein degradation The ability of beef plasma andother food-grade additives in surimi and fishmince preparedfrom Pacific whiting (Merluccius productus) was studied byMorrissey et al [12] The strongest proteolytic inhibitionwas observed with beef plasma protein at a concentrationas low as 1 Reppond and Babbitt reported the increase ingel strength of gels prepared by arrow tooth flounder at aconcentration of 2 with a yellow hue color [16] Weeras-inghe et al characterized the inhibitory activity of these food-grade inhibitors and reported that the inhibitory activity wasmainly because of specific serine proteinase inhibitors [17]The addition of 2 dried bovine plasma to steamed fish-pasteslightly increased the chewiness and hardness but it showeda negative effect on the gel strength [18] Duangmal andTaluengphol reported that the higher levels of beef plasmaprotein unfavorably affected gel characteristics of red tilapiasurimi gels [19]

The effect of porcine plasmaprotein on the bigeye snapper(Priacanthus tayenus) surimi gel characteristics was investi-gated by Benjakul et al [14]The gels supplemented with 05porcine plasma protein had the highest level of deformationand breaking force Benjakul and colleagues later reportedthe effect of porcine plasma protein on the gel characteristicsof surimi from bigeye croaker (Pennahia macrophthalmus)bigeye snapper (P tayenus) barracuda (Sphyraena jello)and threadfin bream (Nemipterus bleekeri) [20] The porcineplasma protein was effective in increasing the deformationand breaking force of kamaboko gels Higher breaking forcesand levels of deformation occurred when chicken plasmaprotein was supplemented to sardine kamaboko gels at levelsup to 2 [21] The inhibitory activities of cysteine proteinaseinhibitor fraction from chicken plasma on Pacific whitingand arrow tooth flounder mince were reported by Rawdkuenet al [22] Furthermore similar results were observed intheir extended study onPacificwhiting surimi where chickenplasma at a level of 2 inhibited the degradation of myosinheavy chain proteins [23]

Ovomucoid is a mucoprotein obtained from egg whitethat has been tested for its potential as a gel-degradationinhibitor [24 25] The addition of 2 ovomucoid couldincrease the breaking strength and gel deformation [28]The autolytic activities of lizardfish (Saurida tumbil) surimiand mince under the application of protease inhibitors wereinvestigated by Yongsawatdigul and Piyadhammaviboon[26] At all preincubation conditions egg white enhancedthe gel-forming capability of S tumbil surimi to a greaterextent than did whey protein concentrateThe addition of 1egg white and preincubation at 25∘C increased the breakingforce by twofold Campo-Deano and Tovar [27] reportedthat the addition of egg albumen at 15 and 2 for Alaskapollock and Pacific whiting surimi respectively enhancedthe gel strength of crab sticks According to Hunt et al theincorporation of 2-3 special dried egg white improved

the gel textural characteristics of Alaska pollock and Pacificwhiting surimi [28]

Whey is the complete set of proteins isolated fromthe watery portion of milk Whey protein is comprisedof 20 milk protein and 80 casein [149] Whey proteinconcentrates have generally been used as an emulsifierfiller water binder protein supplement foam stabilizer andthickener as well as gelling agent [150] Rawdkuen andBenjakul investigated the effect of whey protein concentrateon the gelling characteristics of surimi prepared fromgoatfish(Mulloidichthys vanicolensis) bigeye snapper (P tayenus)lizardfish (S tumbil) and threadfin bream (N bleekeri) [29]All the tested surimi supplemented with 3 whey proteinconcentrate displayed inhibitory activity against autolysis andsignificantly reduced gel whiteness However better water-holding capacity was obtained by increasing concentrationsof whey protein concentrate

Plasma proteins produced from pig cow and chickenbyproducts are relatively affordable and easily collectiblesources [143 151 152] However outbreaks of foot-and-mouthdisease avian influenza andmad cow disease as well as a banonproteins frompig bone and skin in some states for religiouscauses have made it essential to search alternative sources[153 154] Various fish plasma proteins have been testedincluding those from rainbow trout and salmon [31 35 36]

22 Seafood Additives The effects of shrimp head proteinhydrolysate fromdifferent shrimp namely black tiger shrimp(Penaeus monodon) northern pink shrimp (Pandalus eous)and endeavour shrimp (Metapenaeus endeavouri) on thegelling properties of lizardfish (Saurida spp) surimi wereinvestigated by Ruttanapornvareesakul et al [30] It wasreported that the freeze-induced denaturation of lizardfishmuscle protein could be reduced by the supplementation ofshrimp head protein hydrolysate at a concentration of 5resulting in higher Ca-ATPase activity and gel strength Theeffects of rainbow trout plasma proteins on the gelling prop-erties of surimi prepared by Alaska pollock were investigatedby Li et al [31] Gel degradation deformation the breakingforce water-holding capacity and whiteness enhanced withincreasing amounts of rainbow trout plasma protein anddecreased at higher concentrationsThe rainbow trout plasmaprotein at a concentration of 075mgg could be used asa potential protease inhibitor to inhibit gel weakening inAlaska pollock surimi Li et al reported the higher inhibitoryactivities of the recombinant chum salmon cystatin againstautolysis of Alaska pollock surimi [155]

Fish gelatin is extracted from the collagen of fish skinand it is used as a food additive Hernandez-Briones et alstudied the functional and mechanical properties of Alaskapollock surimi gels while using fish gelatin as an additive[32] The increasing concentration of gelatin affected thewhiteness but the sensory panelists were unable to detect itThese results showed that fish gelatin was not effective as afunctional additive in Alaska pollock surimi Nevertheless itcould be added at up to 10 gkg without negatively affectingthe mechanical properties of surimi Yin et al reported asignificant improvement in the endogenous transglutaminaseactivity of Alaska pollock surimi prepared with nanoscaled

4 Journal of Food Quality

Table1Naturalfood

additiv

esused

toim

provethe

gelpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Animalsource

additiv

es

Beefplasma

hydrolysate

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Atlanticmenhaden

(Brevoortia

tyrann

us)

Alaskap

ollock

(Theragra

chalcogram

ma)

Moistu

recontentproteincontent

cook

inglossw

ater-holding

capacitytexturetorsio

ntest

05

ndash15

[15]

Bovine

plasma

Bostaurus

Heatedin

awater

bath

Powder

Arrow

toothflo

under

(Atheresthessto

mias)

Walleye

pollo

ck

Moistu

recontentpu

nchtorsion

colortest

2[16]

Beefplasma

protein

Bostaurus

mdashPo

wder

Pacific

whitin

g(M

erlucciusp

rodu

ctus)

Proteincontentinhibitory

assay

4[17]

Drie

dbo

vine

plasma

Bostaurus

Steaming

Powder

Alaskap

ollock

(Tchalco

gram

ma)

Nutrie

ntcontentpH

water-holding

capacitytexture

and

sensoryevaluatio

n2

[18]

Beefplasma

protein

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Redtilapia

(Oniloticus

xO

placidus)

Colortextureexpressiblewater

protein

totalsulfhydrylcon

tent

2gkg

[19]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Bigeye

snapper

(Pria

canthu

stayenus)

Expressib

ledrip

amou

ntcolor

texturesetting

cond

ition

s05

[14]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Threadfin

bream

(Nem

ipterus

bleekeri)Bigeyes

napp

er(Ptayenus)

Baracuda

(Sphyraena

jello)and

Bigeye

croaker

(Penna

hiamacrophthalmus)

Trichloroacetic

acid-solub

lepeptidescolortextureprotein

content

05

[20]

Chickenplasma

protein

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Sardine

(Sardinella

gibbosa)

Colortextureexpressiblemoistu

re

proteincontentautolysis

activ

ity2

[21]

Cyste

inep

roteinase

inhibitorfrom

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Arrow

toothflo

under

(Astomias)Pacific

whitin

g(M

produ

ctus)

Autolysis

andinhibitory

activ

ity

pHprotein

content

3[22]

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Pacific

whitin

g(M

produ

ctus)

Torsionandfracture

test

dynamic

rheologicalattribute

2[23]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[24]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[25]

Eggwhite(EW)

Gallusgallusd

omesticus

Heatedin

awater

bath

Powder

Lizardfish(Saurid

atumbil)

mince

andsurim

iAu

tolytic

activ

itytexturalattributes

EW1

[26]

Eggalbu

min

Gallusgallusd

omesticus

Heatedin

thec

ooking

roller

Eggwhite

itself

Surim

i-based

crab

sticksfrom

Alaskap

ollock

(AP)

Pacific

whitin

g(PW)

(Mprodu

ctus)

Transie

nttest

streng

thtest

texture

dynamicrheologicaland

physical

attributes

AP

15

PW2

[27]

Journal of Food Quality 5

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Regu

lard

riedegg

white(REW

)speciald

riedegg

white(SEW

)liq

uideggwhite

(LEW

)

Gallusgallusd

omesticus

Heatedin

awater

bath

Spray-dried

powder

Pacific

whitin

g(M

produ

ctus)

Totalsulfhydrylgroup

sfracture

test

dynamicrheologicalattribute

SEW2-3

[28]

Wheyprotein

concentrate

Bostaurus

Heatedin

awater

bath

Wheyprotein

concentrate

Bigeye

snapper(Ptayenu

s)Goatfish

(Mulloidich

thys

vanicolen

sis)

Threadfin

bream

(Nblee

keri)

and

Lizardfish(Stum

bil)

Water-holding

capacitycolor

autolytic

activ

ity3

[29]

Seafoo

dadditiv

esSh

rimphead

proteinhydrolysate

from

northern

pink

shrim

pendeavou

rshrim

pand

blacktig

ershrim

p

Pand

alus

eous

Metapenaeus

endeavouri

Pena

eusm

onodon

Heatedin

awater

bath

Drie

dmatter

Lizardfish

(Saurid

aspp)

Gelstr

engthcolorgel-forming

abilityC

a-AT

Pase

activ

ity5

[30]

Rainbo

wtro

utplasmap

rotein

Oncorhynchu

smykiss

Heatedin

awater

bath

Freeze-drie

dplasma

Alaskap

ollock

Proxim

atea

nalysisw

ater-holding

capacitycolortextureprotein

content

075

mgg

[31]

Fish

gelatin

Com

mercialfishgelatin

(Gelatin

Rousselot)

Heatedin

awater

bath

Powder

Alaskap

ollock

Colorm

echanicalfunctio

nal

sensoryattributes

10gkg

[32]

Nanoscaled

fish-bo

neof

Pacific

whitin

gMprodu

ctus

Heatedin

awater

bath

Powder

Alaskap

ollock

Texturescanning

electron

microscop

y1g10

0g[33]

Nanoscaled

fish-bo

ne(N

FB)+

driedeggwhite

(DEW

)

Mprodu

ctusGallus

gallu

sdom

esticus

Heatedin

awater

bath

Powder

Pacific

whitin

g(M

produ

ctus)

Rheologicaland

texturalattributes

DEW

1+

10mgNFB

Cag

surim

ipaste

[34]

Salm

onbloo

dplasma

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)

Scanning

electronmicroscop

yproteincontentdynamic

rheologicalattributes

1g10

0g[35]

6 Journal of Food QualityTa

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Freeze-drie

dchinoo

ksalm

onplasma(

FSP)

and

concentrate

salm

onplasma

(CSP

)

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)surim

iand

Salm

onmince

Proteolytic

inhibitio

nautolysis

proteincontent

Salm

onminceC

SPgt

FSP

Pacific

whitin

gsurim

iFSP

[36]

Partially

purifi

edtrypsin

inhibitor

from

ther

oeof

yello

wfin

tuna

fish

Thun

nusa

lbacares

Heatedin

awater

bath

Freeze-drie

dBigeye

snapper

(Pria

canthu

smacracanthu

s)Proteolysis

colorw

ater-holding

capacitygellin

gprop

ertie

s3g

100g

[37]

Squidink

tyrosin

ase(SIT)

+tann

icacid

(TA)

Todarodesp

acificus

Heatedin

awater

bath

Mixture

Sardine

(Sardinella

albella)

Tyrosin

asea

ctivityinvitro

oxidationassaycolortexturaland

sensoryattributes

SIT

500U

gprotein+

TA1

[38]

Plantsou

rcea

dditives

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soybean

protein

Wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[39]

Soyprotein

eggwhite(EW)

wheyprotein

concentrate

(WPC

)La

ctalbumin

(LA)

milk

proteiniso

late

(MPI)

Glycinem

ax

Gallusgallusd

omesticus

Bostaurus

Coo

kedin

aste

amcooker

Powder

AlaskaP

ollock

(Tchalco

gram

ma)

Textureexpressib

lemoistu

recontentwater

retentionprop

ertie

sEW

andMPI

[4041]

Legu

mes

eed

extractfrom

blackcowpea

whitecowpea

soybeanseeds

Mun

gbean

peanut

Vignaun

guicu

lata

Glycinem

axVignaradiata

Arachish

ypogaea

mdash

Freeze-drie

dproteinase

inhibitor

extracts

Threadfin

bream

(Nem

ipterid

ae)

ThermalstabilitypHprotein

contentproteinase

inhibitory

assay

Blackcowpea

soybeanseeds

30mgg

[42]

Legu

mes

eed

extractfrom

Cow

pea

pigeon

pea

bambara

grou

ndnu

ts

Vignaun

guicu

lata

Cajanu

scajan

Vo

andzeia

subterranea

mdashPartially

purifi

edTrypsin

Threadfin

bream

(Nem

ipterid

ae)

Sarcop

lasm

icmod

ori-ind

ucing

proteinase

activ

itycolor

30ku

nits

g[43]

bambara

grou

ndnu

tprotein

isolate

Vignasubterranea

Heatedin

awater

bath

Powder

Threadfin

bream

(Nblee

keri)

Colorautolysis

025

g100g

[44]

Soyproteiniso

late

Glycinem

axHeatedin

awater

bath

Com

mercial

soyprotein

isolate

(JinQ

ui1200)

Alaskap

ollock

(Tchalco

gram

ma)

Com

mon

carp

(Cyprin

uscarpio)

Totaln

itrogen

andmoistu

recontentgelstre

ngthcolor

10

[45]

Journal of Food Quality 7Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soyprotein

wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[46]

Dietary

fiber

(DF)

from

peaa

ndchicory+

microbial

transglutaminase

(MTG

ase)

Cichorium

intybu

sPisum

sativ

umHeatedin

awater

bath

Powder

Hake(Mcapensis)

Gilthead

seabream

(Sparusa

urata)

Seab

ass(Dice

ntrarchu

slabrax)

Meagre(Argyrosomus

regius)

Dyn

amicrheologicalattributes

MTG

ase100U

g[47]

Proteiniso

lates

from

Mun

gbean

(MBP

I)black

bean

(BBP

I)bam

bara

grou

ndnu

t(BG

PI)

Phaseolusa

ureus

Phaseolusv

ulgarisV

igna

subterranea

mdashFreeze-drie

dpo

wder

mdash

Scanning

electronmicroscop

yproteolytic

autolyticandtrypsin

inhibitory

activ

ityassaycolor

texturetrichloroacetic

acid-solub

lepeptidec

ontent

1g10

0g[48]

Partially

purifi

edtrypsin

inhibitor

from

adzukibean

Vignaangularis

Heatedin

awater

bath

Freeze-drie

dpo

wder

Threadfin

bream

(Nblee

keri)

Proteincontenttexturecolor

trypsin

inhibitory

activ

ityautolytic

activ

ityassay

3g10

0g[49]

Amylose(A)a

ndam

ylop

ectin

(AP)

mdashHeatedin

awater

bath

Powder

Walleye

pollo

ck(T

chalcogram

ma)

Gelationandbreaking

strength

Amylose70+

Amylop

ectin

4

[50]

Wheatsta

rch

Triticum

aestivum

Heatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Com

pressio

ntest

dynamic

viscoelasticityscann

ingele

ctron

microscop

y

Starch10g

+Surim

i10g

[51]

Natives

weetp

otato

starch(N

SPS)

and

Mod

ified

sweet

potato

starch

(MSP

S)

Ipom

oeabatatas

Heatedon

acontrolled

stress

rheometer

Powder

Alaskap

ollock

(T

chalcogram

ma)

Dyn

amicrheologicalattributes

5[52]

Potato

starch

Solanu

mtuberosum

Heatedin

the

Krehalon

ecasin

gfilm

Powder

Pacific

sand

lance(Am

modytes

personatus

Gira

rd)

Proxim

atea

nalysis

protein

compo

sition

colorfoldingtext

texturalandsensoryattributes

8[53]

Rice

flour

Oryza

sativa

Fried

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorrheologicaland

sensoryattributes

10ndash15

[54]

Rice

flour

Oryza

sativa

Fried

Powder

Threadfin

bream

(Nem

ipterid

ae)

Moistu

recontentpH

color

texturalandsensoryattributes

50

[55]

Rice

flour

Oryza

sativa

Fried

Powder

Goldenthreadfin

bream

(Nem

ipterusv

irgatus)

Gelstr

engthsensoryattributes

14

[56]

Cryoprotectantsa

ndhu

mectants

Xanthan(X)

locustbean

(LB)

gumsa

loneX

LB

ratio

Ceratoniasiliqua

Heatedin

awater

bath

Powder

Silver

carp

(Hypophthalm

ichthys

molitrix)

Torsiontest

gel-formingability

mechanicalattributes

XLB

025075

[57]

Pectin

gum

(HM

LM)+

CaCl2

mdashHeatedin

awater

bath

Gum

and

powder

Silver

carp

(Hm

olitrix)

Water-holding

capacitym

echanical

andtexturalattributes

Pectin

gum1+

CaCl202

[58]

8 Journal of Food Quality

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Chito

san7B

from

praw

nshell

Not

mentio

ned

Heatedin

awater

bath

Not

mentio

ned

Barred

garfish

(Hem

iramphus

far)

ProteincontentSE

Mtextural

attributes

1[59]

Konjac

glucom

annan

aqueou

sdisp

ersio

nAm

orphophallu

skonjac

Heatedin

awater

bath

Aqueou

sdispersio

n

Giant

squid(D

osidicu

sgigas)

Alaskap

ollock

(T

chalcogram

ma)

ProteinsolubilitypH

texturaland

viscoelasticrheologicalattributes

1[60]

Carrageenan+

NaC

lorK

Clmdash

Heatedin

awater

bath

Hydrocollo

idAlaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorcompressio

ntest

Carrageenan1+

KCl15

[61]

Amorphophallu

skonjac

flour

(AKF

)Am

orphophallu

skonjac

Heatedin

awater

bath

Flou

rGiant

squid(D

gigas)

Water

retentionabilitycolor

texturalandsensoryattributes

10

[62]

NaC

l+high

hydrostatic

pressure

(HHP)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Proxim

atea

nalysis

FTIR

SEM

colormechanicalrheologicaland

sensoryattributes

HHP

300MPa

+NaC

l03

[63]

Sodium

chlorid

esugarspolyols

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Larim

ichthys

polya

ctis)

Water

activ

ityV

BNcolor

moistu

recontent

Sodium

chlorid

e4

Glucose10

Glycerin

10

[64]

Starchglycine

sodium

lactate

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Lpolya

ctis)

Water

activ

ityV

BNcolorm

oistu

recontent

Sodium

lactate75

[65]

Glycerol

mdashSteamed

Liqu

idMackerel(Scom

berjaponicu

s)andBrazilian

sand

perch

(Pseud

opercis

semifa

sciata)

Water

activ

itytexturaland

sensory

attributes

20

[66]

Naa

ndCa

salts

ofpo

lyuron

ides

and

carboxym

ethyl

cellu

lose

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gel-

streng

theningeffects

2ndash6

[67]

L-ascorbicacid

(AsA

)and

dehydro-L-

ascorbicacid

(DAs

A)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthanalysis

DAsA

10120583

gg

[68]

Sodium

-L-

ascorbate

(SA)

mdash

Steamed

inNojax

cellu

lose

casin

g

Powder

Alaskap

ollock

(T

chalcogram

ma)

pHtexturaland

sensoryattributes

02

[69]

120596-3

fatty

acids

from

algae

Not

mentio

ned

Heatedin

awater

bath

Oil

Cod

(Gadus

morhu

a)TB

ARS

fattyacid

contentcolor

500m

g85

g[70]

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)

Microscop

icob

servation

viscosity

gel-formingability

10

[71]

Journal of Food Quality 9Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)Th

readfin

bream

(Nem

ipterid

ae)White

croaker(Ge

nyonem

uslin

eatus)

andJapanese

jack

mackerel(Trachu

rus

japonicus)

Proxim

atea

nalysis

color

water-holding

capacityphysic

alattributes

5ndash30

[72]

120596-3

PUFA

s-ric

hoils

Flaxseedalgae

menhaden

krillblend

(flaxseed

algae

krill

811)

Heatedin

awater

bath

Oil

Alaskap

ollock

(T

chalcogram

ma)

Torsiontest

andrheological

attributes

9g10

0g[73]

Ethano

licKiam

woo

dextract

(EKW

E)+

commercialtann

in(C

T)

Hopea

sp

Heatedin

awater

bath

Overdrie

dpo

wder

Strip

edcatfish

(Pangasiu

shypophthalmus)

pHV

BNT

BARS

color

TCA-

solublep

eptid

emoistu

re

proteincontents

texturalattributes

EKWE

008

CT002

ndash004

[74]

Cocon

uthu

skextractw

ithethano

l60(C

HE-E6

0)

80(C

HE-E8

0)

Cocosn

ucifera

Heatedin

awater

bath

Freeze-drie

dpo

wder

Sardine

(Salbella)

Totalpheno

licexpressible

moistu

reT

CA-solub

lepeptideand

proteincontents

colortextual

rheologicalandsensoryattributes

CHE-E6

00125

[75]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Solutio

nMackerel

(Rastre

lligerk

anagurta)

SEMexpressiblemoistu

reprotein

contentcolortexturalandsensory

attributes

OFA

040

OTA

050

OCF

050

OCT

010

[76]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Bigeye

snapper

(Ptayenus)

SEMexpressiblemoistu

reprotein

andfre

eaminoacid

contentcolor

texturalandsensoryattributes

OFA

020

OTA

005

OCF

015

OCT

005

[77]

Eggwhitepo

wder

(EW)whey

protein

concentrate(WPC

)

Gallusgallusd

omesticus

Triticum

aestivum

Heatedin

awater

bath

Powdera

ndconcentrate

Lizardfish

(Stum

bil)mince

andsurim

i

Autolytic

activ

ityT

CA-solub

leoligop

eptid

esprotein

content

texturalattributes

EW4

WPC

4

[26]

Zinc

sulfate

(ZnS

O4)sodium

tripolypho

sphate

(STP

P)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Yello

wstr

ipetrevally

(Sela

roideslep

tolep

is)

Expressib

lemoistu

relipid

phosph

olipidand

proteincontent

Ca-ATP

asea

ctivitycolortextural

attributes

ZnSO460120583

molkg+

STPP

05

[78]

SEMscann

ingelectro

nmicroscop

yFT

IRFou

rier-transfo

rminfrared

spectro

scop

yVBN

volatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stancesT

CAtric

hloroacetic

acid

10 Journal of Food Quality

fish bones [33] Furthermore a study on the rheologicaland textural attributes of Pacific whiting surimi showedthat slow heating and the addition of nanoscaled fish bonessignificantly enhanced gel strength [34]

Fowler and Park reported an enhanced gelling strengthand effectively inhibited proteinase activity in Pacific whitingsurimi gels heated ohmically [35] Fowler and Park laterstudied the effects of salmon plasma from Chinook salmonon proteolytic inhibition of surimi [36] Salmon plasmaeffectively inhibited both serine and cysteine proteases as wellas proteases isolated from Pacific whiting Salmon plasmaconcentrated by ultrafiltration performed slightly better thanfreeze-dried salmon plasma at inhibiting autolysis in salmonmince

Klomklao et al reported inhibitory activity of a par-tially purified trypsin inhibitor (TIYTR) from yellowfintuna (Thunnus albacores) on the gelling characteristics ofbigeye snapper (Priacanthus macracanthus) surimi [37] Theincorporation of TIYTR with a level of 30 g100 g resultedin the enhanced deformation and breaking force of surimigels suggesting that the TIYTR could be employed as anaffordable and alternative proteinase inhibitor to enhance thegel strength of surimi prepared by bigeye snapper

Vate and Benjakul investigated the effects of squid inktyrosinase mixtures of tannic acid and protein on the gellingcharacteristics of sardine surimi [38] The highest deforma-tion and breaking force were obtained when surimi gels wereallowed to react for 90min while being supplemented with1 tannic acid and 500Ug squid ink tyrosinase proteinHowever gels with an added squid ink tyrosinasetannicacid mixture were whiter than the control The surimi gelssupplemented with squid ink tyrosinasetannic acid mixtureshowed the maximum overall acceptance scores suggestingthat it could be used as an additive to increase the surimi gelproperties

23 Plant Source Additives The chicken plasma proteinegg white and beef plasma protein are considered as themost effective protease inhibitors for surimi [17 22 23156] However the use of chicken plasma and beef plasmaprotein has been forbidden because of the occurrence of avianinfluenza and mad cow disease respectively In additionhigher concentrations of beef plasma proteins have also beenassociated with off-flavors while egg white is expensive andhas an unwanted egg-like odor [29 156] Additionally veg-etarians would not want to consume surimi-based productsprepared with additives from animal or even seafood sourcesTherefore alternate food-grade additives are still desired toenhance the gel strength of surimi without affecting thecustomer demandVarious natural additives derived from theplant sources have been briefly described below

231 Legumes Theeffects of vegetable protein contentmois-ture heating and setting conditions on the physical attributesof kamaboko were examined by Yamashita [39] A firm gelwas obtained at 60∘C for kamaboko with soybean proteinand at 80∘C with wheat gluten When the kamaboko gelswere supplemented with 5 vegetable protein the changes injelly strength softness and expressiblewater of the kamaboko

with wheat gluten were somewhat greater than those of thekamaboko with soybean protein According to the results ofChung and Lee the addition of plant proteins including soyprotein isolate lactoalbumin and wheat gluten remarkablylessened the strength of non-animal protein-incorporatedsurimi gels [40] The textural and sensory attributes offiberized surimi gel products were categorized as an increasein overall textural desirability and an increase in gel strengthIn another study egg white and milk protein isolate showedhigher water retention ability than whey protein concentratesoy protein isolate and lactoalbumin [41]

Protein isolates from legume seeds can be used as alter-nate protein additives for the quality improvement of surimigels Legume seed isolates comprise trypsin inhibitors andhave been used as the protease inhibitor in the prepara-tion of surimi and surimi-based products [42 43] Ben-jakul et al reported higher protease inhibitory activities ofinhibitor extracts from soybean and black cowpea seeds[42] A reduced gel-degradation activity (modori) and ahigh thermal stability were reported In another study theyreported inhibitory effects of proteinase inhibitor extractsfrom Bambara groundnuts (Voandzeia subterranea) pigeonpea (Cajanus cajan) and cowpea (Vigna unguiculata) onautolysis and gel-degradation activity (modori) of threadfinbream surimi [43] The whiteness of surimi gels reducedslightly with the addition of proteinase inhibitor Similarresults were obtained by Oujifard and colleagues [44] TheBambara groundnut protein extracts at a level of 025 g100 gshowed improved autolytic inhibition deformation andbreaking force in surimi prepared by threadfin bream (Nbleekeri) [44] However a slight reduction in whiteness wasobserved at increasing levels of Bambara groundnut proteinisolates These studies show that the addition of Bambaragroundnut protein extracts at a suitable level could serve asan alternative food inhibitor to enhance the gelling propertiesof surimi

Plant protein isolates mainly soy protein isolates havebeen used in the surimi industry because of their safety andrational price [45] Luo et al indicated the legumin andvicilin two main legume seed storage proteins as bindersand cogelling agents in surimi gels [45] Protease inhibitorsisolated from legume seeds not only can help to reduce thegel-degradation process in surimi but can also improve thesurimi gel properties by acting as filler or binder Luo etal reported higher breaking force and quality characteristicsof silver carp surimi when supplemented at a ratio of 10soy protein isolate [46] Cardoso et al studied the effects ofdietary fiber and microbial transglutaminase from chicoryand pea on the rheological properties of protein paste fromgilthead sea bream hake meagre and seabass [47] It wasfound that a high degree of protein denaturation boosted gelhardness while a low degree of protein denaturation createdgels with high deformability It shows that the addition ofmicrobial transglutaminase could serve as a possible additivefor gels of those species having lesser protein unfoldingability

Kudre et al studied the effects of black bean (Phaseolusvulgaris) and mung bean (Phaseolus aureus) protein isolateson gelling properties and proteolysis of sardines (Sardinella

Journal of Food Quality 11

albella) surimi [48] An increase in deformation breakingforce and water-holding capacity as well as a lower levelof degradation was observed while the whiteness of kam-aboko gels reduced slightly Therefore mung bean or blackbean protein isolates could be effectively used to retardthe proteolysis in sardine surimi leading to improved gelstrength Klomklao and Benjakul studied the effects of thepartially purified trypsin inhibitor from adzuki bean on thegelling properties and proteolysis of threadfin bream (Nbleekeri) surimi [49] An increase in autolysis and inhibitoryactivity against sarcoplasmic proteinases aswell as an increasein deformation and breaking force of kamaboko gel wasobserved at increasing levels of trypsin inhibitor while gelwhiteness decreased slightly

232 Starch Starch is widely used to make fish-paste prod-ucts as it enhances elasticity and increases the weight ofthe products In attempts to control thermal stability stick-iness andor wetness under different serving and storageconditions the functional characteristics of surimi seafoodproducts have been widely studied using modified starchesStarch is the second most abundantly used ingredient in themanufacturing of fish-paste products because of its higherwater-holding ability and capacity to replace fish proteinspartially while preserving the desired gel features at a reducedcost [69 157ndash161]

Kim et al reported a positive correlation between theamount of added starch and the quality of the food products[162] Konoo et al studied the effects of adding starch andamylose to amylopectin contents of starch on the gela-tion properties of frozen walleye pollack surimi [50] Thebreaking strength of gel was not affected by the changein amylose amylopectin ratio However it increased as thecontent of amylose increased in pregelatinized starch [51]A lower packing effect was observed at 90∘C which hypoth-esized that the gelatinization of starch in fish meat can beprevented at this temperature A strong correlation betweenthe amylose to amylopectin contents and the textural andrheological properties of starch-containing surimi gels wasalso reported by Lanier et al [134]

The addition of normal and modified potato or sweetpotato starch resulted in reductions in the characteristicstorage modulus of surimi sols during heating [52] Surimigels supplemented with potato starch showed the highestfirmness and cohesiveness Yoo reported the best texturalproperties of the sand lance (Ammodytes personatus) fish-paste products at a level of 8 potato starch [53] Thesestudies show that potato or sweet potato starch can also beused as a potent food additive for the production of surimi

233 RiceRice Flour Fish meat and wheat flour are themajor ingredients used for the production of surimi-basedproducts Rice flour however can be an important ingredientto enhance the rheological properties of surimi-based prod-ucts Several attempts have been made to evaluate the poten-tial of rice flour as an alternate of wheat flour in the prepara-tion of surimi products [41] The effect of rice flour additionmethods and milling types on the sensory and rheologicalattributes of surimi products were studied by Cho et al [54]

Roll-mil rice at a concentration of 10ndash15 displayed highergel strength and sensory properties which show that roll-millrice had strong potential for replacing wheat flourThe surimiproducts containing rice flour showed similar rheological andsensory characteristics to those of a finest commercial surimiproduct Hence rice flour might be an effective alternative towheat flour for high-quality surimi products

To replace wheat flour Kwon and Lee examined thequality characteristics of fried fish cakes containing rice flour[55] The total content of corn starch and rice flour was2883 of the total content of fish cake doughThere were nonoteworthy differences in the pHmoisture level appearancecolor flavor taste and overall acceptance as compared tothe control group The addition of 50 rice flour to surimi-based products could be an effective way to increase thecontent of rice flour without decreasing texture acceptabilityYoon et al optimized the content of water and rice flourin surimi-based products [56] The surimi-based productsmanufactured under optimal environment were comparablein gel strength to the commercial products However highersensory evaluation scores were observed compared to thoseof the commercial products These studies advocate that therice flour not only can be employed as an alternative to wheatflour but can also be used to enhance the quality of surimiand surimi-based products

234 Potato Powder The food additives extracted frompotato and potato protease inhibitors used in the preparationof fish-paste products are discussed in Sections 21 232 and244

24 Cryoprotectants and Humectants To inhibit denatura-tion and to lessen the damage of gel quality during coldstorage cryoprotectants are usually added to surimi productsPolyunsaturated fatty acids protein additives polyols sugarsamino acids salts and plant extracts are frequently usedas cryoprotectants and humectants to avoid fluctuationsin myofibrillar proteins promoted by freezing storage orthawing [163] Mechanical properties of surimi gels can beimproved by the addition of numerous hydrocolloids such askonjac carrageenan locust bean xanthan gum and differentmicrobial transglutaminases during the preparation of surimiproducts [57 164ndash166] In contrast the addition of alginateshas been reported to weaken surimi gels [69]

241 Saccharides Xanthan is a nongelling polysaccharideproduced by the aerobic fermentation of Xanthomonascampestris [167] The property of xanthan to form highlyviscous and stable solution at low levels makes it acceptablein the food industry [168] Xanthan displays quite remarkablesynergistic interactions with other nongelling polysaccha-rides of the galactomannan family leading to increases in gelformation and viscosity [168 169] The three commerciallyavailable galactomannans are tara gum locust bean gum andguar gum

The impact of low methoxyl pectin on the mechanicalproperties of silver carp surimi gels was studied by Barreraet al [58] An increase in hardness shear stress and water-holding capacity of the surimi gel was observed while no

12 Journal of Food Quality

significant improvement in the mechanical properties wasobserved as compared to the control Benjakul et al reportedthe effects of prawn-shell chitosan on surimi prepared bybarred garfish (Hemiramphus far) [59] Prawn-shell chitosanat a level of 1 of the surimi gel showed an increase in gel-enhancing effect on the heat-induced gelation of myofib-rillar proteins The addition of microbial transglutaminasegenerally increases the deformation and breaking force ofsurimi gel However this effect was significantly retardedin the presence of prawn-shell chitosan resulting in lowermagnitudes of deformation and breaking force

The viscoelastic properties and the thermal stability oflow-grade squid (Dosidicus gigas) surimi were investigated byIglesias-Otero et al [60] The konjac glucomannan aqueousdispersion at a level of 1 expressed the best rheologicalproperties suggesting that the konjac glucomannan aqueousdispersion may be used to enhance the quality characteristicsof low-grade squid surimi gel Ramırez et al evaluated theeffect of protein-hydrochlorides on the gel-forming ability ofmyofibrillar proteins [142] The xanthanlocust bean gum ata ratio of 025075 showed a positive improvement in themechanical attributes of surimi gels Eom et al investigatedthe impact of carrageenan on the gelation property of salt-based Alaska pollock surimi [61] The addition of 15KCl rather than 2 NaCl significantly enhanced the gellingproperty of 120581-carrageenan-induced surimi gel and showedincreased gel strength breaking force and whiteness values

242 Salts Salts help in protein-protein interaction and theaddition of salt is critical during the processing of fish-pasteproducts However the high levels of sodium in foods andconsequently human consumption of sodium have becomea global issue The prime harmful effects of excess sodiumintake are hypertension and increased blood pressure Sub-sequently these conditions lead to cardiovascular diseasesincluding instances of stroke heart attack and relateddiseases as well as gastric cancer and osteoporosis [170ndash172] Therefore to reduce sodium intake levels in fish-pasteproducts Hwang et al prepared the sodium-reduced friedfish cakes containing potassium as a substitute for sodium [1]The quality characteristics of 30 sodium-reduced fried fishcakes were not notably different from those of full-sodiumfried fish cakes however the addition of potassium changedthe color and reduced consumer acceptance To increase theconsumer preference for sodium-reduced fried fish cakes theuse of different food additives might be advantageous

The weak gel-forming ability and the strong fishy smellof the giant squid (D gigas) make it undesirable for themanufacturing of surimi-based products To overcome theseproblems Choi and Kim used Amorphophallus konjac flourto enhance the quality characteristics of giant-squid surimiproducts [62]The increasing levels ofA konjac flour showedincreases in gel texture and water retention ability while areduction in color and taste was observed as compared tothe commercial surimi products The incorporation of theseasoning ingredients such as sweeteners might be helpfulin removing the fishy smell of D gigas ultimately improvingthe gel properties of giant-squid surimi Cando et al reportedthat the sensory and mechanical properties of surimi gels

with reduced-NaCl contents can be improved by the appli-cation of 300Mpa high hydrostatic pressures [63] The gelsmade with lower-NaCl contents revealed stronger and stablenetworks as showed by the ones with higher-NaCl contents

243 Water Activity It has been reported that humectantshad the greatest effect on lowering water activity (119886

119908) with

the efficiency of the reduction in 119886119908value decreasing in the

order of NaCl sodium lactate glycerin propylene glycoland sorbitol when each of them was combined with otherhumectants [173] Kim and Park reported the impact ofhumectants such as sodium chloride sugars and polyols tolower the water activity (119886

119908) of various model kamaboko gels

[64]The effect of sodium chloride on lowering water activity(119886119908) was the highest among all of the examined treatments

while glucose caused browning reaction on the surface ofkamaboko In another study they examined the effect ofstarch glycine and sodium lactate in lowering the wateractivity (119886

119908) of model kamaboko gels [65] Sanchez Pascua et

al reported that glycerol (15ndash50) was effective in reducingthe water activity (119886

119908) in Brazilian sand perch (Pseudopercis

semifasciata) and mackerel (Scomber japonicus marplatensis)[66] Among the tested humectants the efficiency of thereduction in water activity (119886

119908) was observed decreasing in

the order of sodium lactate glycine and starch

244 Polyuronides The effect of sodium and calcium salts ofcarboxymethyl and polyuronides cellulose on the strength-ening of kamaboko gels was investigated by Niwa et al [67]It was reported that the calcium salts of pectinic acid pecticacid alginic acid and carboxymethyl cellulose enhancedthe breaking force of Alaska pollock surimi whereas theirsodium salts except Na-pectinate failed to increase the break-ing force The increase in the breaking force induced by cal-cium carboxymethyl cellulose vanished upon increasing thedegree of substitution of hydroxyl groups to carboxymethylgroups Furthermore fine cellulose particles enhanced thebreaking strain and breaking force and reduced the amount ofexpressible water but were unsuccessful in the case of coarserparticlesThe addition of potato starch can increase the effec-tiveness even in the presence of coarse particles of cellulose

245 Ascorbic Acid The addition of dehydro-L-ascorbicacid and L-ascorbic acid to Alaska pollock surimi increasedthe gel strength [68] It was suggested that the positiveeffect of L-ascorbic acid on gel formation might be due tothe oxidation of sulfhydryl groups in fish proteins Lee etal studied the effects of sodium-L-ascorbate on the gel-forming abilities of surimi prepared by Alaska pollock [69]Sodium-L-ascorbate remarkably enhanced the gel firmnesscohesiveness strength and sensory properties of the fiber-ized products at a level of 02 It directly influenced thesurimi quality regardless of vacuum treatment indicatingthat airborne oxygen was not important Freeze-syneresisstimulated by ascorbate during frozen storage was lessenedby the application of hydroxypropylated-modified starch

246 Unsaturated Fatty Acids The addition of nutritionallybeneficial 120596-3 fatty acids during surimi preparation could

Journal of Food Quality 13

enhance the gel strength and stability [70] For the effectiveuse of highly unsaturated fatty acids such as docosahexaenoicacid (DHA) and eicosapentaenoic acid (EPA) in surimi-basedproducts Okazaki et al studied the gel-forming properties offrozen walleye pollock surimi containing DHA and EPA [71]They reported that to achieve a good quality product thevigorous agitation of surimi with fish oil is essential to allowthe heat-induced gelation of its emulsified product throughthe formation of fine oil droplets

Fukushima et al investigated changes in the physi-cal properties of heat-treated surimi gels prepared fromthreadfin breamwalleye pollock Japanese jackmackerel andwhite croaker [72] The breaking strain breaking strengthand water-holding capacity of the heat-treated gels becamegreater as the amount of fish oil increased Furthermoresurimi seafood was nutritionally enhanced with 120596-3 polyun-saturated fatty acid- (PUFA-) rich oils isolated from natu-ral sources such as algae flaxseed menhaden blend andkrill [73] The Alaska pollock surimi supplemented with120596-3 PUFA-rich oils showed improved protein fundamentaltextural properties heat-induced gelation and endothermaltransitions These studies show that the interaction of unsat-urated fatty acids and surimi proteins could contribute to theimprovement in gel properties without altering the texturalattributes

247 Plant Ethanol Extracts The effect of commercial tan-nin and ethanolic Kiam wood extract on the gelling char-acteristics of ice stored mackerel (Rastrelliger kanagurta)surimi was investigated by Balange et al [74] During12 d of iced storage pH TBARS TCA-soluble peptide andtrimethylamine (TMA) contents as well as total volatilebase (TVB) of mackerel mince increased while gel-formingability myosin heavy chain band intensity and whitenessdecreased consistently Deterioration lipid oxidation andprotein degradation proceeded as storage time increasedAn increase in deformation and breaking force of surimigel was observed with the addition of 030 commercialtannin or 015 ethanolic Kiam wood extract during the first6 d of storage Therefore commercial tannin and ethanolicKiam wood extract had not shown a gel-enhancing effecton mackerel surimi Furthermore Buamard and Benjakulinvestigated the effects of coconut husk ethanolic isolateson the gel-forming ability of sardine (S albella) surimi [75]Breaking force increasedwith the increasing levels of coconuthusk ethanolic isolates while a decrease in whiteness and nodetrimental effect on the sensory attributes of surimi gel wasobserved It was concluded that the addition of coconut huskextracts at a suitable concentration could enhance the gelstrength of sardine surimi with increased acceptability

25 Compound Additives The effect of different oxidizedphenolic compounds such as tannic acid OTA ferulic acidOFA caffeic acid OCF and catechin OCT on the gellingattributes of mackerel (R kanagurta) surimi was studied byBalange and Benjakul [76] Gels supplemented with 050OTA 040 OFA 010 OCT or 050 OCF showedincreases in deformation and breaking forces while a decreasein the expressible moisture content and myosin heavy chain

band intensity was observed In another study they inves-tigated the effects of oxidized phenolic compounds on thegel-forming abilities of bigeye snapper (P tayenus) surimi[77] An increase in breaking force and deformation witha decrease in expressible moisture contents was observedGels supplemented with the oxidized phenolic compoundshad a finer matrix with smaller strandsThe physicochemicalcharacteristics of natural actomyosin advocate that oxidizedphenolics could trigger the induction of disulfide bondformation or the conformational changes and cross-linkingthrough amino groups Therefore the addition of oxidizedphenolic compounds at an optimum concentration couldenhance the strength of surimi gel

Yongsawatdigul and Piyadhammaviboon reported aninhibition in autolysis of surimi and mince preparedby lizardfish (S tumbil) caused by p-tosyl-L-phenylalanylchloromethyl ketone and phenylmethanesulfonyl fluorideindicating the involvement of myofibrillar-associated serineproteinase Tropomyosin and myosin heavy chain proteinswere mainly hydrolyzed resulting in poor textural prop-erties [26] Arfat and Benjakul investigated the effect ofzinc chloride (ZnCl

2) and zinc sulfate (ZnSO

4) on the gel-

forming abilities of surimi produced by yellow stripe trevally(Selaroides leptolepis) [78] The kamaboko gels with ZnSO

4

added up to levels of 60120583molkg showed increased deforma-tion whiteness and breaking force as well as highly denserand interconnected gels Therefore ZnSO

4at a suitable

concentration could enhance gel strength and whiteness ofdark-fleshed fish surimi

3 Improvement in Quality andFunctionality of Fish-Paste Products

Various food additives from seafood (eg fish invertebratesand seaweed) plants (eg vegetables fruits and herbalmedicines) mushrooms animal sources and functionalmaterials used to improve the quality and functionality offish-paste products are listed in (Table 2) and describedbelow

31 Seafood Additives It has been reported that various typesof seafood namely fish including dried anchovy (Engraulisjaponicus) powder [79 80] pufferfish (Lagocephalus lunaris)powder [88] and skate (Raja kenojei) powder [81 82] andinvertebrates including warty sea squirt (Styela clava) groundflesh [83] its freeze-dried tunic powder [84] omandungi(Styela plicata) ground flesh [85] shrimp (Acetes japonicus)powder [86] and seaweed such as green laver (Ulva spp) [87]have been used to enhance the quality and functionality offish-paste

The boiled and dried Japanese anchovy (E japonicus)is a popular fisheries product in Korea and Japan As theflesh can be eaten together with bone boiled and driedanchovy products are regarded as good sources of calcium[174] Bae and Lee evaluated the properties of fried fish-paste with added anchovy (E japonicus) powder containinga high amount of calcium [79]The fish-paste containing 10anchovy powder displayed the highest values of adhesivenesshardness and strength In the overall acceptance of sensory

14 Journal of Food QualityTa

ble2Naturalfood

additiv

esused

toim

provethe

functio

nalpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Seafoo

dadditiv

es

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

1-2

[79]

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

5[80]

Skate

Rajakenojei

Fried

Hot

wind-dried

skin

and

cartilage

(64)p

owder

Seab

ream

Moistu

recontentcolortextural

andsensoryattributes

3[81]

Skate

Rajakenojei

Steamed

Ferm

ented

flesh

Nemipterusv

irgatus

Aminoacidand

moistu

recontentcolortexturaland

sensoryattributes

20

[82]

Wartyseas

quirt

Styelacla

vaFried

Groun

dflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

5[83]

Wartyseas

quirt

Styelacla

vaFried

Freeze-drie

dtunicp

owder

Frozen

Itoyori

Colortexturaland

sensory

attributes

1[84]

Pleatedseas

quirt

Styelaplica

taFried

Grin

dedflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

15

[85]

Shrim

pAc

etesjaponicus

Fried

Powder

Frozen

seab

ream

surim

iMoistu

recontentcolortextural

andsensoryattributes

5[86]

Green

laver

Ulva

spp

Fried

Powder

Frozen

seab

ream

surim

iColorsensory

attributes

5[87]

Pufferfish

Lagocephalus

luna

risFried

Powder

Nemipterusspp

Moistu

recrude

protein

lipid

colortexturalandsensory

attributes

5[88]

Maesaengi

Capsosiphon

fulve

scens

Fried

Freeze-drie

dpo

wder

Frozen

seab

ream

surim

iColortexturaland

sensory

attributes

5[89]

Redsnow

crab

Chionoecetes

japonicus

Fried

Leg-meat

powder

Frozen

Alaskap

ollock

(Tchalco

gram

ma)

Physiochem

icalandsensory

attributes

6[90]

Plantsou

rcea

dditives

Mulberryleaf

Morus

alba

Fried

Powder

Seab

ream

Colortexturesensory

attributes

05

[91]

Onion

Alliu

mcepa

Fried

Ethano

lextract

Cutla

ssfishpaste

Moistu

recontentTB

CVBN

colorsensoryattributes

3[70]

Lotusleaf

Nelumbo

nucifera

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

05

[92]

Beetroot

andSpinach

Beta

vulga

risand

Spinaciaoleracea

Microwave

inkamaboko

shape

mold

Freshbeet

rootspinach

dish

Not

mentio

ned

Moistu

retexture

analysis

Beetroot10

Spinach15

[93]

Citrus

fruits

Citru

slim

onC

junosC

unshiu

Fortun

ellajaponica

varmargarita

Steamed

Groun

dflesh

pulpwith

out

seeds

Min

Daegu

flesh

Colortexturaland

sensory

attributes

Cumqu

at[94]

Journal of Food Quality 15

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Oatbran

+SiO2

Avenasativa

Boiled

Powder

Frozen

Alaskap

ollock

surim

iColortexturaland

physiochem

icalattributes

6gOatbran10

0gSiO2

[95]

Yam

Dioscorea

japonica

Fried

Powder

Pollo

cksqu

idshrim

pFo

ldingtest

colortexturaland

sensoryattributes

2[96]

WolfberryC

hinese

Goji

Fructuslycii

Fried

Powder

Seab

ream

Texturalandsensoryattributes

3[97]

Redginseng

Pana

xginsengCA

Meyer

Fried

Powder

Not

describ

edColorlipid

oxidation

sensory

attributes

1[98]

Korean

angelicar

oot

Angelicae

gigantis

Radix

Fried

Powder

Seab

ream

Texturalandsensoryattributes

05

[99]

Turm

eric

Curcum

alongaL

Fried

Powder

Pollo

cksqu

idshrim

pColorrheologicalandsensory

attributes

3[100]

Wasabi

Wasabiajaponica

Fried

Freeze-drie

dpo

wder

Silver

pomfre

t(Pam

pusa

rgenteus)

ColorT

BCviablec

ellcou

nt

texturalandsensoryattributes

18

[101]

Wolfip

oriaextensa

Poria

cocos

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

3[102]

Mushroo

madditiv

es

Butto

nmushroo

mAg

aricu

sbisp

orus

Fried

Chop

ped

fresh

Argyrosomus

argentatus

Texturalandsensoryattributes

10

[103]

Enok

imushroo

mFlam

mulina

velutip

esFried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

5[104]

Shiitakem

ushroo

mLentinus

edodes

Fried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

10

[105]

King

oyste

rmushroo

mPleurotuseryngii

Fried

Paste

Silver

whitecroaker(Penn

ahiaargentata)

Texturalandsensoryattributes

10

[106]

King

oyste

rmushroo

mPleurotuseryngii

Steamed

Paste

Cuttlefish

(Sepiaesculen

ta)

Texturalphysio

chem

ical

sensoryattributes

40

[107]

Animalsource

additiv

es

Poultrychicken

Gallusgallus

domesticus

Fried

Breastmeat

batte

r

Itoyori

Japanese

threadfin

bream(Ne

mipterus

japonicus)

Chem

icalcompo

sition

color

fatty

acid

compo

sition

TBARS

sensoryattributes

746

or1493

[108]

Functio

nalfoo

dadditiv

es

Long

-chain

cellu

lose

mdashBo

iled

Powdered

cellu

lose

Alaskap

ollock

surim

iTexturalandrheological

attributes

6[109]

Dietary

fiber

from

ascidian

tunic

Halocynthiaroretzi

Boiled

Refin

eddietaryfib

erAlaskap

ollock

surim

iColortexturalph

ysiological

andsensoryattributes

5[110]

16 Journal of Food Quality

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Fibera

nd120596-3

oil

mdashHeatedin

awater

bath

Powdered

fiber120596

-3oil

Alaskap

ollock

surim

iTexturalandrheological

attributes

Fiber6ndash

10g

and120596-3100

g[111]

Flaxseed

orsalm

onoil

Not

describ

edCoo

kedin

awater

bath

Oil

Frozen

Alaskap

ollock

surim

i(Tchalco

gram

ma)

TBARS

colortexturaland

sensoryattributes

2g10

0gfranks

[112]

Soybeanoil

Glycinem

axHeatedin

awater

bath

Oil

Frozen

silverc

arpsurim

iColortexturalattributes

Soybeanoilgt3

[113]

Calcium

powdero

fcuttlefish

bone

treated

with

aceticacid

Sepiaesculen

taHeatin

gin

awater

bath

Calcium

powder

Alaskap

ollock

surim

iMoistu

recontentcolortextural

andsensoryattributes

009

[114]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Alaskap

ollock

meatp

aste

Colortexturaland

sensory

attributes

017

[115]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Sand

lance

(Hypoptychus

dybowskii)

Acid

andperoxide

valueVBN

sensoryattributes

02

[116]

Cheong

gukjang

Ferm

entedGlycine

max

byBa

cillussp

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

2[117]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 17

evaluation small and large size fish-paste with 1 and 2respectively of added anchovy powder was preferred Thesimilar increasing trend of calcium intensity was observedby Bae et al [80] However the fried fish-paste productscontaining 20 anchovy powder displayed the highest valuesof adhesiveness hardness and strength Regarding overallacceptance in the sensory evaluation the fried fish-pastecontaining 5 anchovy was preferred The optimal amountsof added anchovy in the results from Bae and Lee and Bae etal were different which might have been due to the differentdrying methods and sizes of the anchovies used in each study[79 80] Despite the differences in the two studies the resultssuggest that anchovy powder could be applied to fried fish-paste products to achieve high calcium contents

Skate contains many essential fatty acids includinglinolenic acid linoleic acid arachidonic acid DHA andEPA [175] Skate skin contains high percentages of collagenprotein and calcium [176] while its cartilage is rich inchondroitin sulfate [177] To improve quality and nutrientlevels Cho and Kim prepared fried fish-paste with skate (Rkenojei) powder (hot wind-dried skin and cartilage powder[6 4]) [81] According to Park et al preference testingusing steamed fish-paste product with different levels ofadded 14-day-fermented flesh of skate showed significantincreases in brownness smoothness and skate flavor scores[82] The amino acid contents of fish cake samples with20 skate added had the highest overall preference scoresConsequently the addition of 20 skate powder was optimalfor the steamed fish cake to improve its quality characteristicswith higher protein contents

Warty sea squirt (S clava) aquaculture in the Masanarea of Korearsquos south coast contains abundant unsaturatedfatty acids and essential amino acids in its flesh [178] andglycosaminoglycan in its tunic [179] Warty sea squirt has aunique taste and distinct antioxidant and anticancer activities[180] Fried fish-paste supplemented with 20 warty seasquirt (Korean name miduduk) displayed improved qualityand functionality [83] Choi et al reported a fried fish-paste containing freeze-dried byproduct of warty sea squirt(S clava tunic) [84] The hardness and strength of fish-paste increased with increasing amounts of tunic powderFor overall acceptance in sensory evaluation a fish-pastesupplemented with 1 S clava tunic obtained a relativelyhigher score The results suggested that S clava flesh andtunic could be used for fish-paste products to improve theirquality and functionality Park et al reported improvementin the functional properties of fish-paste by adding S plicata(Korean name omandungi) [85] Fried fish-paste containing20 S plicata indicated the highest values of adhesivenesshardness and strength For overall acceptance in sensoryevaluation a fish-paste containing 15 S plicata obtained thehighest score

Seo and Cho reported the preparation of fish-paste withadded shrimp (A japonicus) powder [86] The hardnessspringiness and cohesiveness increased with the increasingconcentration of shrimp powder However the brittlenessand gumminess reduced In the sensory evaluation the fish-paste prepared with 5 shrimp powder was most preferredCho and Kim reported the preparation of fish-paste with

added green laver (Ulva spp) powder [87] The hardnessspringiness and cohesiveness increased with the increasingconcentration of green laver powder However the brittlenessand gumminess decreased upon the addition of green laverpowder In the sensory evaluation a fish-paste prepared with5 green laver powder was preferred over other fish-pastesThese results suggest that green laver powder could be appliedto fish-paste to improve its quality and functionality

Pufferfish containing taurine hydroxyproline lysine andglycine impart a characteristic taste to food [181] To improvethe taste of fish-paste products Park prepared a fish-pasteby adding green rough-backed pufferfish (L lunaris) pow-der [88] The hardness strength gumminess springinessand chewiness of the fish-paste increased depending onpufferfish powder contentThe preparation of fish-paste withadded Capsosiphon fulvescens powder was reported by Park[89] The hardness springiness strength and cohesivenessincreased with the increasing concentrations of C fulvescenspowder However the brittleness and gumminess reducedwith the addition of C fulvescens powder In the sensoryevaluation overall the fish-pastes prepared with 5 Cfulvescens powderwere preferred over other fish-pastesThusthe results show that C fulvescens powder could be used tocreate fish-paste products with high quality and functionality

Kim et al reported the changes in the sensory and physic-ochemical properties of a fish-paste containing red snow crab(Chionoecetes japonicus) leg-meat powder [90] Hardnessgumminess springiness and cohesiveness increased withincreasing levels of red snow crab leg-meat powder Based onthe sensory evaluation it was concluded that the addition ofred snow crab leg-meat powder at a level of 6 could improvethe quality characteristics of fish-paste products

32 Plant Source Additives It has been reported that variousplant sources namely vegetables (eg mulberry beetrootand spinach) fruits (eg citrus) and herbal medicines (egChinese matrimony vine Korean Angelica root) have asignificant effect in improving the quality and functionalityof fish-paste products

Mulberry (Morus alba) leaf has been used traditionallyto treat a disease symptomized by thirst and stroke [182]Ever since mulberry leaf was included as a food material inthe Food Codex in 1988 by the Ministry of Food and DrugSafety (MFDS Osong Chungju South Korea) Mulberry leafpowder has been used in various processed food productsand health functional foods Shin and Park reported theuse of mulberry leaf powder in the preparation of fish-pasteproducts [91] In a texture meter test the hardness increasedbut the cohesiveness springiness gumminess and brittlenessdecreased with increasing levels of mulberry leaf powder Insensory evaluation the fish-paste with 05 mulberry leafpowder revealed the highest acceptance scores in terms offlavor texture and overall quality

Garden onion (bulb onion Allium cepa) is a perennialplant belonging to Liliaceae and is widely used as a spice andseasoning vegetable in both the East and the West Park etal investigated the quality characteristics of fried fish-pastesupplemented with flavonol-rich ethanol extract of onion[183] In the sensory evaluation as the amount of ethanol

18 Journal of Food Quality

extract of onion increased so did the favorability in termsof flavor and taste Notably 3 ethanol extract of onion hadthe best score in overall acceptance The results indicate thatethanol extract of onion can be used to prepare fried fish-paste products with high quality and functionality

Shin reported the production of fish-paste with addedlotus (Nelumbo nucifera) leaf powder [92] The flavor adhe-siveness and hardness increased with the increasing levels oflotus leaf powder The fish-paste with 05 lotus leaf powderdisplayed the highest acceptance scores in terms of springi-ness pleasant taste appearance texture flavor and overallquality Thorat et al prepared kamaboko containing greenchili coriander ginger garlic spice mixture and groundbeetroot or a spinach dish and then subjected the preparationto microwave cooking [93] Kamaboko prepared with 10beetroot and a 15 spinach dish was found to be superior tothe others

Yang and Cho developed a steamed fish cake with added5 ground citrus fruits with skin [94] The addition of citrusfruits did not disturb the flexibility of surimi The pH ofsurimi samples increased in the following order lemon (Cit-rus limon) citron (Citrus junos) tangerine (Citrus unshiu)kumquat (Fortunella japonica var margarita) and controlThe hardness of surimi was highest for lemon followed bycitron tangerine kumquat and control surimi In the sensoryevaluation surimi containing kumquat demonstrated higherscores in terms of color taste and textural properties Theseresults suggest that surimi could be prepared by adding citrusfruits to improve the quality and functionality

Oat bran is a gluten-free dietary fiber that may decreasethe risk of diabetes and heart diseases The physicochemicalproperties of surimi gels supplemented with oat bran werestudied by Alakhrash et al [95] The oat bran and SiO

2

incorporation (6 g100 g) greatly improved water-holdingcapacity and gel texture while a reduction in whiteness wasobserved Kim and Byun conducted tests on the sensoryand physicochemical characteristics of fish-paste with addedyam (Dioscorea japonica) powder [96] The addition of yampowder increased gumminess strength springiness andcohesiveness In the sensory evaluation the addition of 2yam powder had the best scores in terms of taste color andoverall preference

Fructus lycii is a fruit produced by Lycium barbarumL that has been used for nourishment tonicity and nour-ishment of the blood it has antibacterial anticancer andantioxidant properties [182ndash186] Shin et al prepared friedfish-paste containing dried F lycii powder [97] In the texturalanalysis cohesiveness increased while brittleness and gum-miness decreased with increasing levels of F lycii powderThe 3 F lycii powder sample had the highest acceptancescores in terms of appearance texture taste flavor andoverall acceptability

Red ginseng-based fried fish-pastes containing differentsizes and amounts of red ginseng powder were preparedand their biological properties including lipid oxidation toimprove fish-paste quality were investigated [98] The fish-paste products containing red ginseng powder showed asignificant increase in hardness and chewiness Furthermorean inhibitory effect on lipid oxidation and reduced number

of total microbes during storage were observedThese resultssuggest that high-quality fish-pastes could be achieved withthe addition of 1 red ginseng powder which effectivelyimproved both sensory evaluation and physicochemicalproperties

Angelicae Gigantis Radix (the dried root ofAngelica gigasNikai) more popularly known as Korean Angelica is one ofthe widely used herbal medications [187] It has been usedin Korean medicine as an important medication for anemiaand blood circulatory disorders It has also been used formenstrual pains and postmenopausal syndromes Shin et alreported the development of fish-paste with A gigas powder[99] In a texture test hardness chewiness and brittlenessincreasedwith increasing concentrations of AngelicaeGigan-tis powderHowever cohesiveness and springiness decreasedIn the sensory evaluation the fish-paste with 05 AngelicaeGigantis powder showed the highest acceptance scores forappearance flavor taste texture and overall quality

Turmeric (Curcuma longa) has been used in Ayurvedicmedicine from ancient times as a treatment for inflammatoryconditions It has been reportedly used for its various bio-logical activities including antibacterial antiviral antifungalantioxidative and antiatherogenic effects [188] Turmeric hasbeen grown as a special crop in the central and southern areasaround Jindo in South Korea [189] Choi et al investigatedthe sensory and rheological properties of fish-paste preparedwith turmeric powder [84] In terms of textural attributesthe addition of C longa powder decreased springiness andimproved strength In the sensory evaluation the addition of3 C longa powder was associated with the best scores fortaste and overall preference

Wasabi (Wasabia japonica) has various beneficialhealth properties including antioxidative antimicrobialand antimutagenic activities [190 191] Jang et al reporteda high-quality fried fish-paste product made with silverpomfret (Pampus argenteus) which is one of the savorysoft and delicious types of fish prepared by adding wasabipowder [101] Notably hardness gumminess and chewinessincreased significantly with the addition of wasabi powderIn the sensory evaluation 18 wasabi powder showed thebest score in overall acceptability These results show thatwasabi could be used as a food additive or preservative infish-paste products

White Poria cocos wolf is the inner white part of P cocosa parasite found on Pinus densiflora It is used to treat edemachronic gastritis gastric atony nephrosis acute gastroentericcatarrh emesis dizziness and vomiting [192 193] Shin et alprepared a fried fish cake with added white P cocos powderand studied the textural and sensory characteristics [102]In texture tests brittleness was observed to increase whilespringiness decreased with increasing concentrations of Pcocos powder The fish-paste product containing 3 whitePoria cocos powder showed the highest acceptance scores forflavor appearance texture taste and overall quality

Milk-vetch root is one of the most produced herbalmedicines in Korea It is a peeled and dried root of the herba-ceous perennial herb known as Astragalus membranaceuswhich belongs to the Fabaceae family [194] It has been

Journal of Food Quality 19

reported that milk-vetch root exerts diuretic tonic anti-hypertensive hypoglycemic immune-enhancing antitumorand antiviral effects [195] Kim investigated the sensoryand physicochemical properties of fish-paste prepared withmilk-vetch root powder [196] The strength cohesivenessbrittleness and gumminess of the fish-paste increased whileits springiness decreased with an increasing amount of milk-vetch root powder In the sensory evaluation the addition of10 milk-vetch root powder indicated best scores for tastetexture color and overall preference

33 Mushroom Additives Mushroom is a nutritional andfunctional food as well as a vital source of physiologicallybeneficial medicines Mushrooms have been used as tradi-tional medicines in Korea Japan China and other Asiancountries for curing various diseases including lymphaticdisease gastroenteric disorder oral ulcer and various can-cers [197] It has been reported that edible mushrooms inKorea number approximately 350 species [198] Several ediblemushrooms that are highly preferred have been added to fish-paste to enhance their quality and functionality

Ha et al prepared a fried fish-paste product with addedAgaricus bisporus which is a product described as having aracy flavor and taste [103]The elasticity hardness brittlenessand gumminess of fish-paste with the added mushroomincreased however no significant difference in strengthwas observed Regarding overall acceptance in a sensoryevaluation a fish-paste supplemented with 10 A bisporusmushroom showed the highest scores

Enoki mushroom (Flammulina velutipes) is well knownfor its anticarcinogenic and blood pressure-reducing prop-erties To utilize its functional properties enoki mushroomwas added to fried fish cake [104] The sample containing15 mushroom received the highest values for strengthgumminess and brittleness In the sensory evaluation thefish cakes with 5 mushroom obtained favorable scores foroverall acceptance

Shiitake mushroom (Lentinus edodes) is known for itshigh level of 120573-glucans Son et al investigated the effectsof shiitake mushroom on the textural properties of friedfish cake [105] The fish cake containing shiitake mushroomreceived the highest values for strength hardness gummi-ness and brittleness In the sensory evaluation the fish cakeswith 10 shiitake mushroom sample obtained the best scorefor overall acceptance

Kim et al prepared a fried fish cake using cultured kingoyster mushroom (Pleurotus eryngii) and silver white croaker(Pennahia argentata) surimi to enhance its physiologicaleffects [106] In assessing its quality properties fish cake towhich 10 mushroom was added received the highest valuesfor strength hardness gumminess and brittlenessThe effectof king oyster mushroom on the textural and physicochem-ical properties of steamed cuttlefish (Sepia esculenta) fishcake was investigated by Chung et al [107] The fish-pastewith added king oyster mushroom paste revealed significantdecreases in gumminess cohesiveness and hardness whilethe springiness increased with increasing concentrations ofking oystermushroompasteOn the sensory evaluation basisthe cuttlefish-paste supplemented with 30ndash50 king oyster

mushroom showed higher overall acceptability In the studiesby Kim et al and Chung et al the optimal amounts of kingoyster mushroom differed which might have been due tothe different cooking methods and surimi used in each study[106 107]

34 Animal Source Additives Jin et al investigated the effectof chicken meat on the quality characteristics of Itoyori(Japanese threadfin bream Nemipterus japonicus) surimi[108] The physicochemical properties such as fatty acidcomposition shear force and gel characteristics were affectedby substitution with spent laying hen meat batter Howeversensory characteristics were less affected by this substitutionA huge amount of waste in the processing of grass carp isdiscarded To deal with this waste Gao et al studied theprocessing technology used for fish and mushroom pastewith salted fish cubes mushroom soybean and fermentedsoybeans [199]

35 Functional Food Additives Functional food additivesincluding dietary fiber 120596-3-rich oil calcium additives andpropolis have been used in the preparation of fish-pasteproducts to increase their quality and functionality Westernpopulations have an inadequate quantity of health beneficialdietary fiber in their diets Besides fiber most Western pop-ulations also consume an insufficient amount of 120596-3 PUFAswhile their sodiumconsumption greatly surpasses the recom-mended maximum Debusca et al prepared Alaska pollocksurimi fortified with commercial long-chain cellulose as asource of dietary fiber [109] Fiber fortification up to a level of6 improved both texture and color a slight decline in thesevalues was observed at levels of 8 fiber An increase in gelelasticity and thermal gelation of the fish cake was observed

Yook et al prepared a fish-paste by adding dietaryfiber extracted from ascidian (Halocynthia roretzi) tunic toenhance its physiological properties [110] The hardnessgumminess adhesiveness shear force and chewiness of thefish-paste improved with the incorporation of the ascidiandietary fiber The fish-paste with 5 ascidian dietary fiberscored the highest and was generally preferred by sensorypanels Tolasa et al reported that the oxidative stability andthe uniform dispersion of 120596-3 unsaturated fatty acids can beattained in a highly consistent surimi gel system without theuse of antioxidants [200]

Surimi and surimi-based products are famous through-out the world In fact US consumption increased in the1980s while the rate leveled off thereafter The nutrificationof food products with 120596-3 PUFAs increases the health ben-efits of food consequently increasing their market demandPietrowski et al prepared surimi seafood products nutrition-ally enhanced with 120596-3 PUFAs [201] Although the nutrifica-tion of 120596-3 PUFAs indicated an increase in lipid oxidationit was within limits acceptable to consumers The color ofsurimi seafood nutrified with 120596-3 PUFAs generally improvedbut no effect on textural characteristics was observed

Debusca et al reported that the fortification of Alaskapollock surimi with either 120596-3 oil or dietary fiber alone orin combination improved both the textural and rheologicalproperties [111]The120596-3 oil and fiber in combination revealed

20 Journal of Food Quality

greater gelation of surimi and a slight reduction in color prop-erties indicating their interaction with myofibrillar proteinsThus it was suggested that the 120596-3 oils and fiber could beeffectively used as a fortifying agent to prepare high-qualitysurimi products with nutritional benefits Sell et al preparedsurimi franks fortified with salmon oil or flaxseed [112]The textural properties showed differences between franktypes with the flaxseed franks being cohesive less gummysofter and chewy while the sensory evaluation showed nosignificant differences

Chang et al determined the effects of soybean oil andmoisture contents on the physical properties of surimi gels[113] The increasing levels of soybean oil and moisturecontents resulted in an increase in whiteness and reductionin the chewiness hardness and breaking force Setting incombination with soybean oil improved the textural andcolor parameters of surimi gels indicating that soybean oilcould be used to improve the color and textural properties ofsurimi seafood products

Kim et al prepared boiled fish cake using acetic acid-treated cuttlefish bone as a calcium additive agent [114] Theresults of sensory evaluation of texture and whiteness weresimilar to those without this supplementation In the mineralcontent analysis of heat-induced surimi gel calcium contentincreased depending on the increasing concentration ofacetic acid-treated cuttlefish bone powder while phosphoruscontent did not change The optimal concentration of aceticacid-treated cuttlefish bone powder for the preparation ofhigh-quality heat-induced surimi gel was 009

Kim et al prepared Alaska pollock fried fish-pastesupplemented with propolis [115] The addition of propolisenhanced the antispoiling and antioxidative ability as well asgel strength of fried fish-paste In the sensory evaluation theaddition of 017 propolis showed the best score in overallacceptability In another study Kim et al later studied sand-lance (Hypoptychus dybowskii) meat paste prepared withpropolis [116] Similar to the previous report the addition ofpropolis on the fried fish-paste showed higher antioxidativeand antispoiling activities The fried sand-lance meat pasteprepared with 02 added propolis was the most acceptableFurthermore the bitter taste of the sand-lancemeat paste wasreduced by adding 2 sweet amber powder

Cheonggukjang is an ancient Korean food prepared byfermented soybean It contains high levels of dietary fiberoligosaccharides isoflavones saponin lecithin phytic acidand phenolic compounds among others Its many benefi-cial properties have been reported such as thrombolyticanticancer antimicrobial hepatoprotective antioxidant andcholesterol-lowering effects [202] Park et al reported theuse of fish-paste containing cheonggukjang powder [117]Theincreasing concentrations of cheonggukjang resulted in anincreased value of springiness cohesiveness and hardnesshowever a reduction in brittleness and gumminess values offish-paste was observed

4 Shelf-Life Extension of Fish-Paste Products

Fish-paste products may easily spoil due to residualmicrobes that are not removed by sterilization during the

manufacturing process or by contamination in packagingor the distribution process For such reasons even vacuum-packed fried fish-paste products have a shelf-life of fewerthan 10 days during cold storage which is relatively short[121 122] Various efforts have been made to develop long-term storage solutions for fish-paste products via physicaland chemical methods [118ndash122] Although these methodswere found to be very effective for the long-term storageof fish-paste products they require sensitive and complexmanipulation and are costly

The addition of appropriate food additives to fish-pasteproducts as an effective preservation protocol is anotherstrategy Potassium sorbate is a typical synthetic food preser-vative and is commonly used in processed foods includingfish-paste productsThis material is effective in inhibiting thegrowth of variousmicroorganisms as it has a slight sterilizingeffectThe use of this material is permitted to a concentrationof less than 20 gkg in processed fish meat products (FoodCode Ministry of Food and Drug Safety Republic of Korea)According to the results of Walker sorbates and sorbic acidexert a very low level of mammalian toxicity even in chronicstudies as up to 10 of the diet did not show any carcinogenicactivity [203] In addition Thakur and Patel summarizedthe application of sorbates in the shelf-life extension of fishand fish-based products [204] The physical and chemicalmethods along with natural food preservatives for the long-term storage of fish-paste products are listed in Table 3 andbriefly described below

41 Physical and Chemical Methods Various efforts havebeen focused on developing long-term storage solutions forfish-paste products via physical methods including highpressurization [118] microwave pasteurization [93] highhydrostatic pressure treatment [119] and even irradiation[118 121] In addition it has also been reported that treatmentwith chlorine dioxide solution at an appropriate concentra-tion which is harmless to humans could be used to preventspoilage and to extend the shelf-life [122]

High hydrostatic pressure technology has graduallygained popularity in the food industry over the last twodecades [205] In 2013 the worldwide market for highhydrostatic pressure equipment was estimated to be $350million and it is expected to grow Besides high hydrostaticpressure technologies several types of radiation have alsobeen tested including ultraviolet microwaves and gammairradiation treatments Radiation is generally used to controlbiological hazards in the production of fish-paste productsand to prolong the shelf-life of such products [206 207]Gamma radiation exerts potent antimicrobial effects whereasultraviolet rays are effective for the surface but not interiorsterilization of porous dried fish products (eg fish-pasteproducts) However gamma irradiation treatment demandslarge-scale facilities and higher costs [207 208]

Miyao et al reported that growth of the majority of thepathogenic microorganisms present in surimi was inhibitedat a high pressure of between 300 and 400Mpa [118] Severalpressure-resistant strains were isolated from surimi and wereidentified as Moraxella sp Acinetobacter sp Streptococcusfaecalis and Corynebacterium sp It was suggested that

Journal of Food Quality 21

Table3Naturalfood

additiv

esandph

ysicochemicalmetho

dsused

toim

provethe

shelf-life

offish-paste

prod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Physicalandchem

icalmetho

ds

Highhydrostatic

pressure

mdash

High-pressure

treatmento

rheattre

atment

insampletub

ewith

vacuum

packaging

mdashFrozen

Alaskap

ollock

Microbialactiv

ity40

0MPa

[118]

Highhydrostatic

pressure

mdashNot

cooked

mdash

Tuna

fishpaste

Mackerelp

astewith

paprika

mackerelp

astewith

garlic

mackerelp

astealon

eand

salm

onpaste

Microbialactiv

ity200M

Pa[119]

Co-60

Gam

mar

ays

mdashGrilled

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

texturalsensorym

icrobial

physiochem

icalattributes

75kG

y[120]

Co-60

Gam

mar

ays

mdashFried

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

pHtexturalmicrobial

physiochem

icalattributes

3kGy

[121]

Chlorin

edioxide

(ClO2)

mdashSteamed

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

VBN

TBA

RSpHm

icrobial

physicochemicalsensory

attributes

50pp

m[122]

Naturalfood

additiv

esRe

dpepp

erethano

lextract(RP

EE)

andchop

pedfre

shredpepp

er(C

FRP)

Capsicu

mannu

umFried

Ethano

lextract

andchop

ped

fresh

one

Frozen

Alaskap

ollock

TBC

sensoryattributes

RPEE

10

CF

RP5

[123]

Ethano

lextract(EE)

andwater

extract

(WE)

Phellodendron

amurense

Eugenia

caryophyllu

sPinu

srigida

Bletillastr

iata

andPa

eonia

albiflora

mdashmdash

mdashAntim

icrobialattributes

onpu

trefactiveisolatesfrom

fish

meatp

asteprod

ucts

EE2000

ppm

[124]

Eggwhitelysozyme

(EWL)

andor

sodium

hexametapho

sphate

(SHMP)sod

ium

pyroph

osph

ate(SP

P)

Gallusgallus

domesticus

Fried

Powder

Frozen

Alaskap

ollock

Viablecellcoun

tpH

VBN

biochemicalattributes

EWL5

+SP

P05

+SH

MP

01

[125]

Grapefruitseed

extract

Citru

sparadisi

mdashSolutio

nCom

merciallyavailablefi

shmeat

paste

prod

ucts

Proxim

atec

ompo

sition

textural

biochemicalrheologicalsensory

attributes

1000

ppm

[126]

22 Journal of Food Quality

Table3Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Cinn

amon

bark

extract

Cinn

amom

umcassia

Fried

Extracted

solutio

nFrozen

Alaskap

ollock

Antim

icrobialactiv

itySprayeddiluted

extract(11)

[127]

Alginicacid

hydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Relativev

iscositypHcolor

rheologicalattributes

03

[128]

Chito

sanhydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Viablecellcoun

tsrheological

sensoryattributes

03

[129]

Nisin(N

)and

or

sucrosefattyacid

esters(SFE

)mdash

Steamed

Powdera

ndsolutio

nFrozen

Alaskap

ollock

Viablecellcoun

tantim

icrobial

activ

ityN125120583

gg+

SFE10mg

[130]

Piscicolin

KH1

Carnobacteriu

mmaltalomaticu

mSteamed

Solutio

nCod

fish

Inhibitory

assayproteincontent

antim

icrobialactiv

ity50

AUg

[131]

Zein

andsoyprotein

isolate(SPI)fi

lms

containing

greentea

extract(GTE

)

Zeamays

Glycinem

axCa

melliasin

ensis

Fried

Ediblefilm

(GC-WPI)w

ithGTE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

TBARS

colorm

icrobial

physicalattributes

GTE

1

[132]

Gelidium

corneum

(GC)

-Wheyprotein

isolate(G

C-WPI)

blendfilm

containing

grapefruitseed

extract(GSE

)

Gelidium

corneum

Citru

sparadisiBo

staurus

Not

mentio

ned

Ediblefilm

(GC-WPI)w

ithGSE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

Water

vapo

rpermeability

microbiologicalanalysis

sensory

attributes

GSE

01

[133]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 23

damage to the cell membrane and degradation of ribonucleicacids occurred in the high-pressure-treated cells Malickiet al investigated the use of high hydrostatic pressure toprolong the shelf-life of traditionallymanufactured fish-pastestored under refrigeration (4∘C) for 6 weeks [119] Neitherbacteria nor molds or yeasts were detected in the highhydrostatic pressure-treated fish-paste samples at any timepoint analyzed irrespective of the pressurization conditionsIn conclusion these studies revealed the effectiveness of highhydrostatic pressure to prolong the shelf-life of traditionallymanufactured fish-paste stored under refrigerated conditionsfor up to 6 weeks

Kim et al reported a reduction in the total aerobicbacterial counts in the grilled fish-paste stored at 5∘C andirradiated by gamma rays at a level of 25 kGy or more[120] Additionally the treatment of gamma rays at a levelof 75 KGy at 30∘C showed a significant inhibition in aerobicbacterial growth Cho et al investigated the effect of Co-60 gamma irradiation on fried fish-paste and studied thephysicochemical properties of fish-paste products stored atlow temperature (3 plusmn 1∘C) and room temperature (10ndash20∘C)[121] There was no obvious difference between the vacuum-and air-packed groupsThe irradiation of 3 KGy extended theshelf-life of fish-paste up to 2 times at room temperature and3-4 times at low temperature In both studies the irradiationtreatment caused very little textural degradation and no effecton the sensory characteristics of the samples was observed

Shin et al investigated the effects of chlorine dioxide(ClO2) treatment on the physiochemical andmicrobial prop-

erties of fish-paste products [122] After ClO2treatment

fish-paste samples were individually packed and stored at4∘C The pH and VBN values of fish-paste decreased withincreasing ClO

2concentration ClO

2treatment significantly

reduced the populations of total bacteria yeast and moldduring storage In particular treatment with 50 ppm ClO

2

significantly decreased the total bacterial count the mostamong all ClO

2-treated fish-pastes showing that 50 ppm

chlorine dioxide was the optimum concentration to prolongthe shelf-life of fish-paste products

42 Natural FoodAdditives Theuse of natural food preserva-tives rather than chemical and synthetic food preservatives isofworldwide interest It has been reported that several naturalfood additives could extend the shelf-life of cooked fish andfish products Some examples include onion ethanol extract[183] egg white lysozyme [125] grapefruit seed extract [126]chitosan hydrolysate [129] cinnamon bark extract [127] andred pepper extract [123] as well as mixtures of lysozymessodium hexametaphosphate and sodium pyrophosphate

The shelf-life of fried fish-paste products prepared byadding red pepper ethanol extract was estimated by Yoonet al [123] The shelf-life of the fried fish-paste with added10 red pepper ethanol extract and 5 chopped fresh redpepper was 2 to 3 days longer than that of the commercialfish-paste product thus demonstrating the most effectivepreservation effects According to Ahn et al the extractsof Eugenia caryophyllus Pinus rigida Bletilla striata andPaeonia albiflora exerted strong inhibitory effects on thegrowth of microorganisms isolated from putrefied fish-paste

[124] Notably the ethanol extract was more effective thanwater extract in all tested microorganisms The inhibitionlevel of each extract was evident at 2000 ppm ethanol in thefish-paste

Kim et al investigated the inhibitory effects of lysozymesmixtures of lysozymes and other antibacterial substancessuch as sodium pyrophosphate and sodium hexametaphos-phate on bacterial growth in surimi products [125] Thelysozymes inhibited growth in most of the tested isolatesand themixture of antibacterial substances showed increasedeffects compared with those when they were used individ-ually A mixture of 05 sodium hexametaphosphate 05sodium pyrophosphate and 005 lysozyme in imitationcrab and kamaboko showed the highest inhibitory activ-ity

The stabilizing effects of grapefruit seed extract on fish-paste products were investigated by Cho et al [126] Texturalproperties decreased with increasing storage period Thetreatment of fish products with grapefruit seed extract pro-longed the deterioration of fish-paste product proteins duringstorage up to 4-5 daysThe chemical sensory and rheologicalevaluation revealed that the grapefruit seed extract could beused as an effective additive to extend the shelf-life of fish-paste products

The predominant bacterium in most of the isolatedmicroorganisms from packed and unpacked spoiled fish-paste products is Bacillus sp [127] Notably yeast andmolds are not reported in the vacuum-packed products Ahydrolysate of alginic acid has antimicrobial activity but ithas not been used at industrial scale The alginic acid ata concentration of 03 prolonged shelf-life of fish-pasteproducts by 4 days at 15∘Cand inhibited the growth ofBacillussp isolated from fish-paste products [128] According to theresults of Cho et al the chitosan hydrolysate made withchitosanase from Aspergillus oryzae ATCC 22787 revealedthe strongest antimicrobial activity and inhibited the growthof Bacillus sp isolated from fish-paste products [129] Theaddition of chitosan hydrolysate at a concentration of 03resulted in extended shelf-life of up to 6 days at 15∘C Jeonget al reported that spraying cinnamon bark extract on thesurface of the fried fish-paste products could inhibit thegrowth of spoilage bacteria and mold at room temperatureand resulted in prolonged shelf-life [127]

Yamazaki et al investigated the effects of nisin andsucrose fatty acid esters on the growth of spoilage bacteria infish-paste products [130] Nisin exerted antibacterial activityagainst Bacillus subtilis and Bacillus licheniformis in a liquidmedium at 20∘C and resulted in a longer shelf-life forfish-paste products It was concluded that the addition ofnisin could be used as a potential alternative method toprevent spoilage caused by spore-forming bacteria in fish-paste productsThe bacteriocin produced byCarnobacteriummaltalomaticum had the ability to inhibit both Enterococcussp and Leuconostoc sp which reduce the shelf-life of fish-paste products during preservation [131] The results showedthat the purified bacteriocin piscicolin KH1 andor nisin sig-nificantly inhibited the growth of Leuconostoc mesenteroidesand Enterococcus faecium and could be used as a food-gradepreservative for kamaboko gels

24 Journal of Food Quality

Sakai and Yamaguchi examined the possibility of inhibit-ing lipid oxidation in boiled fish-paste by adding yuzu skinto the surimi [209] The heat-treated control kamabokoand yuzu skin-added kamaboko (citron kamaboko) wererefrigerated at 0∘C for 2 days and after heating the surimithe malonaldehyde content in both kamabokos was reducedThese results suggest that the addition of citron skin sup-pressed lipid oxidation in fish-paste products

Various packing materials and wrapping techniques havealso been employed to keep fish-paste products fresh and freeof contaminants for a longer period of time Lee et al investi-gated the processing conditions and quality stability of retortpouched fried-mackerel fish-paste during storage [210] Themackerel fish-paste was ground with added ingredients friedin soybean oil cooled vacuum-packed in a laminated plasticfilm and finally sterilized at 120∘C for 20min in a hotwater circulating retortThe reported method showed a goodpreservation for 100 days at 25 plusmn 3∘CThe sensory evaluationshowed no significant differences between the prepared fish-paste products and that of products in the market Ha et alexamined the optimum storage conditions for maintainingthe quality of the fried fish-paste in retort pouches [211]Both hardness and gel strength increased with increasingsterilization temperature On the other hand no differenceswere observed in elasticity and water-holding capacity

Lee et al elucidated the antioxidative effects of soyandor zein protein films containing green tea extract on thephysiological properties of fish-paste products during storage[132]The soy protein films showed an increase in yellownesswhile a decrease in yellowness was observed with the zeinfilms The lipid oxidation was retarded at day 2 of storageby wrapping the fried fish-paste products with soy and zeinprotein films containing green tea extract Lim et al prepareda Gelidium corneum whey protein isolate (GC-WPI) blendfilm containing grapefruit seed extract and studied the effectof this film on pathogenic bacterial inhibition during storage[133]TheGC-WPI blend was effective in decreasing the pop-ulations of Salmonella typhimurium Listeria monocytogenesand Escherichia coli on films treated with 01 grapefruitseed extract These studies suggest that packaging fish-pasteproducts in plant-based protein films containing green tea orgrapefruit seed extract could be beneficial to prolong shelf-life

5 Conclusion

The production of surimi dates back to ancient times How-ever advancement in surimi processing technology startedin 1960 with the discovery of cryoprotectants which werehelpful in maintaining the gel quality and functionality offish-paste for relatively longer periods of frozen storage [3]As themarket share of quality-conscious consumers rises thedemand for the use of natural additives rather than chemicalingredients for surimi products will continue to increaseAccording to Park et al the worldwide production of surimi-related products reached around 800000MT by 2011-2012while the main fish sources for surimi products includePacificwhitingAlaska pollock jackmackerel Atkamackerelsouthern blue whiting northern blue whiting and hoki [3]

Surimi is subdivided into high-grade (FA SA and A) andlow-grade (KA KB and RA) types based on the quality ofthe raw fish sources Most of the high-grade surimi is soldin Japan for the production of kamaboko and other high-quality surimi products and in Korea for the production ofpremium crabsticks Low-grade surimi is sold in Europe andthe United States for the manufacturing of crab sticks andin Korea and Japan for the preparation of other fried fishproducts [3] With the technological advancements in thesurimi processing industry it has been possible to use low-grade surimi for the production of fish cakes fish balls andother surimi products

With increasing demand and new processing techniques(eg the pH-shift method) the use of other seafoodresources such as small pelagic species and giant squid forthe production of surimi and surimi products was possible[212] Notably the production of surimi products is cheaperinKorea than elsewhere but industry professionals are alwayssearching for the most inexpensive surimi seafood sourcesHence the production of surimi from aquaculture fish suchas catfish and carp is growing in demand

Food additives from animal and seafood sources suchas fish chicken beef plasma proteins and egg white areconsidered the most effective protease inhibitors for surimiHowever with the outbreak of avian influenza mad cow dis-ease undesirable resulting characteristics and some religiousconstraints there is limited use of these food additives Addi-tionally vegetarians in some parts of the world would notwish to consume surimi-based products containing additivesderived from animals or even from seafood sources Hencethere is a need to identify more effective and alternative food-grade ingredients (eg plant sources seaweed and microal-gae) to be used in the preparation of fish-paste products

Surimi is mainly used for human consumption As suchthe challenges of production cost composition nutritionalvalue and the shelf-life of surimi products can never beneglected This review has provided an overview of nat-ural and synthetic food additives and preservatives usedto enhance the quality functionality and shelf-life of fish-paste products In addition the improvements in the fish-paste product quality and functionality by various foodadditives from seafood plants mushrooms animal sourcesand functional materials were discussed

For decades surimi and surimi-based products have beenwell known in East Asian countries such as Japan and KoreaHowever with advancements in technology they are attract-ing attention in other Asian as well as European countriesWith the increasing consumption worldwide the manufac-turing and processing of fish-paste products may requirenew and improved additives to enhance their acceptability inthe market Continuous scientific innovations and improvedprocessing technology will aid in further advancements andimprovements in this area

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article and regarding thefunding received

Journal of Food Quality 25

Authorsrsquo Contributions

Khawaja Muhammad Imran Bashir and Jin-Soo Kim con-tributed equally to this work

Acknowledgments

This research was a part of the Project no PJT200885entitled ldquoDevelopment andCommercialization of TraditionalSeafood Products Based on the Korean Coastal MarineResourcesrdquo funded by the Ministry of Oceans and FisheriesSouth Korea

References

[1] H-J Hwang S-Y Choi and S-C Lee ldquoPreparation andquality analysis of sodium-reduced fried fish cakesrdquo PreventiveNutrition and Food Science vol 18 no 3 pp 222ndash225 2013

[2] KFDA Food code Article 1-5-12 Korea Food and Drug Admin-istration Seoul Korea 2012

[3] J W Park H Nozaki T Suzuki and J-L Beliveau ldquoHistoricalreview of surimi technology and market developmentsrdquo inSurimi and Surimi seafood J W Park Ed pp 3ndash24 CRC PressNew York NY USA 2013

[4] J A Ramırez R Dıaz-Sobac O G Morales and M VazquezldquoEvaluation of freeze-dried surimi from tilapia and fat sleeper asemulsifiers [Evaluacion de surimi liofilizado de tilapia y dormi-dor como emulsificantes evaluacion de surimi liofilizado detilapia e dormidor como emulsificantes]rdquo Ciencia y TechnologiaAlimentaria vol 2 no 4 pp 210ndash214 1999

[5] J M Aguilera and D W Stanley ldquoFood structuringrdquo inMicrostructural Principles of Food Processing and Engineeringvol 12 p 246 AN Aspen Publishers Gaithersburg MarylandUSA 1999

[6] A P Stone and D W Stanley ldquoMechanisms of fish muscle gela-tionrdquo Food Research International vol 25 no 5 pp 381ndash3881992

[7] S Nakamura and M Ogawa ldquoBiomolecular strategies forpreparation of high quality surimi-based productsrdquo PreventiveNutrition and Food Science vol 10 no 2 pp 191ndash197 2005

[8] M Okada ldquoHistory of surimi technology in Japanrdquo in Surimitechnology T C Lanier and C M Lee Eds pp 3ndash22 MarcelDekker Inc New York NY USA 1992

[9] MIFAFF ldquoStatistics of fisheries processingrdquo Ministry of FoodAgriculture Forestry and Fisheries Seoul Korea 2011

[10] T C Lanier ldquoMeasurement of surimi composition and junc-tional propertiesrdquo in Surimi technology T C Lanier and C MLee Eds pp 123ndash166 Marcel Dekker Inc New York NY USA1992

[11] K-H Chung and C-M Lee ldquoRelationships between physico-chemical properties of nonfish protein and textural propertiesof protein-incorporated surimi gelrdquo Journal of Food Science vol55 pp 972ndash975 1990

[12] M TMorrissey JWWuD Lin andHAn ldquoProtease inhibitoreffects on torsionmeasurements and autolysis of Pacific whitingsurimirdquo Journal of Food Science vol 58 no 5 pp 1050ndash10541993

[13] J W Park ldquoFunctional protein additives in surimi gelsrdquo Journalof Food Science vol 59 no 3 pp 525ndash527 1994

[14] S Benjakul W Visessanguan and C Srivilai ldquoGel propertiesof bigeye snapper (Priacanthus tayenus) surimi as affected by

setting and porcine plasma proteinsrdquo Journal of Food Qualityvol 24 no 5 pp 453ndash471 2001

[15] D D Hamann P M Amato M C Wu and E A FoegedingldquoInhibition of modori (gel weakening) in surimi by plasmahydrolysate and egg whiterdquo Journal of Food Science vol 55 pp665ndash669 1990

[16] K D Reppond and J K Babbitt ldquoProtease inhibitors affectphysical properties of arrowtooth flounder and walleye pollocksurimirdquo Journal of Food Science vol 58 pp 96ndash98 1993

[17] V C Weerasinghe M T Morrissey and H An ldquoCharacteriza-tion of active components in food-grade proteinase inhibitorsfor surimi manufacturerdquo Journal of Agricultural and FoodChemistry vol 44 no 9 pp 2584ndash2590 1996

[18] C-Y Yang ldquoEffect of the addition of bovine plasma on thequality properties of steamed fish pasterdquo The Korean Journal ofFood and Nutrition vol 21 pp 518ndash523 2008

[19] K Duangmal and A Taluengphol ldquoEffect of protein additivessodium ascorbate and microbial transglutaminase on the tex-ture and colour of red tilapia surimi gelrdquo International Journalof Food Science amp Technology vol 45 no 1 pp 48ndash55 2010

[20] S BenjakulW Visessanguan and C Chantarasuwan ldquoEffect ofporcine plasma protein and setting on gel properties of surimiproduced from fish caught inThailandrdquo LWT- Food Science andTechnology vol 37 no 2 pp 177ndash185 2004

[21] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoCysteine proteinase inhibitor from chicken plasma Fractiona-tion characterization and autolysis inhibition of fish myofibril-lar proteinsrdquo Food Chemistry vol 101 no 4 pp 1647ndash1657 2007

[22] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoEffect of chicken plasma protein and some protein additiveson proteolysis and gel-forming ability of sardine (SardinellaGibbosa) surimirdquo Journal of Food Processing and Preservationvol 31 no 4 pp 492ndash516 2007

[23] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoRheological and textural properties of pacific whiting surimigels as influenced by chicken plasmardquo International Journal ofFood Properties vol 11 no 4 pp 820ndash832 2008

[24] M Sugiyama T Mishiro Y Tsukamasa T Suzuki and KTakama ldquoPuncture properties of kamaboko with ovomucoidpasteurized at several temperaturesrdquo Nippon Suisan Gakkaishivol 64 no 1 pp 76ndash81 1998

[25] M Sugiyama T Mishiro Y Tsukamasa et al ldquoPhysical prop-erties of Kamaboko with ovomucoid pasteurized at severaltemperaturesrdquo Nippon Suisan Gakkaishi vol 64 no 1 pp 82ndash87 1998

[26] J Yongsawatdigul and P Piyadhammaviboon ldquoInhibition ofautolytic activity of lizardfish surimi by proteinase inhibitorsrdquoFood Chemistry vol 87 no 3 pp 447ndash455 2004

[27] L Campo-Deano and C Tovar ldquoThe effect of egg albumen onthe viscoelasticity of crab sticks made from Alaska pollock andPacific whiting surimirdquo Food Hydrocolloids vol 23 no 7 pp1641ndash1646 2009

[28] A Hunt J W Park and A Handa ldquoEffect of various types ofegg white on characteristics and gelation of fish myofibrillarproteinsrdquo Journal of Food Science vol 74 no 9 pp C683ndashC6922009

[29] S Rawdkuen and S Benjakul ldquoWhey protein concentrateAutolysis inhibition and effects on the gel properties of surimiprepared from tropical fishrdquo Food Chemistry vol 106 no 3 pp1077ndash1084 2008

26 Journal of Food Quality

[30] Y Ruttanapornvareesakul K Somjit A Otsuka et al ldquoCry-oprotective effects of shrimp head protein hydrolysate on gelforming ability and protein denaturation of lizardfish surimiduring frozen storagerdquo Fisheries Science vol 72 no 2 pp 421ndash428 2006

[31] D K Li H Lin and SM Kim ldquoEffect of rainbow trout (Oncor-hynchus mykiss) plasma protein on the gelation of Alaska pol-lock (Theragra chalcogramma) surimirdquo Journal of Food Sciencevol 73 no 4 pp C227ndashC234 2008

[32] A Hernandez-Briones G Velazquez M Vazquez and J ARamırez ldquoEffects of adding fish gelatin onAlaska pollock surimigelsrdquo Food Hydrocolloids vol 23 no 8 pp 2446ndash2449 2009

[33] T Yin Z H Reed and J W Park ldquoGelling properties of surimias affected by the particle size of fish bonerdquo LWT- Food Scienceand Technology vol 58 no 2 pp 412ndash416 2014

[34] T Yin and J W Park ldquoTextural and rheological properties ofPacific whiting surimi as affected by nano-scaled fish bone andheating ratesrdquo Food Chemistry vol 180 pp 42ndash47 2015

[35] M R Fowler and J W Park ldquoEffect of salmon plasma proteinon Pacific whiting surimi gelation under various ohmic heatingconditionsrdquo LWT- Food Science and Technology vol 61 no 2pp 309ndash315 2015

[36] M R Fowler and J W Park ldquoSalmon blood plasma Effectiveinhibitor of protease-laden Pacific whiting surimi and salmonmincerdquo Food Chemistry vol 176 pp 448ndash454 2015

[37] S Klomklao S Benjakul H Kishimura K Osako and BK Simpson ldquoTrypsin inhibitor from yellowfin tuna (Thunnusalbacores) roe Effects on gel properties of surimi from bigeyesnapper (Priacanthus macracanthus)rdquo LWT- Food Science andTechnology vol 65 pp 122ndash127 2016

[38] N K Vate and S Benjakul ldquoEffect of the mixtures of squid inktyrosinase and tannic acid on properties of sardine surimi gelrdquoJournal of Food Science and Technology vol 53 no 1 pp 411ndash420 2016

[39] T Yamashita ldquoEffects of commercial soybean protein andwheat gluten as subsidiary materials on physical properties ofkamabokordquo Nippon Shokuhin Kogyo Gakkaishi vol 38 no 12pp 883ndash890 1991

[40] K H Chung and C M Lee ldquoFunction of nonfish proteins insurimi-based gel productsrdquo Korean Journal of Society of FoodScience vol 10 pp 146ndash150 1994

[41] K-H Chung and C-M Lee ldquoEvaluation of wheat gluten andmodified starches for their texture-modifying and freeze-thawstabilizing effects on surimi based-productsrdquo Journal of FoodScience and Nutrition pp 190ndash195 1996

[42] S Benjakul S Karoon and A Suwanno ldquoInhibitory effects oflegume seed extracts on fish proteinasesrdquo Journal of the Scienceof Food and Agriculture vol 79 no 13 pp 1875ndash1881 1999

[43] S Benjakul W Visessanguan and P Thummaratwasik ldquoInhi-bition of gel weakening of threadfin bream surimi using Thailegume seed proteinase inhibitorsrdquo Journal of Food Biochem-istry vol 24 no 5 pp 363ndash380 2000

[44] A Oujifard S Benjakul M Ahmad and J Seyfabadi ldquoEffect ofbambara groundnut protein isolate on autolysis and gel prop-erties of surimi from threadfin bream (Nemipterus bleekeri)rdquoLWT- Food Science and Technology vol 47 no 2 pp 261ndash2662012

[45] Y Luo RKuwaharaMKaneniwa YMurata andMYokoyamaldquoEffect of soy protein isolate on gel properties of Alaska pollockand common carp surimi at different setting conditionsrdquoJournal of the Science of Food and Agriculture vol 84 no 7 pp663ndash671 2004

[46] Y Luo H Shen D Pan and G Bu ldquoGel properties of surimifrom silver carp (Hypophthalmichthys molitrix) as affected byheat treatment and soy protein isolaterdquo Food Hydrocolloids vol22 no 8 pp 1513ndash1519 2008

[47] C Cardoso B Ribeiro and R Mendes ldquoEffects of dietary fibreandmicrobial transglutaminase addition on the rheological andtextural properties of protein gels from different fish speciesrdquoJournal of Food Engineering vol 113 no 4 pp 520ndash526 2012

[48] T Kudre S Benjakul and H Kishimura ldquoEffects of proteinisolates from black bean and mungbean on proteolysis and gelproperties of surimi from sardine (Sardinella albella)rdquo LWT-Food Science and Technology vol 50 no 2 pp 511ndash518 2013

[49] S Klomklao and S Benjakul ldquoEffect of trypsin inhibitor inadzuki bean (Vigna angularis) on proteolysis and gel propertiesof threadfin bream (Nemipterus bleekeri)rdquo LWT- Food Scienceand Technology vol 63 no 2 pp 906ndash911 2015

[50] S Konoo H Ogawa and N Iso ldquoEffects of addition of amyloseand amylopectin on the breaking strength of fish meat gelrdquoNippon Suisan Gakkaishi vol 64 no 1 pp 69ndash75 1998

[51] C-S Kong H Ogawa and N Iso ldquoRheological analysis of theeffect of gelatinization of starch added to fish-meat gel based onvolume changesrdquo Fisheries Science vol 65 no 6 pp 930ndash9361999

[52] B-Y Kim W-W Kim and B Yoo ldquoEffect of native and acety-lated sweet potato starch on rheological properties of compositesurimi solrdquo Journal of Food Science and Nutrition vol 13 no 3pp 245ndash248 2008

[53] B-J Yoo ldquoThe effects of alkaline treatment and potato-starchcontent on the quality of fishmeat paste products prepared fromPacific sandlance Ammodytes personatus Girardrdquo Fisheries andAquatic Sciences vol 14 no 3 pp 161ndash167 2011

[54] S M Cho M S Yoon and S-B Kim ldquoEffects of rice flourmilling types and addition methods on rheological and sensoryproperties of surimi productsrdquo Korean Journal of Fisheries andAquatic Sciences vol 46 no 2 pp 139ndash146 2013

[55] Y-M Kwon and J-S Lee ldquoA study on the quality characteristicsof fish cakes containing rice flourrdquo Korean Journal of HumanEcology vol 22 no 1 pp 189ndash200 2013

[56] M Yoon J-S Kim D Kim J Jo and S Cho ldquoOptimization ofthe processing conditions for the preparation of surimi productscontaining rice flourrdquo Fisheries and Aquatic Sciences vol 17 no2 pp 167ndash173 2014

[57] J A Ramırez M Barrera O G Morales and M VazquezldquoEffect of xanthan and locust bean gums on the gelling prop-erties of myofibrillar proteinrdquo Food Hydrocolloids vol 16 no 1pp 11ndash16 2002

[58] A M Barrera J A Ramırez J J Gonzalez-Cabriales and MVazquez ldquoEffect of pectins on the gelling properties of surimifrom silver carprdquo Food Hydrocolloids vol 16 no 5 pp 441ndash4472002

[59] S Benjakul W Visessanguan S Phatchrat and M TanakaldquoChitosan affects transglutaminase-induced surimi gelationrdquoJournal of Food Biochemistry vol 27 no 1 pp 53ndash66 2003

[60] M A Iglesias-Otero J Borderıas and C A Tovar ldquoUse ofKonjac glucomannan as additive to reinforce the gels from low-quality squid surimirdquo Journal of Food Engineering vol 101 no3 pp 281ndash288 2010

[61] S-H Eom J-A Kim B-Y Son et al ldquoEffects of carrageenanon the gelatinization of salt-based surimi gelsrdquo Fisheries andAquatic Sciences vol 16 no 3 pp 143ndash147 2013

Journal of Food Quality 27

[62] S H Choi and S M Kim ldquoQuality properties of giant squid(Dosidicus gigas) surimi-based product manufactured withAmorphophallus konjac flourrdquo Korean Journal of Food Scienceand Technology vol 44 no 4 pp 422ndash427 2012

[63] D Cando B Herranz A J Borderıas and H M MorenoldquoEffect of high pressure on reduced sodium chloride surimigelsrdquo Food Hydrocolloids vol 51 pp 176ndash187 2015

[64] D-S Kim and Y-H Park ldquoEffect of food humectants onlowering water activity of casing kamaboko 1 Effect of loweringwater activity of sodium chloride sugars and polyolsrdquo Bulletinof the Korean Fisheries Society vol 14 pp 139ndash147 1981

[65] D-S Kim and Y-H Park ldquoEffect of food humectant on lower-ingwater activity of casing kamaboko 2 Effect of loweringwateractivity of starch glycine and sodium lactate and prediction ofthe water activity lowing ability of humectantsrdquo Bulletin of theKorean Fisheries Society vol 15 pp 74ndash82 1982

[66] G L Sanchez Pascua M R Casales and M I Yeannes ldquoInflu-ence of water and glycerol contents on the aw of fish pastesrdquoJournal of Aquatic Food Product Technology vol 10 no 1 pp89ndash100 2001

[67] E Niwa K Tsujimoto and S Kanoh ldquoKamaboko gel-strength-ening effect of polyuronides and other polysaccharidesrdquoNipponSuisan Gakkaishi vol 58 pp 85ndash88 1992

[68] R Yoshinaka M Shiraishi and S Ikeda ldquoEffect of AscorbicAcid on theGel Formation of FishMeatrdquoBulletin of the JapaneseSociety for the Science of Fish vol 38 no 5 pp 511ndash515 1972

[69] H G Lee C M Lee K H Chung and S A Lavey ldquoSodiumascorbate affects surimi gel-forming propertiesrdquo Journal of FoodScience vol 57 pp 1343ndash1347 1992

[70] Y Park S D Kelleher D J McClements and E A DeckerldquoIncorporation and stabilization of omega-3 fatty acids insurimi made from cod Gadus morhuardquo Journal of Agriculturaland Food Chemistry vol 52 no 3 pp 597ndash601 2004

[71] E Okazaki Y Yamashita and Y Omura ldquoEmulsification of fishoil in surimi by high-speed mixing and improvement of gel-forming abilityrdquo Nippon Suisan Gakkaishi vol 68 no 4 pp547ndash553 2002

[72] H Fukushima E Okazaki S Noda and Y Fukuda ldquoChangesin physical properties water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oilrdquoNippon Shokuhin Kagaku Kogaku Kaishi vol 54 no 1 pp 39ndash44 2007

[73] B N Pietrowski R Tahergorabi and J Jaczynski ldquoDynamicrheology and thermal transitions of surimi seafood enhancedwith 120596-3-rich oilsrdquo Food Hydrocolloids vol 27 no 2 pp 384ndash389 2012

[74] A K Balange S Benjakul and S Maqsood ldquoGel strengtheningeffect of wood extract on surimi produced frommackerel storedin icerdquo Journal of Food Science vol 74 no 8 pp C619ndashC6272009

[75] N Buamard and S Benjakul ldquoImprovement of gel properties ofsardine (Sardinella albella) surimi using coconut husk extractsrdquoFood Hydrocolloids vol 51 pp 146ndash155 2015

[76] A K Balange and S Benjakul ldquoEffect of oxidised phenolic com-pounds on the gel property of mackerel (Rastrelliger kanagurta)surimirdquo LWT- Food Science and Technology vol 42 no 6 pp1059ndash1064 2009

[77] A Balange and S Benjakul ldquoEnhancement of gel strength ofbigeye snapper (Priacanthus tayenus) surimi using oxidisedphenolic compoundsrdquo Food Chemistry vol 113 no 1 pp 61ndash702009

[78] Y A Arfat and S Benjakul ldquoEffect of zinc sulphate on gellingproperties of phosphorylated protein isolate from yellow stripetrevallyrdquo Food Chemistry vol 141 no 3 pp 2848ndash2857 2013

[79] M-S Bae and S-C Lee ldquoQuality characteristics of fried fishpaste containing anchovy powderrdquo Journal of the Korean Societyof Food Science and Nutrition vol 36 no 9 pp 1188ndash1192 2007

[80] M-S Bae J-U Ha and S-C Lee ldquoQuality properties of highcalcium fish paste containing anchovyrdquo Korean Journal of Foodand Cookery Science vol 23 pp 561ndash566 2007

[81] H-S Cho and K-H Kim ldquoQuality characteristics of fish pastecontaining skate (Raja kenojei) powderrdquo Journal of the EastAsian Society of Dietary Life vol 21 pp 808ndash813 2011

[82] Y H Park E Y Bum E R Jeon and LH Jung ldquoEffect of addedskate (Raja kenojei) on the quality characteristics of steamedfishmeat pasterdquo Food Science and Biotechnology vol 23 no 5 pp1453ndash1458 2014

[83] S-M Park B-B Lee Y-M Hwang and S-C Lee ldquoQualityproperties of fish paste containing Styela clavardquo Journal of theKorean Society of Food Science and Nutrition vol 35 pp 908ndash911 2006

[84] S-Y Choi E-Y Choi K-E Lee A-S Song S-H Park and S-C Lee ldquoPreparation and quality analysis of fish paste containingStyela clava tunicrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 41 no 11 pp 1591ndash1595 2012

[85] S-M Park H-K Seo and S-C Lee ldquoPreparation and qualityproperties of fish paste containing Styela plicatardquo Journal of theKorean Society of Food and Nutrition vol 35 pp 1256ndash12592006

[86] J-S Seo and H-S Cho ldquoQuality characteristics of fish pastewith shrimp powderrdquo Korean Journal of Food Preservation vol19 pp 519ndash524 2012

[87] H-S Cho and K-H Kim ldquoQuality properties of fish pastecontaining green laver powderrdquo Journal of the Korean Societyof Food Culture vol 29 pp 421ndash427 2014

[88] I-D Park ldquoQuality characteristics of fish paste containingLagocephalus lunaris powderrdquo Journal of the Korean Society ofFood Culture vol 28 pp 657ndash663 2013

[89] I Park ldquoQuality properties of fish paste containingCapsosiphonfulvescens powderrdquo Journal of The Korean Society of FoodCulture vol 31 no 4 pp 357ndash363 2016

[90] B-M Kim J-H Jung M-J Jung D-S Kim J-Y Jun and I-H Jeong ldquoThe quality characteristics and processing of fishpaste containing red snow crabChionoecetes japonicus leg-meatpowderrdquo Korean Journal of Fisheries and Aquatic Sciences vol49 pp 1ndash6 2016

[91] Y-J Shin and G-S Park ldquoQuality characteristics of fish-pastecontaining mulberry leaf powderrdquo Journal of the East AsianSociety of Dietary Life vol 15 pp 738ndash745 2005

[92] Y-J Shin ldquoQuality characteristics of fish paste containing lotus(Nelumbo nucifera) leaf powderrdquo Korean Journal of Food andCookery Science vol 23 pp 947ndash953 2007

[93] A D Thorat V R Joshi A U Pagarkar and A K BalangeldquoMicrowave pasteursation of fish paste product-Kamabokowith Beetroot and Spinachrdquo Ecology Environment and Conser-vation vol 13 no 1 pp 113ndash118 2007

[94] M-O Yang and E-J Cho ldquoQuality properties of surimi withadded citrus fruitsrdquo Journal of East Asian Society of Dietary Lifevol 17 pp 58ndash63 2007

[95] F Alakhrash U Anyanwu and R Tahergorabi ldquoPhysicochemi-cal properties of Alaska pollock (Theragra chalcograma) surimigels with oat branrdquo LWT- Food Science and Technology vol 66pp 41ndash47 2016

28 Journal of Food Quality

[96] J-S Kim and G-I Byun ldquoMaking fish paste with yam (Dios-corea japonica Thumb) powder and its characteristicsrdquo KoreanJournal of Culinary Research vol 15 pp 57ndash69 2009

[97] Y-J Shin J A Lee and G-S Park ldquoa Quality characteristics offish pastes containing Lycii fructus powderrdquo Journal of the EastAsian Society of Dietary Life vol 18 pp 22ndash28 2008

[98] D-W Shim J Jiang J-H Kim et al ldquoEffects of size adjustedwith red ginseng powders on quality of fish pastesrdquo Journal ofthe Korean Society of Food Science and Nutrition vol 41 no 10pp 1448ndash1453 2012

[99] Y-J Shin J A Lee and G-S Park ldquoQuality characteristics offish paste containing Angelicae gigantis Radix powderrdquo KoreanJournal of Food and Cookery Science vol 24 pp 699ndash705 2008

[100] S Choi ldquoQuality characteristics of fish paste containing Cur-cuma longa L powderrdquo The Korean Journal of Food and Nutri-tion vol 25 no 4 pp 833ndash841 2012

[101] J-A Jang H-A Kim and S-K Choi ldquoQuality characteristicsof fish cake made with silver pomfret (Pampus argenteus) withadded wasabi powderrdquo Journal of the East Asian Society ofDietary Life vol 20 pp 103ndash112 2010

[102] Y-J Shin K-S Kim and G-S Park ldquoTexture and sensorycharacteristics of fish paste containing white Poria cocos wolfpowderrdquo Korean J Food Cookery Sci vol 25 pp 119ndash125 2009

[103] J-U Ha S-G Koo H-Y Lee Y-M Hwang and S-C LeeldquoPhysical properties of fish paste containing Agaricus bisporusrdquoKorean Journal of Food Science and Technology vol 33 pp 451ndash454 2001

[104] S-G Koo Y-K Ryu Y-M Hwang J-U Ha and S-C LeeldquoQuality properties of fish-paste containing enoki mushroom(Flammuilna velutipes)rdquo Journal of the Korean Society of FoodScience and Nutrition vol 30 pp 288ndash291 2001

[105] M-H Son S-Y Kim J-U Ha and S-C Lee ldquoTexture prop-erties of surimi gel containing shiitake mushroom (Lentinusedodes)rdquo Journal of the Korean Society of Food Science andNutrition vol 32 pp 859-853 2003

[106] S-Y Kim M-H Son J-U Ha and S-C Lee ldquoPreparationand characterization of fried surimi gel containing king oystermushroom (Pleurotus eryngii)rdquo Journal of the Korean Society ofFood Science and Nutrition vol 32 pp 855ndash858 2003

[107] S I Chung S Y Kim Y J Nam andM Y Kang ldquoDevelopmentof surimi gel from king oyster mushroom and cuttlefish meatpasterdquo Food Science and Biotechnology vol 19 no 1 pp 51ndash562010

[108] S K Jin J H Park and S J Hur ldquoEffect of substituting surimiwith spent laying hen meat on the physicochemical character-istics of fried fish pasterdquo Food and Bioprocess Technology vol 7no 3 pp 901ndash908 2014

[109] A Debusca R Tahergorabi S K Beamer K E Matak and JJaczynski ldquoPhysicochemical properties of surimi gels fortifiedwith dietary fiberrdquo Food Chemistry vol 148 pp 70ndash76 2014

[110] H-S Yook J-W Lee H-J Lee B-S Cha S-Y Lee and M-W Byun ldquoQuality properties of fish paste prepared with refineddietary fiber from ascidian (Halocynthia roretzi) tunicrdquo Journalof the Korean Society of Food Science and Nutrition vol 29 pp642ndash646 2000

[111] A Debusca R Tahergorabi S K Beamer S Partington andJ Jaczynski ldquoInteractions of dietary fibre and omega-3-rich oilwith protein in surimi gels developed with salt substituterdquo FoodChemistry vol 141 no 1 pp 201ndash208 2013

[112] C Sell S Beamer J Jaczynski and K E Matak ldquoSensorycharacteristics and storage quality indicators of surimi franks

nutritionally enhanced with omega-3 rich flaxseed oil andsalmon oilrdquo International Journal of Food Science amp Technologyvol 50 no 1 pp 210ndash217 2015

[113] T Chang C Wang X Wang L Shi H Yang and M CuildquoEffects of soybean oil moisture and setting on the textural andcolor properties of surimi gelsrdquo Journal of Food Quality vol 38no 1 pp 53ndash59 2015

[114] J-S Kim M-L Cho and M-S Heu ldquoQuality improvement ofheat-induced surimi gel using calcium powder of cuttle Sepiaesculenta bone treated with acetic acidrdquo Journal of the KoreanFisheries Society vol 36 pp 198ndash203 2003

[115] G-W Kim G-H Kim J-S Kim et al ldquoQuality characteristicsof fried fish paste of Alaska pollack meat paste added withpropolisrdquo Journal of the Korean Society of Food Science andNutrition vol 37 no 4 pp 485ndash489 2008

[116] G-W Kim G-H Kim J-S Kim et al ldquoQuality of fried fishpaste prepared with sand-lance (Hypoptychus dybowskii) meatand propolis additiverdquo Journal of the Korean Fisheries Societyvol 41 pp 170ndash175 2008

[117] B Park H Cho and S Park ldquoStudy on quality characteristicsof fish paste containing cheonggukjang powderrdquo Journal of TheKorean Society of Food Culture vol 30 no 2 pp 213ndash219 2015

[118] SMiyao T Shindoh KMiyamori and T Arita ldquoEffects of highpressurization on the growth of bacteria derived from surimi(fish paste)rdquo Nippon Shokuhin Kogyo Gakkaishi vol 40 pp478ndash484 1993

[119] A Malicki Z Sysak S Bruzewicz J Zrodłowska-Danek andM Szpak ldquoApplication of high hydrostatic pressure to extendthe shelf-life of traditionally produced fish pasterdquo MedycynaWeterynaryjna vol 66 pp 695ndash698 2010

[120] J-H Kim J-Y Jeon S-R Ryu et al ldquoMicrobial quality andphysiochemical changes of grilled fish paste in a group-mealservice affected by gamma-irradiationrdquo Korean Journal of FoodPreservation vol 11 pp 522ndash529 2004

[121] H-O Cho J-H Kwon M-W Byun and M-K Lee ldquoPreserva-tion of fried fish-paste by Irradiationrdquo Korean Journal of FoodScience and Technology vol 17 pp 474ndash481 1985

[122] H-Y Shin Y-J Lee I-Y Park J-Y Kim S-J Oh and K BSong ldquoEffect of chlorine dioxide treatment onmicrobial growthand qualities of fish paste during storagerdquo Journal of the KoreanSociety for Applied Biological Chemistry vol 50 pp 42ndash47 2007

[123] S S YoonH Kim YM Lee E J Jeong andY J Cha ldquoShelf-lifeextension effects of fish paste product by adding pepper extractrdquoin Proceedings of the Korean Nutrition Society Conference p 216Seoul Korea 2001

[124] E-S Ahn M-S Kim and D-H Shin ldquoScreening of natu-ral antimicrobial edible plant extract for dooboo fish pastemakkoli spoilage microorganismrdquo Korean Journal of FoodScience and Technology vol 26 pp 733ndash739 1994

[125] Y-M Kim B-H Lee S-H Lee I-S Shin and T-S LeeldquoThe preservative effect of egg white lysozyme added surimiproductsrdquo Bulletin of the Korean Fisheries Society vol 21 pp269ndash275 1988

[126] S-H Cho I-S Joo I-W Seo and Z-W Kim ldquoPreservativeeffect of grapefruit seed extract on fish meat productrdquo Journalof Food Hygiene and Safety vol 6 pp 67ndash72 1991

[127] E-T Jeong M-Y Park E-W Lee U-T Park and D-S ChangldquoAntimicrobial characteristics against spoilage microorganismsand food preservative effect of cinnamon (Cinnamomum cassiaBlume) bark extractrdquo Korean Journal of Life Science vol 8 pp648ndash653 1998

Journal of Food Quality 29

[128] D-S Chang H-R Cho H-S Lee M-Y Park and S-M LimldquoDevelopment of alginic acid hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 823ndash826 1998

[129] H-R Cho D-S Chang W-D Lee E-T Jeong and E-WLee ldquoUtilization of chitosan hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 817ndash822 1998

[130] K Yamazaki T Tashiro S Shirahama J-Y Jun and Y KawaildquoGrowth inhibition of spore-forming bacteria in fish-pasteproducts by Nisinrdquo Nippon Shokuhin Kagaku Kogaku Kaishivol 61 no 2 pp 70ndash76 2014

[131] K Hashimoto M L Bari Y Inatsu S Kawamoto and J ShimaldquoBiopreservation of kamaboko (steamed surimi) using pisci-colin KH1 produced by Carnobacteriummaltalomaticum KH1rdquoJapanese Journal of FoodMicrobiology vol 28 pp 193ndash200 2011

[132] S H Lee M S Lee S K Park D H Bae S D Ha and K BSong ldquoPhysical properties of protein films containing green teaextract and its antioxidant effect on fish paste productsrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1063ndash1067 2004

[133] G-O Lim Y-H Hong and K B Song ldquoIncorporating grape-fruit seed extract into Gelidium corneum-whey protein isolateblend packaging film increases the shelf life of fish paste -Research noterdquo Journal of Food Science and Nutrition vol 13no 4 pp 370ndash374 2008

[134] T C Lanier J Yongsawatdigul and P Carvajal-RondanellildquoSurimi gelation chemistryrdquo in Surimi and Surimi Seafood J WPark Ed pp 101ndash139Marcel Dekker NewYork NYUSA 2013

[135] M Kinoshita H Toyohara and Y Shimizu ldquoPurification andproperties of a novel latent proteinase showing myosin heavychain-degrading activity from threadfin-bream musclerdquo TheJournal of Biochemistry vol 107 no 4 pp 587ndash591 1990

[136] D H Wasson J K Babbitt and J S French ldquoCharacterizationof a heat stable protease from arrowtooth flounder Atheresthesstomiasrdquo Journal of Aquatic Food Product Technology vol 1 no3-4 pp 167ndash182 1993

[137] T A Seymour M T Morrissey M Y Peters and H An ldquoPuri-fication and characterization of pacific whiting proteasesrdquoJournal of Agricultural and Food Chemistry vol 42 no 11 pp2421ndash2427 1994

[138] H An V Weerasinghe T A Seymour and M T MorrisseyldquoCathepsin degradation of Pacific whiting surimi proteinrdquoJournal of Food Science vol 59 pp 1013ndash1017 1994

[139] AFDF Ground fish quality chart Alaska fisheries departmentfoundation Anchorage Alaska 1992

[140] G Sylvia S Larkin and M T Morrissey ldquoQuality and resourcemanagement bioeconomic analysis of the Pacific whitingindustryrdquo in Recent Advances inMarine Science and TechnologyO Bellwood H Choat and N Saxena Eds James CookUniversity Townsville QS Australia 1994

[141] S H Choi and S M Kim ldquoDevelopment of giant squid(Ommastrephes bartrami) surimi-based products with gel tex-ture enhancers and the effects of setting on gel qualityrdquo Journalof the Korean Society of Food Science and Nutrition vol 41 no7 pp 975ndash981 2012

[142] J A Ramırez R M Uresti G Velazquez and M VazquezldquoFood hydrocolloids as additives to improve the mechanicaland functional properties of fish products A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1842ndash1852 2011

[143] S-K Kim H-G Byun P-J Park and F Shahidi ldquoAngiotensinI converting enzyme inhibitory peptides purified from bovine

skin gelatin hydrolysaterdquo Journal of Agricultural and FoodChemistry vol 49 no 6 pp 2992ndash2997 2001

[144] I Kimura M Sugimoto K Toyoda N Seki K-I Arai andT Fujita ldquoA study on the cross-links reaction of myosin inkamaboko rsquosuwarirsquo gelsrdquo Nippon Suisan Gakkaisi vol 57 pp1386ndash1396 1991

[145] H An M Y Peters and T A Seymour ldquoRoles of endogenousenzymes in surimi gelationrdquo Trends in Food Science amp Technol-ogy vol 7 no 10 pp 321ndash327 1996

[146] R Nopianti N Huda andN Ismail ldquoA review on the loss of thefunctional properties of proteins during frozen storage and theimprovement of gel-forming properties of Surimirdquo AmericanJournal of Food Technology vol 6 no 1 pp 19ndash30 2011

[147] A M Martın-Sanchez C Navarro J A Perez-Alvarez and VKuri ldquoAlternatives for efficient and sustainable production ofsurimi A reviewrdquo Comprehensive Reviews in Food Science andFood Safety vol 8 no 4 pp 359ndash374 2009

[148] Korea Agro-Fisheries and Food Trade Corporation Processedfood segmented market survey-fish cake market Korea Agro-Fisheries and Food Trade Corporation Seoul Korea 2014

[149] D Kraft and A DerMarderosian The A-Z guide to food asmedicine CRC Press Boca Raton Fla USA 2016

[150] C V Morr and E A Foegeding ldquoComposition and function-ality of commercial whey and milk protein concentrates andisolates a status reportrdquo Food Technology vol 44 pp 100ndash1121990

[151] A Saiga T Okumura T Makihara et al ldquoAngiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chickenbreast muscle extractrdquo Journal of Agricultural and Food Chem-istry vol 51 no 6 pp 1741ndash1745 2003

[152] B Li F Chen X Wang B Ji and Y Wu ldquoIsolation and iden-tification of antioxidative peptides from porcine collagenhydrolysate by consecutive chromatography and electrosprayionization-mass spectrometryrdquo Food Chemistry vol 102 no 4pp 1135ndash1143 2007

[153] A Trampuz R M Prabhu T F Smith and L M BaddourldquoAvian Influenza A New Pandemic Threatrdquo Mayo ClinicProceedings vol 79 no 4 pp 523ndash530 2004

[154] M C Gomez-Guillen B Gimenez M E Lopez-Caballeroand M P Montero ldquoFunctional and bioactive properties ofcollagen and gelatin from alternative sources A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1813ndash1827 2011

[155] D Li X Fu and S M Kim ldquoProduction of chum salmoncystatin from the recombinant Saccharomyces cerevisiae opti-mized using response surface methodologyrdquo Biotechnology andBioprocess Engineering vol 15 no 2 pp 314ndash323 2010

[156] H Akazawa Y Miyauchi K Sakurada H Wasson and K DReppond ldquoEvaluation of protease inhibitors in Pacific whitingsurimirdquo Journal of Aquatic Food Product Technology vol 2 no3 pp 79ndash95 1994

[157] A Hunt K J K Getty and J W Park ldquoRoles of starch in surimiseafood A reviewrdquo Food Reviews International vol 25 no 4 pp299ndash312 2009

[158] T Suzuki Fish and Krill Protein Processing Technology AppliedScience Publishers London UK 1981

[159] C M Lee ldquoSurimi process technologyrdquo Food Technology vol38 pp 69ndash80 1984

[160] M C Wu D D Hamann and T C Lanier ldquoRheological andcalorimetric investigations of starch-fish protein systems duringthermal processingrdquo Journal of Texture Studies vol 16 pp 53ndash74 1985

30 Journal of Food Quality

[161] M C Wu T C Lanier and D D Hamann ldquoRigidity and vis-cosity changes of croaker actomyosin during thermal gelationrdquoJournal of Food Science vol 50 no 1 pp 14ndash19 1985

[162] S-K Kim S-T Yang and E-H Lee ldquoThe starch content of fish-paste products onmarketrdquo Journal of the Korean Society of FoodScience and Nutrition vol 7 pp 41-42 1978

[163] G AMacDonald T C Lanier and P A Caruajal ldquoStabilizationof protein in surimirdquo in Surimi and Surimi Seafood J W ParkEd pp 91ndash125 Marcel Dekker Inc New York NY USA 2000

[164] J A Ramırez I A Santos O G Morales M T Morrisseyand M Vazquez ldquoApplication of microbial transglutaminaseto improve mechanical properties of surimi from silver carputilizacionde transglutaminasa microbiana paramellora-las-propiedades mecanicas de surimide carpaplateada utiliza-cionde transglutaminasamicrobiana paramejorarlaspropieda-des mecanicas de surimide carpaplateadardquo Ciencia y TecnologıaAlimentaria vol 3 no 1 pp 21ndash28 2000

[165] M C Gomez-Guillen A J Borderıas and P MonteroldquoSalt nonmuscle proteins and hydrocolloids affecting rigiditychanges during gelation of giant squid (Dosidicus gigas)rdquoJournal of Agricultural and Food Chemistry vol 45 no 3 pp616ndash621 1997

[166] J W Park ldquoIngredient technology and formulation develop-mentrdquo in Surimi and Surimi Seafood J W Park Ed pp 91ndash125Marcel Dekker Inc New York NY USA 2000

[167] F Garcıa-Ochoa V E Santos J A Casas and E Gomez ldquoXan-than gum production recovery and propertiesrdquo BiotechnologyAdvances vol 18 no 7 pp 549ndash579 2000

[168] A I Rodrıguez-Hernandez and A Tecante ldquoDynamic vis-coelastic behavior of gellan- 120580 -carrageenan and gellan-xanthangelsrdquo Food Hydrocolloids vol 13 no 1 pp 59ndash64 1999

[169] J A Casas and F Garcıa-Ochoa ldquoSophorolipid production byCandida bombicola Medium composition and culture meth-odsrdquo Journal of Bioscience and Bioengineering vol 88 no 5 pp488ndash494 1999

[170] H J Lim ldquoA study on the calcium and sodium intakes andurinary calcium excretion of preschool children in BusanrdquoKorean Journal of Nutrition vol 34 pp 786ndash796 2001

[171] WHO ldquoDiet nutrition and the prevention of chronic diseasesReport of a joint WHOFAO expert consultationrdquo Tech RepWHO World Health Organization Geneva Switzerland 2003

[172] L K Dahl ldquoPossible role of salt intake in the development ofessential hypertensionrdquo International Journal of Epidemiologyvol 34 no 5 pp 967ndash972 2005

[173] H-K Jeong D-S Kim S-J Chun K-S Jo and Y-H ParkldquoEffect of food humectant on lowering water activity of casingKamaboko 3rdquo Bulletin of the Korean Fisheries Society vol 16 pp88ndash96 1983

[174] J Han E Kim M Cheong S Chee and K Chee ldquoBioavailabil-ity and digestibility of organic calcium sources by bone healthindexrdquo Journal of Nutrition and Health vol 43 no 1 pp 12ndash252010

[175] M K Lee ldquoA study of the bio-functional evaluation of Rajaskates caught in Huksando areardquo Journal of the Kwangju HealthCollege vol 21 pp 253ndash265 1996

[176] S H Cho Extraction and characterization of gelatin andantimicrobial peptide from skate (Raja kenojei) skins ChonnamNational University Gwangju Korea 2003

[177] J H Choi ldquoIsolation and purification of in chondroitin sulfatefrom skate cartilagerdquo Tech Rep Pukyong National UniversityBusan Korea 2004

[178] Y G Jo ldquoThe sterol composition of Styela clavardquo Journal of theKorean Fisheries Society vol 11 pp 97ndash101 1978

[179] S H Ahn ldquoExtraction of glycosaminoglycans from Styela clavatunicrdquo Biotechnology and Bioprocess Engineering vol 18 pp180ndash185 2003

[180] J J Kim S J Kim S H Kim H R Park and S C LeeldquoAntioxidant and anticancer activities of extracts from Styelaclava according to the processing methods and solventsrdquoJournal of the Korean Society of Food Science and Nutrition vol35 pp 278ndash283 2006

[181] T Aoki K Takata and N Kunisaki ldquoComparison of nutrientcomponents of six species of wild and cultured fishesrdquo Bulletinof the Japanese Society for the Science of Fish vol 57 pp 1927ndash1934 1991

[182] Committee Donguibogam Translated Donguibogam Bubin-munwha Press Seoul Korea 1999

[183] Y-K Park H-J Kim and M-H Kim ldquoQuality characteristicsof fried fish paste added with ethanol extract of onionrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1049ndash1055 2004

[184] G L Dong J J Hyun and E-R Woo ldquoAntimicrobial prop-erty of (+)-lyoniresinol-3120572-O-120573-D- glucopyranoside isolatedfrom the root bark of Lycium chinense Miller against humanpathogenic microorganismsrdquo Archives of Pharmacal Researchvol 28 no 9 pp 1031ndash1036 2005

[185] C C Wang S C Chang B S Inbaraj and B H ChenldquoIsolation of carotenoids flavonoids and polysaccharides fromLycium barbarum L and evaluation of antioxidant activityrdquoFood Chemistry vol 120 no 1 pp 184ndash192 2010

[186] Z Zhang X Liu T Wu et al ldquoSelective suppression of cervicalcancer Hela cells by 2-O-120573-d- glucopyranosyl-l-ascorbic acidisolated from the fruit of Lycium barbarum Lrdquo Cell Biology andToxicology vol 27 no 2 pp 107ndash121 2011

[187] J S Kil M G Kim H M Choi et al ldquoInhibitory effects ofAngelicae GigantisRadix on osteoclast formationrdquo PhytotherapyResearch vol 22 no 4 pp 472ndash476 2008

[188] ANiranjan andD Prakash ldquoChemical constituents and biolog-ical activities of turmeric (Curcuma longa L) - a reviewrdquo Journalof Food Science and Technology vol 45 pp 109ndash116 2008

[189] K S Kim M G Choung and S H Park ldquoQuantitativedetermination and stability of curcuminoid pigments fromturmeric (Curcuma longaL) rootrdquo Korean Journal of CropScience vol 50 pp 211ndash215 2005

[190] I S Shin and J M Lee ldquoStudy on antimicrobial and antimuta-genic activity of horseradish (Wasabia japonica) root extractsrdquoJournal of the Korean Fisheries Society vol 31 pp 835ndash841 1998

[191] Y J ChoA study on the antioxidative and antimicrobial activitiesof wasabi (Wasabia koreana Cruciferae) extracts [PhD thesis]Sungshin Womens University Seoul Korea 2008

[192] A-S Kang T-S Kang H-R Shon et al ldquoStudies on improve-ment of artificial cultivation and antioxidative activity of Poriacocosrdquo The Korean Journal of Mycology vol 27 pp 378ndash3801999

[193] J-H Lee Y J Lee J-K Shin et al ldquoEffects of triterpenoidsfrom Poria cocos Wolf on the serotonin type 3A receptor-mediated ion current in Xenopus oocytesrdquo European Journal ofPharmacology vol 615 no 1ndash3 pp 27ndash32 2009

[194] K R Im M J Kim T K Jung and K S Yoon ldquoAnalysisof isoflavonoid contents in Astragalus membranaceus Bungecultivated in different areas and at various agesrdquo The KoreanSociety for Biotechnology and Bioengineering vol 25 pp 271ndash276 2010

Journal of Food Quality 31

[195] Y E Lee and S H Hong Oriental Medicine Food MaterialsKyomunsa Seoul Korea 2003

[196] D H Kim ldquoQuality characteristics of fish paste prepared withAstragalus membranaceus powderrdquo Food Engineering Progressvol 15 pp 362ndash369 2011

[197] S-E Kim B S Hwang J-G Song S W Lee I-K Lee andB-S Yun ldquoNew bioactive compounds from Korean nativemushroomsrdquoMycobiology vol 41 no 4 pp 171ndash176 2013

[198] National Institute of Agricultural Science The Mushrooms inKorea Dongbang Media Co Ltd Seoul Korea 2004

[199] Y-J Gao M Zhang and W-P Chen ldquoStudy on processing offish paste with waste of grass carprdquo Journal of Food Science andBiotechnology vol 31 pp 1031ndash1038 2012

[200] S Tolasa C M Lee and S Cakli ldquoPhysical and oxidativestabilization of omega-3 fatty acids in surimi gelsrdquo Journal ofFood Science vol 75 no 3 pp C305ndashC310 2010

[201] B N Pietrowski R Tahergorabi K E Matak J C Tou andJ Jaczynski ldquoChemical properties of surimi seafood nutrifiedwith 120596-3 rich oilsrdquo Food Chemistry vol 129 no 3 pp 912ndash9192011

[202] S H Kim J L Yang and Y S Song ldquoPhysiological function ofcheonggukjangrdquo Food Industry and Nutrition vol 4 pp 40ndash461999

[203] R Walker ldquoToxicology of sorbic acid and sorbatesrdquo Food Addi-tives amp Contaminants Part A vol 7 no 5 pp 671ndash676 1990

[204] B R Thakur and T R Patel ldquoSorbates in fish and fish productsmdasha reviewrdquo Food Reviews International vol 10 no 1 pp 93ndash1071994

[205] C-Y Wang H-W Huang C-P Hsu and B B Yang ldquoRecentadvances in food processing using high hydrostatic pressuretechnologyrdquo Critical Reviews in Food Science and Nutrition vol56 no 4 pp 527ndash540 2016

[206] J H Kwon M W Byun and J S Kim ldquoMicrobiological andorganoleptic qualities of boiled-dried anchovies during post-irradiation periodrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 25 pp 283ndash287 1996

[207] J Noh and J H Kwon ldquoThe quality and thermoluminescenceproperties of dried pollack during storage following irradia-tionrdquo Korean Journal of Food Science and Technology vol 36pp 711ndash716 2004

[208] I Tukenmez M S Ersen A T Bakioglu A Bicer and VPamuk ldquoDose dependent oxidation kinetics of lipids in fish dur-ing irradiation processingrdquo Radiation Physics and Chemistryvol 50 no 4 pp 407ndash414 1997

[209] T Sakai and T Yamaguchi ldquoEffects of yuzu peel addition onthe lipid oxidation in kamaboko Effects of yuzu peel additionon the lipid oxidation in kamabokordquo Bulletin of the Faculty ofAgriculture Miyazaki University vol 57 pp 101-102 2011

[210] E-H Lee K-S Oh J-G Koo H-S Park S-Y Cho and Y-J Cha ldquoStudies on processing and keeping quality of retortpouched foods (3) Preparation and keeping quality of retortpouched fried mackerel meat pasterdquo Bulletin of the KoreanFisheries Society vol 17 pp 373ndash382 1984

[211] J-H Ha E-H Lee J-S Kim S-G Ji and J-G Koo ldquoA study onthe thermal treatment conditions of retort pouched fried fish-paste 1 Influence of thermal treatment conditions on qualityrdquoBulletin of the Korean Fisheries Society vol 20 pp 573ndash581 1987

[212] P Guenneugues and J Ianelli ldquoSurimi resources and marketrdquoin Surimi and surimi seafood J W Park Ed pp 25ndash53 MarcelDekker Inc New York NY USA 2013

Research ArticleDevelopment of a Chemically Defined Medium forBetter Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31

Wenli Liu12 Lanwei Zhang23 and Huaxi Yi3

1College of Chemistry and Environmental Engineering Shenzhen University Shenzhen Guangdong 518060 China2School of Food Science amp Technology Harbin Institute of Technology 73 HuangHe Avenue Harbin Heilongjiang 150090 China3College of Food Science and Engineering Ocean University of China Yushan Road 5 Qingdao Shandong 266100 China

Correspondence should be addressed to Lanwei Zhang zhanglwhiteducn and Huaxi Yi yihxouceducn

Received 31 March 2017 Revised 17 July 2017 Accepted 2 August 2017 Published 6 September 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Wenli Liu et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The macro- and micronutrients in traditional medium such as MRS used for cultivating lactic acid bacteria especially forbacteriocin production have not been defined preventing the quantitative monitoring of metabolic flux during bacteriocinbiosynthesis To enhance Enterocin Y31 production and simplify steps of separation and purification we developed a simplifiedchemically definedmedium (SDM) for the growth of Enterococcus faeciumY31 and production of its bacteriocin Enterocin Y31Wefound that the bacterial growthwas unrelated toEnterocinY31 production inMRS therefore both the growth rate and theEnterocinY31 production were set as the index for investigation Single omission experiments revealed that 5 gL NaCl five vitamins twonucleic acid basesMgSO

4sdot7H2OMnSO

4sdot4H2OKH

2PO4 K2HPO4 CH3COONa fourteen amino acids and glucosewere essential

for the strainrsquos growth and Enterocin Y31 production Thus a novel simplified and defined medium (SDM) was formulated with30 components in total Consequently Enterocin Y31 production yield was higher in SDM as compared to either MRS or CDMSDM improved the Enterocin Y31 production and simplified the steps of purification (only two steps) which has broad potentialapplications

1 Introduction

Bacteriocins are ribosomally synthesised antimicrobial pro-teins or protein complexes that inhibit other bacteria andthey either have a narrow antimicrobial spectrum (againstthe same species) or broad antimicrobial spectrum (againstacross genera) [1 2] Bacteriocin produced by lactic acidbacteria (LAB) is generally regarded as safe (GRAS) andQualified Presumption of Safety (QPS) status [3 4] andit is a desirable trait as a food additive for extending theshelf-life of the fermented food and controlling the safetyof foods [5 6] Based on their molecular structure bac-teriocins can be divided into four groups class I bacte-riocins contain posttranslational modifications (lantibioticsand molecular weight le 5 kDa) class II bacteriocins areunmodified and include small heat-stable nonlanthionine-containing peptides [7] The third class includes large

heat-labile bacteriocins Finally the fourth class comprisescomplex bacteriocins containing a protein moiety with oneor more other lipids or carbohydrates [8] Most bacteriocinsproduced by the Enterococcus faecium group of LAB are classII bacteriocins One subgroup class IIa contains bacteriocinswith certain sequence motifs in their N-terminal halves andis active against the food pathogen Listeria monocytogenes[9] Class IIa bacteriocins have become a focus of researchowing to their low molecular weight good dispersity andhigh thermostability This is also a case of Enterocin Y31produced by E faecium Y31 in the current work [10]

Enterocin Y31 is a class IIa bacteriocin produced byE faecium Y31 [11] Previous research results showed thatEnterocin Y31 had broad spectrum inhibition activity againstBacillus subtilis ATCC 6633 Escherichia coli ATCC 25922Listeria monocytogenes ATCC 19111 Bacillus cereus CICC20463 Staphylococcus aureus and Salmonella enterica serovar

HindawiJournal of Food QualityVolume 2017 Article ID 9017452 8 pageshttpsdoiorg10115520179017452

2 Journal of Food Quality

TyphimuriumATCC 14028The isoelectric point of EnterocinY31 was 825 it was stable in both acidity and alkalescenceconditions hence Enterocin Y31 has a broad applicationprospect (not published) However two main drawbacks ofEnterocin Y31 with regard to application in foods are asfollows (1) bacteriocins are secreted in very small quan-tities in the production media and (2) the media used togrow the bacteriocin-producing strains are very complex[12] as the LAB are fastidious organisms requiring aminoacids B vitamins and various minerals for their growthThese components are normally provided by sources such assoybean meal yeast extract and meat extract All of thesesources contain proteins and peptides as sources of aminoacids which are often very closely related to the bacteriocinproduced Therefore purification of bacteriocin from sucha complex medium requires a series of steps At each stepthere is some loss and sometimes after the final purificationthe antimicrobial activity may be completely lost Complexmedia do not allow the examination of all individual mediumfactors [13 14] affecting bacteriocin production

Ricciardi reported a modified chemically defined med-ium to promote the growth of Lactobacillus casei and Lacto-bacillus plantarum groups [15] In the present study weimproved the chemically defined medium to improve theyield of Enterocin Y31 produced by E faecium Y31 Thereare four objectives of this study (1) to develop a newand improved production method for Enterocin Y31 (pro-duced by E faecium Y31) (2) to determine the macro- andmicronutrients necessary for cultivating E faecium Y31 andimproving Enterocin Y31 production (3) to develop a noveland simple separation and purificationmethod for EnterocinY31 (avoiding a series of chromatography steps and the lossof Enterocin Y31 activity) and (4) to compare Enterocin Y31production in a defined medium with that in a complexmediumThis is feasible using a completely defined mediumand a minimal medium for bacteriocin production can thusbe established

2 Materials and Methods

21 Strains and Growth Conditions The bacteriocin-pro-ducer strain E faecium Y31 isolated from Chinese traditionalfermented foods (fermented vegetable juice from Lanzhou)was previously found to produce class IIa bacteriocin [10]which wasmaintained as stock cultures inMRSmediumwith18 glycerol at minus80∘C

Escherichia coli ATCC 25922 was selected as a sensitivestrain for antimicrobial activity assays because the bacte-riocin produced by E faecium Y31 has the highest activityagainst E coli ATCC 25922 in gram-negative bacteria

22 Medium The growth of E faecium Y31 and productionof Enterocin Y31 in a defined medium in a fermenter werecompared with those in MRS (reference medium) used forthe optimisation of the growth of E faecium Y31 and theproduction of Enterocin Y31 This medium CDM consistedof 44 components described by Khan et al [12] (listed inTable 1) All chemicals used for the preparation of the definedmedium were of analytical grade and obtained from either

Sigma-Aldrich (St Louis MO USA) or BDH ChemicalsLtd (Poole UK) For all the experiments aqueous stocksolutions of the individual components were prepared inthe appropriate concentrations and sterilized by autoclav-ing with the exception of the heat-sensitive componentsThe heat-sensitive amino acids (asparagine glutamine andtryptophan) all of the B vitamins and FeSO

4were filter-

sterilized (pore size 022120583m membrane Millipore CorpBillerica MA USA) All the stock solutions were then storedat 4∘C except FeSO

4which was freshly prepared before each

experiment because it is prone to oxidation during storage Inaddition to the defined medium MRS medium was used asa reference for comparison with the defined medium beforeeach experiment

23 Determination of the Antimicrobial Activity of EnterocinY31 The antimicrobial activity of bacteriocin was monitoredusing the agar well diffusion assay (AWDA) as describedpreviously [16] with some modifications E faecium Y31 wascultured for two or three generations and then the cell-free supernatants (CFSs) of E faecium Y31 were preparedby centrifuging for 30min at 10000timesg Aliquots (80 120583L) ofthe cell-free supernatants (CFSs) of E faecium Y31 wereadded to the wells (6mm diameter) on double-layer agarplates previously inoculated with 02mL overnight cultureof the indicator strain E coli ATCC 25922 Plates were keptstatic at room temperature for 3 h to allow diffusion of theCFSs evenly in the agar and then the plates were incubatedfor 24 h at 37∘C The bacteriocin titre was determined byeliminating the effect of the organic acid eliminating theeffect of H

2O2 and protease verificationThe diameter of the

zone of inhibition (not including the wells) was measuredusing a Vernier caliper An arbitrary unit (AUmL) wasdefined as the reciprocal of the highest dilution that producedan inhibition zone Specific activity was expressed as that unitper milligram of protein

24 Protein Concentration Determination Protein concen-tration was determined by the BCA (bicinchoninic acid)microassay method (Pierce Rockford IL USA) [17]

25 Monitoring of the Growth of E faecium Y31 The ODvalue of the fermentation liquid of E faecium Y31 wasmonitored with UV spectrophotometry at 600 nm each hourSterile culture medium was used as blanks to subtract thebackground value Samples having an OD600 nm value ofmore than 07 were diluted with the sterile culture mediumand the corrected OD value was obtained by multiplying thedilution factor ODmax (600 nm) represents the maximumOD value of the growth of E faecium Y31 ODmax (600 nm)was calculated before any centrifugation

26 Determination of the Relative Growth Rate The relativegrowth rate was calculated according to Monod [18] Thefollowing equation was used to calculate the growth rate

120583 = [(lnOD2minus lnOD

1) divide (1199052minus 1199051)] divide 120583CDM (1)

where 120583 is the relative growth rate (hminus1) ln is the symbol fornatural logarithm and OD

1and OD

2are the corrected OD

Journal of Food Quality 3

Table 1 Composition of CDM and SDMmedium

Constituent ContentCDM SDM

Amino acids (g Lminus1)L-Asparagine 100 100L-Aspartic acid 100 mdashL-Glutamic acid 100 100L -Glutamine 100 mdashL-Cys 100 100L-Alanine 100 mdashL-Arginine 100 100Glycine 100 100L-Histidine 100 100L-Isoleucine 100 100L-Leucine 100 100L-Lysine 100 100L-Methionine 100 100L-Phenylalanine 100 100L-Proline 100 mdashL-Serine 100 100L-Threonine 100 100L-Tryptophan 100 100L-Tyrosine 100 mdashL-Valine 100 mdash

Nucleic acid bases (g Lminus1)AdemomeSO

4002 002

Guanine 002 mdashInosine 002 mdashXanthine 002 mdashUracil 002 002Thymine 002 mdashOrotic acid 002 mdash

B vitamins (mgsdotLminus1)Biotin 2000 2000Para-aminobenzoic acid 1000 mdashNicotinic acid 200 200Ca-pantothenic acid 2000 2000Riboflavin 200 200Folic acid 200 200Cyanocobalamin 200 mdashThiamine 1000 mdashPyridoxal 2000 mdash

Minerals (gsdotLminus1)Manganese sulfate 005 005Magnesium sulfate 01 010Ferrous sulfate7H

2O 002 mdash

CaCl2

mdash mdashSodium citrate 500 500Potassium dihydrogen phosphate 200 200Dipotassium hydrogen phosphate 700 700

Table 1 Continued

Constituent ContentCDM SDM

Carbon source (gsdotLminus1)Glucose 1500 1500

Others (gsdotLminus1)Tween 80 100 100Glycerol mdash mdashNaCl mdash 500

27 Effects of NaCl CaCl2 and Glycerol on the Growth of Efaecium Y31 and Enterocin Y31 Production To determine theeffects of these components 5 gL 10 gL 15 gL and 20 gLNaCl 10 gL CaCl

2 and 50 gL glycerol were individually

added to 1000mLCDM andCDMmediumwith no addtionswas used as a control wherein the inoculum size was 2fermentation temperature was 37∘C and inoculum time was24 h The culturing liquid was then centrifuged for 20minat 10000timesg and then the CFSs were used to determineEnterocin Y31 activity and ODmax (24 h)

28 Effects of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth ofE faecium Y31 and Enterocin Y31 Production According tothe Leave One Out (LOO) technique each amino acid Bvitamin mineral and nucleic acid base was sequentially andindividually omitted from 1000mLCDMmedium andCDMwithout additions was used as a control The inoculum sizewas 2 fermentation temperature was 37∘C and inoculationtime was 24 h The culture liquid was then centrifugedfor 20min at 10000timesg and then the CFSs were used todetermine Enterocin Y31 activity and ODmax (24 h)

The following terms were used to describe the rela-tionship between each medium component and growth asdetermined by the single omission technique A constituentwas considered essential if its omission resulted in less thanhalf the maximum strain growth rate and production ofbacteriocin of the positive control stimulatory when itsabsence resulted in the fact that the growth rate and thebacteriocin production was between 50 and 80 of thatobserved in complete CDM and nonessential if the growthrate and Enterocin Y31 production was 80 (or more) of thatobtained in the complete CDM

29 Purification of Enterocin Y31 E faecium Y31 was allowedto grow in the SDM (Table 1) for 24 h The cells were thenremoved by centrifugation (11800timesg 25min) The CFSswere then filtered through a 022 120583m filter (low-protein-binding HVLP filter Millipore Corp) to remove any remain-ing cells These filtered CFSs were referred to as crude bacte-riocin The crude bacteriocin was subjected to ultrafiltrationof 1 kDa and 30 kDa The retentate from the 1 kDa step wasthen subjected to Tricine-SDS-PAGE

210 Statistical Analyses All experiments were preformedseparately three times and mean plusmn standard deviation (SD)values were calculated from triplicate determinations All

4 Journal of Food Quality

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 320002

0604

081012141618202224

ODpHInhibition zone diameter (mm)

Time (h)

OD

35404550556065707580

pH

0

2

4

6

8

10

12

14

Inhi

bitio

n zo

ne (

mm

)

Figure 1 Relationship between the growth of the bacteriocinogenicstrain and Enterocin Y31 production

data were subjected to one-way analysis of variance (one-way ANOVA) Comparison of means was performed withDuncanrsquos multiple range tests Statistical significance was setat 119875 lt 005

3 Results and Discussion

31 Relationship between the Growth of the Strain andEnterocin Y31 Activity The growth of E faecium Y31 wasunrelated to EnterocinY31 activity inMRSmedium as shownin Figure 1 The result was consistent with the result ofBacterocin J23 produced by Lactobacillus paracasei J23 asdescribed by Huaxi Yi in our research group (not published)whichwas inconsistentwith the result of Salivaricin producedby L salivarius CRL 1328 [19] thus the growth rate of EfaeciumY31 and Enterocin Y31 activity were used as detectionindexes for developing a novel chemical defined mediumEnterocin Y31 activity could be detected at the exponentialphase of the producing strain (9 h) and reached its highestvalue of 1126 plusmn 036mm at stationary phase of producingstrain (24 h) ODmax remained stable at 16 h of fermentationof strain Y31 thus ODmax (16 h) was used as an index of thestrain growth status

32 Effect of NaCl Concentration on the Growth of E faeciumY31 and Enterocin Y31 Production Theeffect of NaCl at 5 gL10 gL 15 gL and 20 gL was determined in CDMwith CDMwith no additives as the control The results indicated thatthe growth of E faecium Y31 and production of EnterocinY31 were not significant difference when adding 5 gL or10 gL NaCl and 0 gL and 15 gL NaCl had no effect onthe growth of strain Y31 and production of Enterocin Y31When the concentration of NaCl was 20 the growth of Efaecium Y31 and production of Enterocin Y31 reduced whichshowed the significant difference when compared to 0 gLand 15 gL NaCl We can conclude that 20 gL NaCl have anegative effect on the growth of strain Y31 and the productionof Enterocin Y31 When the adding concentration of NaClwas 5 gL the ODmax (16 h) of E faecium Y31 was highest

150

155

160

165

170

175

180

Enterocin Y31 production (AUmg protein)

CDM

(con

trol)

bc c

bc

ab

a

b b bab

a

GR

(16B

)

ODmax (16 B)

10A

L N

aCl

15A

L N

aCl

20A

L N

aCl

5A

L N

aCl 0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 2 Effect of NaCl concentration on the growth of Enterococ-cus faecium Y31 and Enterocin Y31 production Means not sharing acommon superscript letter are significantly different fromeach other(119875 lt 005)

172 plusmn 001 and the antibacterial activity also reached themaximum value 128364 plusmn 4140AUmg protein Based thesignificant difference analysis we could conclude that 5 gLNaCl stimulated the growth of strain Y31 (119875 lt 005) andhad no effect on the production of Enterocin Y31 (Figure 2)Similar results have been reported in a study of nutritionalrequirements of L salivarius CRL 1328 producing Salivaricin[19] Considering that the condition for the growth of Efaecium Y31 was crucial 5 gL NaCl was added to the novelchemically defined medium SDM (the medium ingredientsof SDM were listed in Table 1)

33 Effect of CaCl2 and Glycerol on the Growth of E faeciumY31 and Enterocin Y31 Production The results shown inTable 2 indicated that adding 10 gL CaCl

2to CDM had no

effect on the growth of E faecium Y31 but had a negativeeffect on the production of Enterocin Y31 (119875 lt 005) whereasadding 50 gL glycerol had a slight negative effect on thegrowth of E faecium Y31 (119875 lt 005) and a negative influenceon Enterocin Y31 production (119875 lt 005)

34 Effect of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth of Efaecium Y31 and Enterocin Y31 Production According to theLeaveOneOut (LOO) technique each amino acid B vitaminmineral and nucleic acid base was sequentially omitted ina series of prepared formulations along with CDM as acontrol The results shown in Table 3 indicated that L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser and L-Cys areessential amino acids which had an effect on the growth ofE faecium Y31 and Enterocin Y31 production and the stim-ulatory amino acids mainly included L-Asn L-Glu L-Iso L-Lys and L-Try Omitting the stimulatory amino acids resultedin the slow growth of E faecium Y31 and low production

Journal of Food Quality 5

Table 2 Effects of CaCl2and glycerol on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Added components ODmax (600 nm) after 16 h Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003b 124224 plusmn 4141c

10 gL CaCl2

170 plusmn 002b 28986 plusmn 4141a

50 gL glycerol 153 plusmn 003a 56591 plusmn 4181b

Note CDM is explained in Table 1 and means in the same row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

Table 3 Effect of omitting a single amino acid on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Omitted amino acid ODmax (16 h) Relative growth rate Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003h 100 124224 plusmn 4141cd

L-Ala 150 plusmn 005g 90 122843 plusmn 6325cd

L-Arg 076 plusmn 002c ng mdasha

L-Asp 143 plusmn 004g 93 117322 plusmn 6325cd

L-Asn 091 plusmn 003d 60 122843 plusmn 8225cd

L-Cys 100 plusmn 004de 44 mdasha

L-Glu 152 plusmn 004g 72 110420 plusmn 2391c

L-Gln 171 plusmn 004h 84 124224 plusmn 5686d

L-Gly 061 plusmn 003ab ng mdasha

L-His 066 plusmn 003bc ng mdasha

L-Iso 106 plusmn 004ef 79 66252 plusmn 8251b

L-Leu 071 plusmn 003bc ng mdasha

L-Lys 116 plusmn 004f 80 62111 plusmn 4140b

L-Met 053 plusmn 002a ng mdasha

L-Phe 077 plusmn 002c ng mdasha

L-Pro 181 plusmn 003h 71 110420 plusmn 6545cd

L-Ser 049 plusmn 003a ng mdasha

L-Thr 068 plusmn 002bc ng mdasha

L-Try 112 plusmn 003ef 80 57322 plusmn 2391b

L-Tyr 170 plusmn 007h 100 120082 plusmn 3487cd

L-Val 196 plusmn 008i 98 122843 plusmn 6582cd

Note ldquongrdquo represents that the strain did not grow and ldquomdashrdquo represents that there was no inhibition activity CDM is explained in Table 1 and means in thesame row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

of Enterocin Y31 Therefore the essential amino acids andstimulatory amino acids were included in the SDM (listedin Table 1) A previous study reported the similar results asZhang et al found that six amino acids (arginine histidineisoleucine leucine methionine and valine) were necessaryfor the lactococci enterococci and streptococci [20]

Pyridoxal and pantothenic acid are essential B vitaminswhich had an effect on the growth of E faeciumY31 and Ente-rocin Y31 production and the stimulatory B vitamins mainlyincluded niacin and riboflavin Wherein the stimulatory Bvitamins could not result in the growth arrest of E faeciumY31 and the biosynthesis arrest of Enterocin Y31 they couldcause low growth rate and low biosynthesis volume There-fore the essential and stimulatory B vitamins were neededin the SDM Omitting folic acid would cause a reduction of80 in the ODmax (16 h) of E faecium Y31 therefore folicacid is also needed for the growth of E faecium Y31 and theproduction of Enterocin Y31 (Figure 3) It has been reported

that nutritional requirements of L delbrueckii ssp lactis CRL581 growthwere nicotinic acid and pyridoxal and pantothenicacid whereas the growth of L delbrueckii ssp lactis CRL654 requires niacin and pantothenic acid and riboflavinand cyanocobalamin were found to be stimulatory for bothstrains [21] Research results about S thermophilus strains(ST1 ST7 ST8 ST11 ST18 and ST21) indicated that riboflavinwas essential for the growth of all strains whereas Ca-pantothenic acid and nicotinic acid were also required [22]

In the present study MgSO4sdot7H2O was an essential min-

eral andMnSO4sdot4H2OKH

2PO4 K

2HPO4 andCH

3COONa

were stimulatory minerals which had an effect on the growthof E faecium Y31 and Enterocin Y31 production (Figure 4)The necessity of magnesium and phosphate has previouslybeen reported by other researchers for various LAB species[20 23 24]

Adenine and uracil are stimulatory nucleic acids whichhad an effect on the growth of E faecium Y31 and Enterocin

6 Journal of Food Quality

Non

e (CD

M)

Pyrid

oxal

Thia

min

e

Nia

cin

D-B

iotin

Ribo

flavi

n

Cyan

ocob

alam

in

Folic

acid

p-A

min

oben

zoic

acid

Pant

othe

nic a

cid

02040608101214161820

Omitted vitamins

f

b

f

c

f

d

e ef

a

d

b

d

b

ccd

cdcd

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 3 Effect of individually omitting each B vitamin on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Y31 production (Figure 5) No nucleic acid was essential forthe growth of E faecium Y31 and Enterocin Y31 production

35 Comparison of Enterocin Y31 Production onMRSMediumand SDM A novel chemical defined medium (SDM) wasdeveloped (Table 1 and Figures 3 4 and 5) and SDMcontainedNaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

and uracil Strain Y31 grew better on SDM than on MRSmedium (Figure 6) As shown in Figure 7 Enterocin Y31production on SDM was 16 times than that on MRS

36 Purification and Characterization of Enterocin Y31 Afterthe removal of cells from the defined medium the cell-free supernatant was subjected to ultrafiltration through a30 kDa ultrafiltration membrane The active permeate liquorwas then subjected to a second ultrafiltration step using a1 kDa NMWL The antimicrobial activity was again foundin the retentate (10240AUL) Enterocin Y31 was purified byTricine-SDS-PAGE and its molecular weight was 674 kDa(showed in Figure 8)

4 Conclusion

When culturing E faecium Y31 using novel chemical definedmedium (SDM) Enterocin Y31 production increased 16times than that on MRS The ingredients were composedof NaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-ThrL-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

Non

e (CD

M)

Am

mon

ium

citr

ate d

ibas

ic

MnS

O4 middot 4

H2O

MgS

O4 middot 7

H2O

KH2P

O4

K2H

PO4

Sodi

um ac

etat

e

0204060810121416182022

Omitted minerals

d d

b

a

b

c ce e

b

a

c

d d

Enterocin Y31 production (AUmg protein)$

GR

(16B

)$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

Figure 4 Effect of individually omitting each a mineral on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Non

e (CD

M)

Aden

ine

Gua

nine

Inos

ine

Xant

hine

Oro

tic ac

id

Ura

cil

Thym

ine

14

15

16

17

18

19

20

Omitted nucleic acid bases

d

a

c

d d d

b

d

d

abbc

d d d

a

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

Figure 5 Effect of individually omitting each a nucleic acid baseon the growth of Enterococcus faecium Y31 and Enterocin Y31production Means not sharing a common superscript letter aresignificantly different from each other (119875 lt 005)

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

uracil and glucose which were the macro- and micronu-trients needed by biosynthesis of Enterocin Y31 SDM washelpful to the growth of E faecium Y31 and EnterocinY31 production improvement In addition SDM avoided aseries of chromatography steps and the loss of Enterocin Y31

Journal of Food Quality 7

0 5 10 15 20 25 30 3500020406081012141618202224

Time (h)

SDMMRS

GR

(16B

)

Figure 6 Growth of Enterococcus faecium Y31 on MRS and SDM

0 5 10 15 20 25 30 3502468

10121416182022

Time (h)

Inhi

bitio

n zo

ne d

iam

eter

(mm

)

SDMMRS

Figure 7 Enterocin Y31 productions on MRS and SDM

Enterocin Y31

M 140 +$

30+$

20 +$

10 +$

46 +$

17 +$

Figure 8 Tricine-SDS-PAGE of Enterocin Y31 M protein marker1 Enterocin Y31

activity only two steps of ultrafiltration and Tricine-SDS-PAGE were needed to separate and purify Enterocin Y31Therefore chemically defined medium has better potentialfor improving the bacteriocin production and reducing thesteps of separation and purification Chemically definedmedia is useful for purification of not only large bacteriocinssuch as Enterocin Y31 but also small peptide bacteriocinsThe alternative use of a chemically defined medium meetsthe nutritional requirements of strains producing bacteri-ocins and therefore is an excellent alternative to reduce theload of contaminating peptides from the medium therebydecreasing the purification steps To our knowledge no suchstudies have been conducted to improve class IIa bacteriocinEnterocin Y31 production and purify Enterocin Y31

Ethical Approval

This study complies with the research ethics guidelines and itdoes not contain any studies with human or animal subjects

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article

Acknowledgments

This work was financially supported by the 60th Finan-cial Grant from China Postdoctoral Science Foundation(Grant no 2016M602534) the Youth Innovation TalentsProject of General Higher School in Guangdong Province(2016KQNCX144) and theNationalNatural Science Founda-tion of China (Grants nos 31571850 31771988 and 31701621)

References

[1] R C R Martinez M Wachsman N I Torres J G LeBlancS D Todorov and B D G D M Franco ldquoBiochemical anti-microbial and molecular characterization of a noncytotoxicbacteriocin produced by Lactobacillus plantarum ST71KSrdquo FoodMicrobiology vol 34 no 2 pp 376ndash381 2013

[2] I M Aasen T Moslashretroslash T Katla L Axelsson and I StorroslashldquoInfluence of complex nutrients temperature and pH on bacte-riocin production by Lactobacillus sakei CCUG 42687rdquo AppliedMicrobiology andBiotechnology vol 53 no 2 pp 159ndash166 2000

[3] P Alvarez-Sieiro M Montalban-Lopez D Mu and O PKuipers ldquoBacteriocins of lactic acid bacteria extending thefamilyrdquo Applied microbiology and biotechnology vol 100 no 7pp 2939ndash2951 2016

[4] F A C Martinez E M Balciunas A Converti P D Cotterand R P De Souza Oliveira ldquoBacteriocin production by Bifido-bacterium spp A reviewrdquo Biotechnology Advances vol 31 no 4pp 482ndash488 2013

[5] E F OrsquoShea P D Cotter R P Ross and C Hill ldquoStrategiesto improve the bacteriocin protection provided by lactic acidbacteriardquo Current Opinion in Biotechnology vol 24 no 2 pp130ndash134 2013

[6] A-M Zouhir E Kheadr I Tahiri J Ben Hamida and IFliss ldquoCombination with plant extracts improves the inhibitoryaction of divergicin m35 against Listeria monocytogenesrdquo Jour-nal of Food Quality vol 31 no 1 pp 13ndash33 2008

8 Journal of Food Quality

[7] J Pei Y Yuan and T Yue ldquoPrimary characterization of bacteri-ocin paracin C - A novel bacteriocin produced by Lactobacillusparacaseirdquo Food Control vol 34 no 1 pp 168ndash176 2013

[8] D Drider and S Rebuffat ldquoClassification of Bacteriocins fromGram-Positive Bacteriardquo in Prokaryotic Antimicrobial Peptidespp 29ndash53 Springer New York NY USA 2011

[9] T Aymerich H Holo L S Havarstein M Hugas M Garrigaand I F Nes ldquoBiochemical and genetic characterization of ente-rocin A from Enterococcus faecium a new antilisterial bac-teriocin in the pediocin family of bacteriocinsrdquo Applied andEnvironmental Microbiology vol 62 no 5 pp 1676ndash1682 1996

[10] W Liu L Zhang H Yi et al ldquoQualitative detection of class IIabacteriocinogenic lactic acid bacteria from traditional Chinesefermented food using a YGNGV-motif-based assayrdquo Journal ofMicrobiological Methods vol 100 no 1 pp 121ndash127 2014

[11] W Liu L Zhang J Shi et al ldquoAssessment of the safety and appli-cations of bacteriocinogenic Enterococcus faecium Y31 as anadjunct culture in North-eastern Chinese traditional fermen-tation paocairdquo Food Control vol 50 pp 637ndash644 2015

[12] H Khan S H Flint and P-L Yu ldquoDevelopment of a chemicallydefined medium for the production of enterolysin A fromEnterococcus faecalis B9510rdquo Journal of Applied Microbiologyvol 114 no 4 pp 1092ndash1102 2013

[13] M Silva d M Andrade d S A Bauermeister et al ldquoA SimpleDefined Medium for the Production of True Diketopiperazinesin Xylella Fastidiosa and Their Identification by Ultra-FastLiquidChromatography-Electrospray Ionization IonTrapMassSpectrometryrdquoMolecules vol 22 no 6 p 985 2017

[14] E Texeira J Checa A Rıal et al ldquoA New Chemically DefinedMedium for Cultivation of Streptococcus Pneumoniae SerotyperdquoJournal of Biotech Research vol 6 p 54 2015

[15] A Ricciardi R G Ianniello E Parente and T Zotta ldquoModifiedchemically definedmedium for enhanced respiratory growth ofLactobacillus casei and Lactobacillus plantarum groupsrdquo Journalof Applied Microbiology vol 119 no 3 pp 776ndash785 2015

[16] U Schillinger and K Lucke F ldquoAntibacterial activity of Lacto-bacillus sake isolated from meatrdquo Applied and EnvironmentalMicrobiology vol 55 no 8 pp 1901ndash1906 1989

[17] P K Smith R I Krohn G Hermanson et al ldquoMeasurement ofprotein using bicinchoninic acidrdquo Analytical biochemistry vol150 no 1 pp 76ndash85 1985

[18] J Monod ldquoThe Growth of Bacterial Culturesrdquo Annual Reviewsin Microbiology vol 3 no 1 pp 371ndash394 1949

[19] E V Pingitore EMHebert F Sesma andM E Nader-MacıasldquoInfluence of vitamins and osmolites on growth and bacteriocinproduction by Lactobacillus salivarius CRL 1328 in a chemicallydefinedmediumrdquoCanadian Journal of Microbiology vol 55 no3 pp 304ndash310 2009

[20] G Zhang D AMills and D E Block ldquoDevelopment of chemi-cally defined media supporting high-cell-density growth ofLactococci Enterococci and Streptococcirdquo Applied and Environ-mental Microbiology vol 75 no 4 pp 1080ndash1087 2009

[21] E M Hebert R R Raya and G S De Giori ldquoNutritionalrequirements of Lactobacillus delbrueckii subsp lactis in achemically defined mediumrdquo Current Microbiology vol 49 no5 pp 341ndash345 2004

[22] C Letort and V Juillard ldquoDevelopment of a minimal chemi-cally-defined medium for the exponential growth of Streptococ-cus thermophilusrdquo Journal of AppliedMicrobiology vol 91 no 6pp 1023ndash1029 2001

[23] N Terrade and R Mira de Orduna ldquoDetermination of theessential nutrient requirements of wine-related bacteria fromthe genera Oenococcus and Lactobacillusrdquo International Journalof Food Microbiology vol 133 no 1-2 pp 8ndash13 2009

[24] F M Saguir and M C M De Nadra ldquoImprovement of a chem-ically definedmedium for the sustained growth of Lactobacillusplantarum nutritional requirementsrdquo Current Microbiologyvol 54 no 6 pp 414ndash418 2007

Research ArticleLipid Oxidation Color Changes and MicrobiologicalQuality of Frozen Beef Burgers Incorporated with ShiraziThyme Cinnamon and Rosemary Extracts

Hadi Hashemi Gahruie Seyed Mohammad HashemHosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan Shad

Department of Food Science and Technology School of Agriculture Shiraz University Shiraz Iran

Correspondence should be addressed to Mohammad Hadi Eskandari eskandarshirazuacir

Received 3 January 2017 Revised 17 March 2017 Accepted 11 April 2017 Published 21 May 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Hadi Hashemi Gahruie et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In this study the oxidative stability of beef burgers incorporated with Shirazi thyme cinnamon and rosemary extracts wascompared with that of BHT-incorporated and antioxidant-free samples The chemical composition TBARS metmyoglobin pHcolor and microbial and sensory characteristics were evaluated during storage at minus18∘C for 2 months The results indicated thatShirazi thyme and cinnamon extracts did not change the colorimetric properties significantly (119875 lt 005) Incorporating naturalantioxidants led to a significant (119875 lt 005) reduction in TBARS (3658ndash4634) and metmyoglobin (1625ndash1847) as compared tocontrol Except for the control sample total microbial counts of burgers were lower than the maximum allowed limit Burgersformulated with Shirazi thyme revealed the lowest amount of total count Regarding the sensory characteristics the overallacceptability of different samples decreased in the order of cinnamon gt BHT gt Shirazi thyme gt rosemary gt control Finally theresults showed that these plant extracts can be utilized as an alternative to synthetic antioxidants in formulation of burgers

1 Introduction

Meat and meat products are among the most importantprotein sources in the daily diet of people living in developedcountries Beef burger is almost the most popular meatproduct consumed by millions of people from all over theworld The common processes (such as mincing cookingand salt addition) applied in the production of burgersenhance the formation of reactive oxygen species thereforethe resultant product is highly vulnerable to oxidation [1]Lipid and protein oxidations have been reported as theprincipal reason for the decreased quality of burgers duringstorage resulting in decreasing the shelf life [2ndash4]

Application of antioxidants is the best strategy to pre-vent oxidation reactions [5] Synthetic antioxidants such asBHT TBHQ and BHA have various adverse human healtheffects including allergy headache asthma and dermatitis

Therefore the application of natural antioxidants (such asherbal essential oils and extracts) is of interest and canbe observed in a growing number of research works [6ndash8](Aliakbarlu et al 2016)Moreover consumers are increasinglydemanding for green-labeled food products such as thosecontaining natural antioxidant Natural compounds can beobtained from natural sources such as plants fruits vegeta-bles oil seeds spices team honey bee pollen and cereals[9] A lot of extracts have been approved as GRAS (GenerallyRecognized as Safe) that is the addition of these chemicals orsubstances into food is considered safe by experts and theirapplication is exempted from the usual Federal Food Drugand Cosmetic Act (FFDCA) [10]

The potential of natural antioxidants in preventing thelipid oxidation in different food products has been evaluatedby many researchers around the world [11] It has beenreported that the extracts of kinnow rind pomegranate rind

HindawiJournal of Food QualityVolume 2017 Article ID 6350156 9 pageshttpsdoiorg10115520176350156

2 Journal of Food Quality

Hamburger ingredients Extracts (20 g herb + 500 ml water)

Preparation of base batter

Formula 1without additives

(control)

Formula 2with BHT(100 ppm)

Formula 3with Shirazi thyme

(22 mlkg)

Formula 4with rosemary

(28 mlkg)

Formula 5with cinnamon

(73 mlkg)

Analysis (0 15 30 45 and 60 days)

Chemical analysis

Chemical compotation(i) Moisture

(ii) Protein(iii) Fat(iv) Carbohydrate(v) Ash

Deterioration criteria(i) TBARS

(ii) pH(iii) Metmyoglobin

Microbiological analysis(i) Total aerobic bacterial count

Sensory analysis(i) Appearance

(ii) Texture(iii) Taste(iv) Odor(v) Overall acceptance

Color analysis(i) Llowast

(ii) alowast

(iii) blowast

(iv) ΔE

Production and storage at minus18∘C

Figure 1 Schematic diagram of experimental design

and seed powders were significantly able to decrease the lipidoxidation in goat meat patties [12] The effects of natural(sage and rosemary) and synthetic (BHT) antioxidants onprotein oxidation discoloration and texture of refrigeratedpatties produced from pig liver have been studied by Estevezet al [13] Authors reported that the antioxidant propertiesof natural and synthetic antioxidants were similar In treatedsamples the increase in the carbonyl content as a result ofoxidation was significantly (P lt 005) lower than controlsamples Moreover antioxidants could successfully protectheme molecules from degradation Among different naturalantioxidants it has been reported that the extracts of Shirazithyme cinnamon and rosemary reveal substantial antioxi-dant capacity [14]

The main objective of the current study was to comparethe effects of Shirazi thyme cinnamon and rosemary extracts(denoted as natural antioxidants) with those of BHT on pro-tein and lipid oxidations and physicochemicalmicrobial andsensory characteristics of frozen beef burgers during storageThe results of this study may have potential implications

in substituting the synthetic antioxidants with nature-madeones

2 Materials and Methods

A schematic representation of beef burger production isshown in Figure 1

21 Materials Beef flanks (18 fat) from freshly slaughteredanimals (24 hours post slaughter)were purchased froma localmarket (Shiraz Iran) and transported to the laboratory ininsulated polystyrene ice-boxes The meat was ground (MeatGrinder Philips HR2743 AmsterdamNetherlands) througha perforated plate with a hole diameter of 5mm Thiobar-bituric acid (Sigma-Aldrich St Louis MO USA) 1133-tetraethoxypropane (Sigma-Aldrich St Louis MO USA)and diphenyl-2-picrylhydrazyl (DPPH∙) (Sigma-Aldrich StLouisMOUSA) soy protein isolate (SPI 90 protein SonicCo India) onions salt spices and ruskwere also used in thisstudy

Journal of Food Quality 3

22 Plant Extracts Shirazi thyme (Zatariamultiflora) cinna-mon (Cinnamomum zeylanicum) and rosemary (Rosmarinusofficinalis) were purchased from a local grocery The genusand species were certified by experts from the Herbariumof Biology Department (Shiraz University Shiraz Iran)Dried plants were powdered with a mill and then kept inpolyethylene bags at room temperature before extraction

221 Extract Preparation Plant powder (20 g) was thor-oughly mixed with boiling distilled water (500mL) for5min followed by filtration through Whatman grade No 1filter papers and concentration in rotary evaporator (BuchiRotavapor R Switzerland) at 50∘C [15]

222 DPPH Radical Scavenging Activity Antioxidant activ-ity of natural extracts and BHT was calculated using DPPHfree radicalmethod described by Cam et al [16]The amountsof extracts required to replace BHT were calculated basedon the IC50 of BHTThe required amounts of natural extractsshould have equal antioxidant activity to BHT

23 Beef Burger

231 Burger Preparation and Storage The formulation ofbeef burger used in this study was composed of beef (70)onions (134) rusk (4) water (8) SPI (3) salt (1)black (03) and red (02) peppers Ground meat saltwater and minced onion were mixed together After thatSPI was added and then mixed for 15min to obtain ahomogenousmixture Rusk and spices were added in the nextstep Finally natural extracts andor BHT were incorporatedinto the homogenate and thenmixing process was continuedThe concentration of BHT was 100 ppm A burger maker(9 cm internal diameter) was used to shape the mixture intopatties of approximately 90 g and 5mm thickness Burgers(15 patties per treatment) were then packed in light-resistantpolyethylene containers and frozen at minus18∘C Analyses wereperformed during 15-day intervals for two months Beforeanalysis the samples were thawed at +4∘C and then hand-mixed for 30 s

232 Chemical Analysis Moisture protein fat and ashcontents of burgers were determined according to the AOACmethods [17] Carbohydrate content was estimated by sub-tracting the total amounts of moisture protein fat and ashfrom 100

233 pH Measurement Meat sample (10 g) was homog-enized with 50mL deionized water for 1min pH wasmeasured at room temperature using a digital pH meter(Suntex TS-1 Taiwan) equipped with a probe-type combinedelectrode (Ingold) through direct immersion of electrode intothe mixture [17]

234 Instrumental Color Evaluation Color attributes of beefburgers were measured by 119871lowast119886lowast119887lowast method described byYam and Papadakis [18] The values of 119871lowast (brightness) 119886lowast(redness-greenness) and 119887lowast (yellowness-blueness) weremea-sured on the whole outer surfaces of beef burger A wooden

box (50 times 50 times 60 cm3) equipped with a natural daylightsource (6500K) and a digital camera (CanonPowershotA540of six megapixels resolution) in a vertical position and adistance of 25 cm from the samples was used for takingphotos Adobe PhotoshopCS6 was applied to determine theaverage surface color

235 Determination of Lipid Oxidation Lipid oxidationwas monitored by measuring thiobarbituric acid reactivesubstances (TBARS) Meat sample (4 g) was homogenizedwith 20mL trichloroacetic acid solution (20 wv) and thencentrifuged at 3000119892 for 10min The supernatant (2mL) wasmixed with 2mL thiobarbituric acid solution (01 wv indouble distillated water) followed by heating in a water bathat 100∘C for 30min and then cooling to room temperatureTherefore TBARS were extracted in chilled atmosphere Theabsorbance of each extract was measured at 520 nm in aspectrophotometer (spec 1650PC Shimadzu Japan) 1133-tetraethoxypropane was used to develop the standard curvefor TBARS assay TBARS values were reported as mg ofmalonaldehyde per kg of beef burger [7]

236 Metmyoglobin Measurement A modified method ofAn et al [19] was used to measure the metmyoglobincontent in raw beef burgers The sample (4 g) was mixedin a homogenizer with 20mL of phosphate buffer (004MpH 68) and then stored at 1∘C for 1 h The mixture wasthen centrifuged at 3500119892 and 4∘C for 30min Finally thesupernatant was filtered through Whatman grade No 1filter paper The absorbance of the solution was measuredat 525 572 and 700 nm Metmyoglobin () was calculatedaccording to the following equation

Metmyoglobin () = [1395 minus [(119860572 minus 119860700)(119860525 minus 119860700)]]times 100

(1)

Total Aerobic Bacterial Count Total aerobic bacteria werequantified every 15 days using the method described byAliakbarlu et al (2016) Beef burgers (10 g) were asepti-cally transferred into individual stomaching bags containing90mL of sterile saline (09) and homogenized for 2minSerial 10-fold dilutions were prepared in saline and 100 120583Lfrom appropriate dilutions was spread on the surface of platecount agar for total aerobic count (TMC) and then incubatedat 35∘C for 24 h

237 Sensory Evaluation Sensory analyses have been per-formed by 20 trained panelists from the Department of FoodScience and Technology (Shiraz University) Panelists wereboth male and female in the age range of 23ndash28 years oldPanelists were selected based on their previous experiences inconsuming traditional beef burgers Moreover they receivea preparatory session before the sensory test to train themhow to describe all evaluated factors completely Burgers werefried at 150∘C in a forced draft oven to a core temperatureof 72∘C and kept warm in the oven for 3ndash8min until thesensory testing [20] Rectangular pieces of approximately

4 Journal of Food Quality

2 cm were cut from the center of each burger and then servedat room temperature Each panelist randomly evaluated threepieces of all formulations and asked to give a numericalvalue between 1 and 9 for the following attributes taste 1(imperceptible) to 9 (extremely intense) texture attributesand juiciness 1 (extremely dry) to 9 (extremely moist)appearance 1 (extremely soft) to 9 (extremely tough) andodor 1 (imperceptible) to 9 (extremely intense) Tap waterwas provided for panelists to rinse their mouth betweendifferent samples At the end of evaluation each panelist wasasked to give an overall score from 1 (dislike very much) to9 (like very much) for the overall acceptability of differentformulations

24 Statistical Analysis A completely randomized blockdesign with five treatments (including antioxidant-free (con-trol) treatment and those incorporated with BHT cinnamonrosemary and Shirazi thyme extracts) was used in this studyExperiments were performed during a 60-day storage periodat 15-day intervals (0 15 30 45 and 60) Independent blocks(developed from three different batches) were replicatedthree times at each sampling point A two-way analysisof variance (ANOVA) and Duncanrsquos multiple range tests(SAS 80 software SAS Institute Inc Cary NC USA) wereperformed to analyze the effect of treatments storage periodand their interaction on the physicochemical microbial andsensory characteristics of beef burgers at a confidence levelof 005 In the analysis models the treatments storage timesand their interaction were assigned as fixed effects and thereplications as random effects

The given scores of different sensory attributes werecompared between the treatments using general linear model(GLM) Duncanrsquos multiple range tests were used for compar-ison of means at a confidence level of 005 Treatments andassessors were considered as main effects and the replicationsas random effects Data was reported as mean plusmn standarderror (SE)

3 Results and Discussion

31 Antioxidant Activity of Extracts The IC50 values (definedas the concentration of an antioxidant required to reduce theinitial DPPH concentration by 50 using DPPH free radicalmethod described by Cam et al [16]) of natural extracts(including Shirazi thyme cinnamon and rosemary) andsynthetic BHT were 0022 0373 0062 and 0107mgmLrespectively Therefore the amounts of Shirazi thyme cinna-mon and rosemary concentrated extracts required to replace100 ppm BHT in formulation were 22 73 and 28mL per kgof beef burger respectively Cinnamon is a source of bioactivecompounds such as cinnamaldehyde eugenol and coumarin[21] The effect of cinnamon extract as direct scavengersof free radicals has been studied by Roussel et al [22]Carnosic acid and carnosol are the main bioactive com-pounds present in the rosemary extract [23] According toSharififar et al [24] the major chemical compounds presentin Shirazi thyme were carvacrol (3365) thymol (3759) p-cymene (772) 120574-terpinene (388) and 120573-caryophyllene(206)

40

45

50

55

60

65

70

75

80

Met

myo

glob

in (

)

15 30 45 600Storage period (days)

ControlBHTCinnamon extract

Rosemary extractShirazi thyme extract

Figure 2 Effect of incorporating Shirazi thyme cinnamon androsemary extracts on the metmyoglobin () developed in raw beefburgers during frozen storage at minus18∘C

32 Physicochemical Properties of Beef Burger The resultsindicated that the samples contained 5913 moisture 19protein 12 fat 772 carbohydrate and 2 ash

33 Color Stability When assessing meat a consumer paysa great attention to its color which as a visual impressionis induced mainly by the presence of pigments but it alsodepends on tissue composition and meat structure Hencethe color of fresh meat is an important quality parameterthat determines a consumerrsquos response and decision to buyor not to buy that product at retail Changes in 119871lowast 119886lowast and119887lowast values of beef burgers during frozen storage are shown inTable 1 No significant difference (119875 gt 005) was observedbetween the samples incorporated with natural antioxidantsand those incorporated with BHT at production time (day 0)resulting in low Δ119864 values at early stages of storage All of theformulations showed significant decrease in 119886lowast during frozenstorage Formulation incorporated with rosemary extractshowed lower amounts of 119886lowast at the end of storage timeThe significant decrease in 119886lowast values indicated the red colorreduction of products during storage this is despite the factthat BHT- and extract-incorporated treatment significantlyreduced the Met-mb development ratio in comparison tocontrol one (Figure 2) During the first 30 days of storage119871lowast values increased significantly (119875 lt 005) then remainedconstant During frozen storage changes in the amountsof 119871lowast in cinnamon- (642) or Shirazi thyme-incorporatedsamples (597) were less than those in other formulationsSamples incorporated with rosemary extract showed the leastredness (433)

A significant decrease in 119886lowast values of raw pork pat-ties containing grape seed extract and bearberry has beenreported over a 12-day storage by Carpenter et al [25]however 119887lowast values (particularly of control samples) increasedsignificantly (119875 lt 005) Similarly Nunez de Gonzalez et al[26] reported that 119886lowast value of beefs stored under refrigeration

Journal of Food Quality 5

Table 1 Effect of addition of Shirazi thyme cinnamon and rosemary extracts and BHT on 119871lowast 119886lowast 119887lowastand Δ119864 values of raw beef burgersduring frozen storage at minus18∘CParameter Sample Storage period (days)

0 15 30 45 60

119871lowastControl 6033 plusmn 088 glowastlowast 5800 plusmn 058 hi 7133 plusmn 034 abc 7167 plusmn 034 ab 7267 plusmn 067 aBHT 5867 plusmn 088 ghi 5733 plusmn 034 i 6833 plusmn 034 de 6933 plusmn 034 cd 7067 plusmn 067 abc

Cinnamon extract 6033 plusmn 067 g 5433 plusmn 034 j 5967 plusmn 067 gh 6533 plusmn 067 f 6800 plusmn 058 deRosemary extract 5733 plusmn 034 i 5433 plusmn 082 i 6967 plusmn 088 bcd 7133 plusmn 088 abc 7167 plusmn 034 ab

Shirazi thyme extract 5733 plusmn 146 i 5667 plusmn 067 i 5700 plusmn 058 i 6700 plusmn 058 ef 6833 plusmn 067 de

119886lowastControl 1133 plusmn 034 a 833 plusmn 034 de 833 plusmn 034 de 767 plusmn 034 ef 667 plusmn 034 fghBHT 1100 plusmn 058 ab 667 plusmn 034 fgh 767 plusmn 067 ef 700 plusmn 058 fg 667 plusmn 034 fgh

Cinnamon extract 933 plusmn 034 cd 733 plusmn 034 efg 667 plusmn 034 fgh 567 plusmn 034 hij 533 plusmn 034 ijkRosemary extract 1167 plusmn 034 a 533 plusmn 034 ijk 533 plusmn 034 ijk 467 plusmn 034 jk 433 plusmn 034 k

Shirazi thyme extract 1000 plusmn 058 667 plusmn 034 fgh 633 plusmn 034 ghi 567 plusmn 034 hij 533 plusmn 034 ijk

119887lowastControl 2333 plusmn 034 kl 2500 plusmn 058 ij 3233 plusmn 034 bc 3267 plusmn 067 b 3400 plusmn 058 aBHT 2233 plusmn 034 lmn 2333 plusmn 034 kl 3100 plusmn 058 cd 3133 plusmn 067 bcd 3167 plusmn 067 bcd

Cinnamon extract 2167 plusmn 034 mno 2267 plusmn 034 lm 2533 plusmn 034 ij 2600 plusmn 058 i 2767 plusmn 034 hRosemary extract 2033 plusmn 0340 2100 plusmn 058 no 2900 plusmn 058 fgh 3067 plusmn 034 de 3133 plusmn 067 bcd

Shirazi thyme extract 2300 plusmn 000 klm 2433 plusmn 034 jk 2833 plusmn 034 gh 2933 plusmn 034 efg 3033 plusmn 034 def

Δ119864lowastlowastlowastControl 000 plusmn 000 f 1700 plusmn 025 aBHT 272 plusmn 069 e 1409 plusmn 018 bc

Cinnamon extract 282 plusmn 072 e 1078 plusmn 095 dRosemary extract 442 plusmn 104 e 1559 plusmn 102 ab

Shirazi thyme extract 354 plusmn 030 e 1229 plusmn 080 cdlowastlowastData represent averages of three independent repeats plusmn standard errorslowastlowastMeans with different letters are significantly different (119875 le 005)lowastlowastlowastFor each storage time the color difference (Δ119864) was calculated by comparing the color attributes of different formulations with those of control sample

for 10 weeks decreased significantly (119875 lt 005) The resultsof the current study showed that high antioxidant activity ofnatural extracts can be potentially used to develop naturalcolor stabilizers particularly for controlling 119871lowast and 119887lowast valuesin frozen beef burger

As mentioned already samples incorporated with BHTand natural extracts did not show any significant differencein Δ119864 value at the beginning of the storage time However atthe end of storage the lowest and highest changes in Δ119864wereobserved in cinnamon-incorporated and control samplesRedmeat color is an important property of visual appearanceand could influence meat purchasing decisions more thanany other quality parametersThe color of meat products andmeat is influenced by metmyoglobin percentage in muscleInitially the myoglobin was changed into oxymyoglobin(light pink color) which could result in brighter redmeat andthen oxymyoglobin was oxidized into metmyoglobin duringstorage [7]

34 Metmyoglobin Content Assay The amount of metmyo-globin has been positively linked to the extent of proteinoxidation in meat products The heme complex of heme(in) proteins consists of iron in the ferrous state (Fe+2)which turns into the ferric state (Fe+3) via a process calledautoxidation [27] The effects of natural extracts on thechanges of metmyoglobin content are shown in Figure 2Themaximum amount of metmyoglobin (7426) was measuredin antioxidant-free samples The presence of antioxidantsresulted in a significant decrease (1625ndash1847) in the

amounts of metmyoglobin developed during storage whichwas attributed to the strong antioxidant activity An etal [19] evaluated the percent metmyoglobin of the porkjerky samples incorporated with different kimchi powderconcentrations It has been reported that the metmyoglobincontents () of the samples prepared with various kimchipowder levels (ranged from 81 to 83) were significantly(119875 lt 005) lower than that of control sample (85) [19]There was no significant difference between the amounts ofmetmyoglobin under the influence of natural extracts or BHTindicating that these natural extracts can be utilized as asubstitute for BHT to prevent discoloration

The myoglobin reactions with peroxides result in theformation of lipid oxidation promoting compounds [28]The lowest amount of metmyoglobin was measured in thesamples formulated with cinnamon extract indicating thatit was more effective than the other antioxidants (eithernatural or synthetic) in preventing metmyoglobin formationA reverse relationship between the metmyoglobin level and119886lowast value was observed in this study A decrease in 119886lowast valuescorresponding to the decreased redness of lamb meat as aresult of myoglobin oxidation (metmyoglobin formation) hasbeen reported previously [29 30]

Metmyoglobin content increased during storage Thelowest increasing rate was observed in the samples incor-porated with rosemary extract The highest amount of met-myoglobin was observed in the control sample at the endof storage Changes in the metmyoglobin content of controlsample became significant after 15 days

6 Journal of Food Quality

Table 2 Thiobarbituric acid reactive substances (TBARS) values (mg malonaldehyde per kg) of beef burger during frozen storage at minus18∘CSample Storage period (days)

0 15 30 45 60Control 012 plusmn 001lowast 015 plusmn 002 020 plusmn 002 023 plusmn 001 041 plusmn 004BHT 010 plusmn 001 013 plusmn 001 015 plusmn 002 018 plusmn 001 023 plusmn 002Cinnamon extract 011 plusmn 001 013 plusmn 001 016 plusmn 001 017 plusmn 002 024 plusmn 002Rosemary extract 011 plusmn 001 013 plusmn 002 017 plusmn 002 019 plusmn 002 022 plusmn 002Shirazi thyme extract 012 plusmn 001 014 plusmn 002 017 plusmn 002 018 plusmn 001 026 plusmn 002lowastData represent averages of three independent repeats plusmn standard errors

35 Oxidative Stability Initiation is the step in which afatty acid radical is produced Two notable initiators inoxidative stability are OH∙ and HOO∙ which combines witha hydrogen atom to make water and a fatty acid radical Thefatty acid radical is not a very stable molecule so it reactsreadily with molecular oxygen thereby creating a peroxyl-fatty acid radical This radical is also an unstable species thatreacts with another free fatty acid producing a different fattyacid radical and a lipid peroxide or a cyclic peroxide if ithad reacted with itself This cycle continues as the new fattyacid radical reacts in the same wayThe radical reaction stopswhen two radicals react and produce a nonradical speciesThe lipid oxidation leads to produce of some componentscausing off-flavors and reduced nutritional quality such asmalondialdehyde and 4-hydroxynonenal

Thiobarbituric acid test can be used to determine thesecondary products of lipid oxidation in different foods suchas meat and its products [31] Thiobarbituric acid reactivesubstances (TBARS) values of different formulations (as afunction of storage time) are shown in Table 2 Exceptfor control sample the variations in TBARS values of theother formulations revealed a similar pattern Due to theabsence of antioxidant in formulation the observed changesin TBARS values of control were significantly (119875 lt 005)higher than others (8636 higher than rosemary) Natu-ral extracts were as effective as BHT for preventing lipidoxidation in beef burgers This observation indicated thatnatural herbal extracts are suitable replacers for syntheticantioxidant It has been reported that rosemary oleoresin(7704) and a mixture of BHT and BHA (7869) wasequally efficient in inhibiting the lipid oxidation of breakfastsausage containing 25 turkey meat [32] These findings arealso in good agreement with those of Mielnik et al [33] whoreported lower TBARS values after cooking of mechanicallydeboned turkey meat already stored in dark cold and treatedwith rosemary (8834) and grape seed extracts (8383)Sanchez-Escalante et al [34] reported that incorporatingrosemary essential oil into beef patties led to a significant(119875 lt 005) decrease (6400) in TBARS values during coldstorage The essential oil of rosemary was also effective inpreventing (7243) the rancidity of heat-treated turkeymeatproducts [35] It has also been reported that rosemary extractaddition into deboned poultry meat can protect (9820) theproduct from cooking-induced oxidation [36]

Regardless of sample type examined TBARS valuesincreased significantly during the frozen storage and reached

43

45

47

49

51

53

55

57

59

Tota

l aer

obic

bac

teria

l cou

nt (l

og cf

ug)

15 30 45 600Storage period (Days)

52

53

54

55

56

57

58

59

6

61

pH

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

Figure 3 Total aerobic bacterial count (log cfug) (solid symbols)and pH value (open symbols) of different beef burger formulationsas a function of storage time

to a maximum amount of 041mg malonaldehyde per kg inantioxidant-free (control) sample after 60 days At TBARSvalues of 20 off-flavors are definitely detectable and themeatis considered to be unacceptable [37]

36 Changes in pH Values Changes in pH values of beefburgers during frozen storage are shown in Figure 3 Allformulations revealed relatively similar pH values just afterproduction ranging from 588 to 593 coinciding with theISIRI 2008 Mohamed and Mansour [38] similarly reportedthat no significant differences (119875 gt 005) were observed in thepH values of beef patties after incorporating natural herbalextracts

A downward pattern of different rates was observed in thepH values of all formulations during frozen storage As nomicrobial growth was expected during storage the decreasein the pH values could be attributed to the microbial growthduring thawing (by consuming sugar and producing organicacids) Control sample had the lowest pH (551) at the end ofstorage Emiroglu et al [39] reported that the pH values of

Journal of Food Quality 7

all fresh ground beef patty samples treated with thyme andoregano generally decreased after sixth day of storage (119875 gt005)

Also the result showed that to decrease pH amount oflipid oxidation and metmyoglobin significantly increasedLapidot et al (2005) evaluated lipid peroxidation of grilledred turkey muscle (Donor Kabab) as affected by pH In thisstudy they show indeed that lipid peroxidation and myo-globin of a real fast food (turkey Doner Kebab shawarma) issignificantly more rapidly oxidized at pH 30 than at pH 50

37 Microbial Growth As shown in Figure 3 total aerobicbacterial counts of antioxidants-incorporated formulationswere not significantly (119875 lt 005) different The highestamount of total count was observed in control sample(Figure 3) Shirazi thyme-incorporated beef burgers had thelowest microbial count which could be attributed to thehigh antimicrobial properties resulting from thymol and car-vacrol The antibacterial mechanism of thymol and carvacrolis the disruption of the cytoplasmic membrane which raisesits permeability and depolarizes its potential Total countof frozen raw beef burger should be lower than 6 log cfug[40] Except for the control sample the microbial counts ofbeef burgers were lower than the maximum allowed countA relatively good correlation was observed between the pHvalues and total aerobic counts For example control samplehad the lowest pH and the highestmicrobial count Rosemaryextract (1000 ppm) inhibitory effect on the microbial growthof surface-applied beef steaks has been reported by Djenaneet al [41] However Sanchez-Escalante et al [34] reportedthat rosemary did not affect the microbial counts of beefpatties during storage (3 logCFUg)

An increase in the microbial counts was observed duringstorage but not beyond the standard range As a rule ofthumb in good manufacturing and hygienic practices duringpreparation of beef burger and its related products rapidand proper storage is important for decreasing the microbialgrowth and enhancing the shelf life

Vieira et al [42] studied the effect of frozen storage condi-tions (temperature and length of storage) on microbiologicaland sensory quality of rustic crossbred beef at different statesof ageing The result showed that psychrotrophic bacteriaincreased (138 logCFUg) significantly during 90-day storage38 Sensory Properties Color flavor and texture are themostimportant sensory attributes which influence the acceptabil-ity of meat products by consumers [43] Sensory evaluationresults of cooked beef burgers are shown in Figure 4 Gener-ally incorporating Shirazi thyme cinnamon and rosemaryextracts into beef burger formulations had no significantinfluence on the sensory properties Although samples for-mulated with Shirazi thyme and cinnamon extracts with6944 and 7167 acceptability obtained the highest tastescores by panelists (119875 lt 005) The antioxidant prop-erties of natural extracts were the main reason for theincreased sensory scores of natural extract-incorporatedformulations through preventing the formation of oxidation-mediated off-flavors and off-odors (short-chain aldehydes

4

45

5

55

6

65

7Appearance

Taste

OdorTexture

Overall

ControlBHTRosemary extract

Shirazi thyme extractCinnamon extract

Figure 4 Sensory evaluation of different beef burger formulationsa 9-point descriptive scale (1 = extremely poor and 9 = highlyacceptable) was used during evaluation

and ketones) during storage Moreover the presence ofpleasant volatile constituents in natural extracts (particu-larly in cinnamon and Shirazi thyme) led to an increasedsensory score in comparison to the BHT-incorporatedformulation

A significant increase in the flavor scores of beef pattiesincorporated with antioxidant mechanically deboned poul-try meat during frozen storage was similarly reported byMohamed and Mansour [38]

4 Conclusion

This work aimed to study the possible replacement ofsynthetic antioxidant BHT with natural extracts (includingShirazi thyme cinnamon and rosemary extracts) in beefburger formulation Different samples were prepared thendifferent characteristics such as protein and lipid oxidationand physicochemical microbial and sensory properties wereevaluated during frozen storage Herbal extracts could inhibitthe lipid oxidation in formulated burgers Moreover it wasdemonstrated that natural herbal extracts were generallybetter than BHT in preventing the lipid and protein oxi-dations as well as improving the sensory attributes of beefburgersTherefore it can be concluded that natural extracts ofShirazi thyme (0022mgmL) cinnamon (0373mgmL) androsemary (0062mgmL) can be used as natural substitutesfor BHT (0107mgmL)This substitutionmay have potentialimplication for developing green-labeled meat product Infuture studies it would be informative to study the effect ofmixed extracts and their possible synergistic or antagonisticeffects in extending the shelf life of meat products

8 Journal of Food Quality

Additional Points

Practical Applications Beef burger containing natural antiox-idant is one of themost important functional food for humanconsumption attributable to its nutritional properties andhealth effects However the nutraceutical properties of thisfood have improved due to alternative BHT with extractsThe present investigation demonstrated the effects of addingvarious natural antioxidants to the beef burger so as tomonitor the changes that occur to the physicochemicalantimicrobial and sensorial properties of the beef burger

Conflicts of Interest

The authors declare that they have no conflicts of interest

Acknowledgments

This research project was financially supported by ScientificAffairs Shiraz University and Department of Food Scienceand Technology Shiraz University Shiraz Iran

References

[1] D Ladikos and V Lougovois ldquoLipid oxidation in muscle foodsa reviewrdquo Food Chemistry vol 35 no 4 pp 295ndash314 1990

[2] C JMussinan andM JMorello ldquoFlavor analysis developmentsin isolation and characterizationrdquo American Chemical Societypp 343ndash358 1998

[3] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWTmdashFoodScience and Technology vol 68 pp 385ndash390 2016

[4] G Comi E Tirloni D Andyanto M Manzano and LIacumin ldquoUse of bio-protective cultures to improve the shelf-life and the sensorial characteristics of commercial hamburg-ersrdquo LWTmdashFood Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[5] F Shahidi ldquoAntioxidants in food and food antioxidantsrdquoFoodNahrung vol 44 pp 158ndash163 2000

[6] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[7] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[8] H H Hashemi Gahruie M H Eskandari G Mesbahi andM A Hanifpour ldquoScientific and technical aspects of yogurtfortification a reviewrdquo Food Science and Human Wellness vol4 no 1 pp 1ndash8 2015

[9] K Yamazaki S Kawamorita H Ohmiya and M SawamuraldquoDirected ortho borylation of phenol derivatives catalyzed by asilica-supported iridium complexrdquo Organic Letters vol 12 no18 pp 3978ndash3981 2010

[10] A Roberts and L A Haighton ldquoA hard look at FDArsquos review ofGRAS noticesrdquo Regulatory Toxicology and Pharmacology vol79 pp S124-S128 2016

[11] H H Hashemi Gahruie E Ziaee M H Eskandari andS M Hosseini ldquoCharacterization of basil seed gum-basededible films incorporated with Zataria multiflora essential oilnanoemulsionrdquo Carbohydrate Polymers vol 166 pp 93ndash1032017

[12] S K Devatkal K Narsaiah and A Borah ldquoAnti-oxidant effectof extracts of kinnow rind pomegranate rind and seed powdersin cooked goatmeat pattiesrdquoMeat Science vol 85 no 1 pp 155ndash159 2010

[13] M Estevez R Ramırez S Ventanas and R Cava ldquoSage androsemary essential oils versus BHT for the inhibition of lipidoxidative reactions in liver paterdquo LWTmdashFood Science andTechnology vol 40 no 1 pp 58ndash65 2007

[14] E Abdollahzadeh M Rezaei and H Hosseini ldquoAntibacterialactivity of plant essential oils and extracts the role of thymeessential oil nisin and their combination to control listeriamonocytogenes inoculated in minced fish meatrdquo Food Controlvol 35 no 1 pp 177ndash183 2014

[15] A Alaklabi I A Arif A Ahamed R Surendra Kumar andA Idhayadhulla ldquoEvaluation of antioxidant and anticanceractivities of chemical constituents of the saururus chinensis rootextractsrdquo Saudi Journal of Biological Sciences 2017

[16] M Cam Y Hısıl and G Durmaz ldquoClassification of eightpomegranate juices based on antioxidant capacity measured byfourmethodsrdquo FoodChemistry vol 112 no 3 pp 721ndash726 2009

[17] AOAC Association of Official Agricultural Chemists ldquoOfficialmethods of analysis of AOAC Internationalrdquo in AgricultureChemicals Contaminants Drugs vol 1 AOAC InternationalArlington VA USA 16th edition 1995

[18] K L Yam and S E Papadakis ldquoA simple digital imagingmethodfor measuring and analyzing color of food surfacesrdquo Journal ofFood Engineering vol 61 no 1 pp 137ndash142 2004

[19] K-I An J-H Choi Y-S Choi et al ldquoEffects of kimchi powderon quality characteristics of semi-dried pork jerkyrdquo KoreanJournal for Food Science of Animal Resources vol 30 no 2 pp198ndash205 2010

[20] B Kodal Coskun E Calikoglu Z Karagoz Emiroglu and KCandogan ldquoAntioxidant active packaging with soy edible filmsand oregano or thyme essential oils for oxidative stability ofground beef pattiesrdquo Journal of Food Quality vol 37 no 3 pp203ndash212 2014

[21] B Shan Y Z Cai M Sun and H Corke ldquoAntioxidant capacityof 26 spice extracts and characterization of their phenolicconstituentsrdquo Journal of Agricultural and Food Chemistry vol53 no 20 pp 7749ndash7759 2005

[22] A-M Roussel I Hininger R Benaraba T N Ziegenfuss andR A Anderson ldquoAntioxidant effects of a cinnamon extract inpeople with impaired fasting glucose that are overweight orobeserdquo Journal of the American College of Nutrition vol 28 no1 pp 16ndash21 2009

[23] S Moreno T Scheyer C S Romano and A A VojnovldquoAntioxidant and antimicrobial activities of rosemary extractslinked to their polyphenol compositionrdquo Free Radical Researchvol 40 no 2 pp 223ndash231 2006

[24] F Sharififar M H Moshafi S H Mansouri M Khodashenasand M Khoshnoodi ldquoIn vitro evaluation of antibacterial andantioxidant activities of the essential oil and methanol extractof endemic Zataria multiflora Boissrdquo Food Control vol 18 no7 pp 800ndash805 2007

[25] R Carpenter M N OrsquoGrady Y C OrsquoCallaghan N M OrsquoBrienand J P Kerry ldquoEvaluation of the antioxidant potential of grape

Journal of Food Quality 9

seed and bearberry extracts in raw and cooked porkrdquo MeatScience vol 76 no 4 pp 604ndash610 2007

[26] M T Nunez de Gonzalez B S Hafley R M Boleman R KMiller K S Rhee and J T Keeton ldquoAntioxidant propertiesof plum concentrates and powder in precooked roast beef toreduce lipid oxidationrdquo Meat Science vol 80 no 4 pp 997ndash1004 2008

[27] M P Richards and M A Dettmann ldquoComparative analysisof different hemoglobins autoxidation reaction with peroxideand lipid oxidationrdquo Journal of Agricultural and FoodChemistryvol 51 no 13 pp 3886ndash3891 2003

[28] J Everse and N Hsia ldquoThe toxicities of native and modifiedhemoglobinsrdquo Free Radical Biology and Medicine vol 22 no6 pp 1075ndash1099 1997

[29] C Kennedy D J Buckley and J P Kerry ldquoInfluence of differentgas compositions on the short-term storage stability of mother-packaged retail-ready lamb packsrdquo Meat Science vol 69 no 1pp 27ndash33 2005

[30] J P Kerry M G OrsquoSullivan D J Buckley P B Lynch andP A Morrissey ldquoThe effects of dietary 120572-tocopheryl acetatesupplementation and modified atmosphere packaging (MAP)on the quality of lamb pattiesrdquo Meat Science vol 56 no 1 pp61ndash66 2000

[31] J Fernandez J A Perez-Alvarez and J A Fernandez-LopezldquoThiobarbituric acid test for monitoring lipid oxidation inmeatrdquo Food Chemistry vol 59 no 3 pp 345ndash353 1997

[32] S Barbut D B Josephson and A J Maurer ldquoAntioxidantproperties of rosemary oleoresin in Turkey sausagerdquo Journal ofFood Science vol 50 no 5 pp 1356ndash1359 1985

[33] M B Mielnik K Aaby and G Skrede ldquoCommercial antioxi-dants control lipid oxidation in mechanically deboned turkeymeatrdquoMeat Science vol 65 no 3 pp 1147ndash1155 2003

[34] A Sanchez-Escalante D Djenane G Torrescano J A Beltranand P Roncales ldquoThe effects of ascorbic acid taurine carnosineand rosemary powder on colour and lipid stability of beef pattiespackaged in modified atmosphererdquoMeat Science vol 58 no 4pp 421ndash429 2001

[35] M B Mielnik S Sem B Egelandsdal and G Skrede ldquoBy-products from herbs essential oil production as ingredient inmarinade for Turkey thighsrdquo LWTmdashFood Science and Technol-ogy vol 41 no 1 pp 93ndash100 2008

[36] J H Macneil P S Dimick and M G Mast ldquoUse of chemicalcompounds and a rosemary spice extract in quality mainte-nance of deboned poultry meatrdquo Journal of Food Science vol38 no 6 pp 1080-1081 1973

[37] E TEC ldquoMeat technology update 1-6 2009rdquo[38] H M H Mohamed and H A Mansour ldquoIncorporating

essential oils of marjoram and rosemary in the formulation ofbeef patties manufactured with mechanically deboned poultrymeat to improve the lipid stability and sensory attributesrdquoLWTmdashFood Science and Technology vol 45 no 1 pp 79ndash872012

[39] Z K Emiroglu G P Yemis B K Coskun and K CandoganldquoAntimicrobial activity of soy edible films incorporated withthyme and oregano essential oils on fresh ground beef pattiesrdquoMeat Science vol 86 no 2 pp 283ndash288 2010

[40] ISIR Raw frozen hamburgermdashSpecifications vol 2304 Instituteof standards and industrial research of Iran Karaj Iran 3rdedition 2008

[41] DDjenane A Sanchez-Escalante J A Beltran andP RoncalesldquoAbility of 120572-tocopherol taurine and rosemary in combination

with vitamin C to increase the oxidative stability of beef steakspackaged in modified atmosphererdquo Food Chemistry vol 76 no4 pp 407ndash415 2002

[42] C Vieira M T Diaz B Martınez and M D Garcıa-CachanldquoEffect of frozen storage conditions (temperature and lengthof storage) on microbiological and sensory quality of rusticcrossbred beef at different states of ageingrdquo Meat Science vol83 no 3 pp 398ndash404 2009

[43] J Aliakbarlu and S Khalili Sadaghiani ldquoEffect of avishaneshirazi (zataria multiflora) and clove (syzygium aromaticum)essential oils on microbiological chemical and sensory proper-ties of ground sheep meat during refrigerated storagerdquo Journalof Food Quality vol 38 no 4 pp 240ndash247 2015

Research ArticleOptimization of Ultrasound Extraction of Cactus Pear(Opuntia ficus indica) Seed Oil Based on AntioxidantActivity and Evaluation of Its Antimicrobial Activity

Mariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-CansinoErnesto Alaniacutes-Garciacutea Luis Delgado-Olivares Joseacute Alberto Ariza-OrtegaEsther Ramiacuterez-Moreno and Joseacute de Jesuacutes Manriacutequez-Torres

Centro de Investigacion Interdisciplinario Area Academica de Nutricion Instituto de Ciencias de la Salud Universidad Autonoma delEstado de Hidalgo Circuito Actopan-Tilcuautla SN Ex Hacienda La Concepcion 42160 San Agustın Tlaxiaca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 20 February 2017 Accepted 9 April 2017 Published 27 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Marıa de los Angeles Ortega-Ortega et alThis is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The purpose of the present study was to determine the optimal ultrasound conditions (amplitude level and time) for the extractionof cactus pear seed oil with the highest antioxidant activity using a closed system Seed oil was analyzed for yield antioxidant activityby ABTS and DPPH and antimicrobial activity Conventional extraction methods were assessed for comparison Amplitude levelsignificantly affected antioxidant activity in linear terms (p lt 00001 DPPH and p lt 0001 ABTS resp) so at lower amplitudes thehigher antioxidant activity was achieved The optimum ultrasound extraction conditions were of 78 amplitude for 10min andyielded antioxidant activity values of 6625mg AAE100 g and 289120583mol TE100 g for ABTS and DPPH respectively Comparedwith conventional extraction methods ultrasound exhibited lower oil yield and antioxidant activity but had the potential toachieve comparable results if multiple ultrasound extractions are performed in the time needed by conventional methods Seed oilsshowed similar antimicrobial activity despite the extraction method and were more effective against Escherichia coli The resultsdemonstrated that ultrasound can be an alternative extraction method of seed oils from fruits such as cactus pear

1 Introduction

Cactus pear fruit (Opuntia ficus indica) is common in aridand semiarid regions around the world [1] This fruit that ismainly consumed fresh in Mexico [2] is composed by pulppeel and seeds [3] According to several studies cactus pearfruit has bioactive compounds [4 5] with high antioxidantand antimicrobial activity [6 7] Some of these compoundsare found in the seeds [8] which comprise 3 to 15 of thecactus pear pulp [9] and are usually considered waste afterpulp processing [7] Seeds also have a high content of oil(988 gkg) [10] characterized by high levels of linoleic andoleic acids [7] and other components as phenols [11] all whichmay contribute to humanhealth [12] Currently seed oils havebeen used as natural agents for food preservation [13] andmany have exhibited antimicrobial and antioxidant activity

some of these oils are from pumpkin [14] apple [15] blackcumin [16] and basil [17] among other seeds Cactus pearseeds fromOpuntia dillenii also have a high antioxidant activ-ity derived from bioactive compounds such as polyphenolsand polyunsaturated fatty acids [18] Some polyunsaturatedfatty acids have also been identified in seeds from Opuntiaficus indica [19 20] implying that these seeds may also havehigh antioxidant activity

Seed oil is usually extracted by means of conventionalmethods such as Soxhlet and maceration using heat agita-tion or long extraction times [21] Microwave supercriticalfluids and ultrasonic assisted extraction are unconventionalmethods that exert a physical effect on the sample [22]Ultrasound has been used to extract antioxidants frommanyfood materials including seeds Ultrasound and ultrasound-assisted extractions use sound waves to produce cavitation

HindawiJournal of Food QualityVolume 2017 Article ID 9315360 9 pageshttpsdoiorg10115520179315360

2 Journal of Food Quality

microbubbles that collapse violently in the sample and facili-tate the release and extraction of several compounds [23ndash25]Some researchers had evaluated ultrasound-assisted extrac-tion in an open system using a sonicator probe directly onthe liquid sample to obtain seed oil fromflaxseed [26] Koreanpine [27] and pomegranate [28] The purpose of the presentstudy was to optimize the extraction conditions of cactuspear seed oil using ultrasound in a closed system based onantioxidant activity and using response surfacemethodologyYield extraction and antioxidant and antimicrobial activitywere compared with conventional methods

2 Materials and Methods

21 Sample Green cactus pear (Opuntia ficus indica) Reynavariety was provided by the Mexican Association CoMeN-Tuna (Consejo Mexicano del Nopal y la Tuna AC ofActopanHidalgoMexico) in spring of 2012Thegreen cactuspear seeds were obtained after several washes with water thatremoved the pulp and residues The seeds were leaved todry at ambient temperature until they reached a moisture of643 After the seeds were crushed using an industrial mill(Cyclotec 1093 Tecator Hoganas AB Sweden) the powderwas passed through a mesh sieve to obtain a particle size ofapproximate 05mm and then stored in sealed plastic bags atroom temperature and dark conditions

22 Ultrasound Extraction Ultrasound (VCX-1500 Sonic ampMaterials Inc Newtown CTUSA) at 1500Wwith a constantfrequency of 20 kHz and a probe of 25mm was used forthe extraction of green cactus pear seeds oil Extractionfrom milled and sieved seeds (20 g) was carried out at anamplitude and time ranges of 80 to 90 and 5 to 15minrespectively and a fixed outlet temperature of 25∘C A sampleof 400mL was introduced in a jacketed vessel with waterat 4∘C circulating through the secondary layer [29] Afterextraction the aqueous and solid phases were separatedby filtration using a vacuum pump (DOA-P704-AA GASTManufacturing Inc BentonHarbor MI USA) Both phasesaqueous and solid (this last was dried) (Weston 74-1001-wWeston Products LLC Strongsville OH USA) were mixedwith hexane for 30min and then separated from the solventby filtration The aqueous phase was centrifuged (Allegra25R Beckman Couler CA USA) at 10000 rpm for 30minat 4∘C and was stored in plastic containers and kept frozenuntil analysis The solid phase was stored in hermeticallysealed bags in the dark The solvent obtained from the twophaseswas evaporated (BUCHILabortechnikAG Flawil SGSwitzerland) at 40∘C to obtain the oil

23 Soxhlet Extraction Soxhlet extraction was performedaccording to the AOAC [30] Milled and sieved seeds (5 g)hexane (120mL) and a universal fat extraction system (BuchiLabortechnik AG Flawil SG Switzerland) were used

24 Maceration Extraction Milled and sieved seeds (10 g)were introduced in a previously defatted cotton bag andthen immersed in 200mL of hexane in a closed glass at atemperature of asymp25∘C After the sample was stored in a dark

place for 24 hrs the oil was obtained after solvent evaporationusing a rotary evaporator (BUCHI Labortechnik AG FlawilSG Switzerland) at 40∘C

25 Yield Oil yield was determined according to Chouguiet al [31] using the following equation

Oil () = (1198721 minus11987201198722 ) times 100 (1)

where1198720 is the weight of the empty Eppendorf tube (g)1198721is the weight of the Eppendorf tube after evaporation (g) and1198722 is the weight of the milled seeds (g)

The oil was stored in 2mL amber Eppendorf tubes atminus32∘C until analysis

26 Determination of Antioxidant Activity

261 ABTS Assay Antiradical capacity by ABTS was mea-sured according to Kuskoski et al [32] The radical cation221015840azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) diam-monium salt (ABTS∙+) was produced by reacting 7mMABTSstock solution with 245mM potassium persulfate in thedark at room temperature for 16 hrs before being used TheABTS∙+ solution was diluted with deionized water to anabsorbance of 070 plusmn 010 at 754 nm An aliquot of 20120583L ofsample was added to 980120583L of the diluted ABTS∙+ solutionand absorbance readings were taken after 7min incubationat room temperature The absorbance of the mixture wasmeasured at 754 nm in themicroplate reader (PowerWaveXSUV-Biotek software KC Junior VT USA) and antioxidantcapacity was expressed as mg ascorbic acid equivalent per100 g of oil (mg AAE100 g)

262 DPPH Assay Antiradical activity was measured using11-diphenyl-2-picrylhydrazyl (DPPH∙) radical as describedby Morales and Jimenez-Perez [33] A methanol-acetatesolution (74mg100mL) of the stable DPPH∙ radical wasprepared A sample aliquot of 100120583Lwas placed into vials and500 120583L of DPPH∙ solution was added before the mixture wasleft to sit at room temperature for 1 hr Finally absorbancewasmeasured at 520 nm in the microplate reader (Power WaveXS UV-Biotek software KC JuniorWinooski VT USA) andantioxidant activity was expressed as 120583mol of Trolox equiva-lents per 100 g of oil (120583mol TE100 g)

27 Experimental Design

271 Optimization The optimization of the ultrasoundextraction conditions was performed using the responsesurface methodology (RSM) with a central composite rotat-able design for two independent extraction variables at fivelevelsThe independent extraction variables (amplitude level80ndash90 time 5ndash15min) were determined based on prelimi-nary experiments where higher antioxidant activity by ABTSand DPPH was observed Design consisted in thirteen com-binations with five central points replicates (Table 1) Exper-imental data were subjected to multiple nonlinear regression

Journal of Food Quality 3

Table 1 Experimental design matrix

Numbera Pattern Amplitude level () Time (min)119883119894 119883119895

(1) 00 85 10(2) +minus 90 5(3) ++ 90 15(4) 00 85 10(5) A0 92 10(6) minusminus 80 5(7) 00 85 10(8) a0 78 10(9) 0A 85 17(10) minus+ 80 15(11) 00 85 10(12) 00 85 10(13) 0a 85 3aNonrandomized

analysis (JMP 702 SAS Institute Inc Cary NC USA) fittedto a second-order polynomial model

119884 = 1205730 +2

sum119894=1

120573119894119883119894 +2

sum119894=1

1205731198941198941198832119894 +sum119894

sum119895=119894+1

120573119894119895119883119894119883119895 (2)

where 119884 is the predicted response 1205730 is the constant coeffi-cient120573119894 is the lineal coefficient120573119894119894 is the quadratic coefficientand120573119894119895 is the interaction coefficients In thismodel119883119894 and119883119895are the independent extraction variables amplitude level ()and time (min) respectively

The adequacy of themathematicalmodel was determinedusing the coefficient 1198772The significance of the model regres-sion coefficients was evaluated using an analysis of varianceThree-dimensional curves from the response surface plotswere obtained to interpret the effects of the interactionbetween independent variables on the response variablesContour plots were generated to represent the extrapolationand interpret the optimization of the extraction variablesusing the Sigma Plot 123 graphing software (SYTAT softwareInc Richmond CA USA)

272 Treatment Comparison Comparison between extrac-tion methods (ultrasound-optimized Soxhlet and macera-tion) was carried out by a one-way analysis of variance(ANOVA) All determinations were performed in triplicateand significant differences between means were determinedby Duncan test (p le 005) using the SPSS program (150 SPSSInc Chicago IL USA)

28 Scanning Electron Microscopy Scanning electron micro-scopy (SEM) was used to examine the morphological alter-ations caused to the cactus pear seeds before and after theultrasound extraction Samples deposited on the siliconwaferwere coated with a thin layer of gold (Denton VacuumDesk V Moorestown NJ USA) applying 20 millitorr and

20mA during 4min Samples were observed in a scanningelectronic microcopy (JEOL JSM-6300 Peabody MA USA)at 1000 and 500 amplifications and micrographs were takento establish the structural comparison between both samples

29 Antimicrobial Activity The green cactus pear seed oilwas tested against one Gram-positive bacteria Staphylococ-cus aureus (ATCC 1654) and two Gram-negative bacteriaEscherichia coli (ATCC 25922) and Pseudomonas aeruginosa(ATCC 27853) All microorganisms were obtained from theMexicanMicrobial Culture Collection of CINVESTAV of theNational Polytechnic Institute (Mexico) For each microor-ganism bacterial suspensions were made in a soybean-casein digest medium to a concentration of approximately108 CFUmL

To evaluate the antimicrobial activity and the mini-mum inhibitory concentration (MIC) the disk diffusionmethod was used Each bacterial suspension (100 120583L fromthe 108 CFUmL) was spread on prepared agar plates (sterileStandardMethodsAgar for bacteria) Filter sterile paper discs(6mm in diameter) were impregnated with 6667 50 3333and 1667 120583L of the undiluted oil and were placed on theinoculated plates The negative control was hexane whileampicillin (10 120583g) and streptomycin (10 120583g) were used aspositive controls The plates where incubated at 37∘C (ArsaAR-130 Felisa Jalisco Mexico) for 24 hrs The diameters ofthe inhibition zones were measured in millimeters and theresults of MIC were expressed as 120583g120583L

3 Results and Discussion

31 Extraction Yield Table 2 shows the oil yields achievedby the ultrasound treatments The extraction yield variedfrom 375 to 6 and the maximum yield was obtained at thehighest amplitude level of 92 Oil yield strongly dependedon amplitude level probably because at high amplitudes thecavitation effect increases [21] and induces physical changeson the structure of the seed such as disruption of the cell wallsreduction of the particle size and increase of exposure areaThese conditions may facilitate the penetration of the solventand thus the extraction of oil [26 28 34] The maximumyield was achieved after 10min of treatment and longertimes (15min) at high amplitudes (90) did not increase oilextraction (Table 2) Albeit time is an important variable afteryield reaches a peak a longer treatment does not maximizeextraction the same was described by Zhang et al [27] forKorean pine seed who demonstrated that oil yield increasedwith time but when it reached amaximum yield equilibratedand then decreased gradually This may be attributed to aninitial complete fracture of the cell walls during the firstminutes of the cavitation effect [26 28 34]

32 Antioxidant Activity of Green Cactus Pear Seed OilExtracted by Ultrasound Due to the complexity of theoxidation processes it is advisable to performmore than onemethod to obtain the antioxidant profile of a sample [35]In order to determine the antioxidant activity of the green

4 Journal of Food Quality

Table 2 Extraction yield and antioxidant activity of green cactus pear seed oil extracted by ultrasound under different conditions

Extraction conditions Antioxidant activity

Amplitude level () Time (min) Oil yield () ABTS DPPHmg AAE100 g 120583mol TE100 g

85 10 575 plusmn 003 6615 plusmn 407 24610 plusmn 09290 5 415 plusmn 001 5598 plusmn 313 14176 plusmn 39090 15 485 plusmn 002 5993 plusmn 445 16702 plusmn 11485 10 525 plusmn 001 6812 plusmn 659 23601 plusmn 32292 10 600 plusmn 006 5584 plusmn 236 10163 plusmn 46880 5 525 plusmn 001 6607 plusmn 217 26707 plusmn 73785 10 375 plusmn 000 6837 plusmn 392 24505 plusmn 23778 10 540 plusmn 010 6599 plusmn 501 28926 plusmn 02685 17 560 plusmn 006 6578 plusmn 037 26009 plusmn 13380 15 540 plusmn 000 6691 plusmn 320 28496 plusmn 09385 10 575 plusmn 000 6773 plusmn 040 27755 plusmn 17185 10 530 plusmn 010 6744 plusmn 389 24508 plusmn 29285 3 550 plusmn 010 6763 plusmn 000 25005 plusmn 199plusmn standard deviation

Table 3 Antioxidant activity regression coefficients of the ultra-sound extraction conditions

Coefficient ABTS DPPH1205730 67562964a 24996199a

120573119894 minus3927762b minus6357459a120573119895 02724311 71702572120573119894119895 077572 18421052120573119894119894 minus3719624b minus2977102b120573119895119895 minus0826106 004258041198772adj 093 096120573119894 amplitude level 120573119895 time significance levels a119901 lt 00001 b119901 lt 0001

cactus pear seed oil two parameters were evaluated antiox-idant and scavenging capacity by ABTS and DPPH respec-tively The results and experimental design are described inTable 2 Antioxidant activity ranged from 5584 to 6837mgAAE100 g for ABTS and 10163 to 28926120583mol TE100 g forDPPH A 1198772 value closest to one or at least of 080 indicates agood fit of themodel [36]The1198772 values for ABTS andDPPHwere 093 and 096 respectively (Table 3) indicating thatthe averages obtained adjusted to the mathematical responsesurface model

33 Effect of Ultrasound Extraction Conditions on the Antiox-idant Activity of Cactus Pear Seed Oil In this study asecond-order polynomial model for predicting the antiox-idant activity of green cactus pear seed oil was obtainedby multiple linear regression analysis of the experimentaldata Table 3 shows the regression coefficients and significantprobabilities of the linear quadratic and interaction effects ofthe ultrasound conditions on the seed oil antioxidant activityBoth ABTS and DPPH values were significantly affected byamplitude level in linear term (120573119894) at 119901 lt 00001 DPPH and119901 lt 0001 ABTS respectively as well as in its quadratic term

(120573119894119894) at 119901 lt 0001 DPPH and ABTS The three-dimensionalsurface plots constructed to observe the effect of ultrasoundprocessing (Figure 1) demonstrated that antioxidant activitywas higher when the applied amplitude decreased

34 Optimization of the Ultrasound Extraction Conditions ofCactus Pear Seed Oil Optimal extraction conditions wereselected from the overlapped contour plots inwhich the effectof amplitude level and time on the antioxidant activity ofgreen cactus pear seed oil was considered

Figure 2 shows the optimal zone where the highestantioxidant activity by ABTS and DPPH was achieved Theconditions corresponded to amplitude of 78 applied for10min In this zone the values for antioxidant activity wereof 6625mg AAE100 g and 289 120583mol TE100 g for ABTS andDPPH respectively

35 Comparison between Methods

Extraction Yield and Antioxidant Activity Figure 3 comparesthe oil yields obtained by the three extraction methodsThe results revealed that the yield obtained using the opti-mized ultrasound extraction was significantly lower than theobtained with the Soxhlet and maceration procedures Thehigher oil yield obtained by Soxhlet could be attributed to theconstant and extended contact (4 to 6 hrs) of the sample withthe solvent at high temperatures in addition to the repeatedwashing cycles [37] The ultrasound yield was closer to thatof maceration method but this last one required longer time(24 hrs) as compared to 10min ultrasound treatment

The results of antioxidant activity by ABTS andDPPH areshown in Figure 4 Both parameters were significantly higherin the oil extracted by Soxhlet (5433 plusmn 084mg AAE100 gand 26660 plusmn 197 120583mol TE100 g resp) compared to theother extraction methods The ultrasound and macerationextractions exhibited similar antioxidant activity by ABTSwhile DPPH was significantly higher for the ultrasound seed

Journal of Food Quality 5

45

50

55

60

65

70

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(mg

AA

E100

g)A

ntio

xida

nt ac

tivity

(a)

50

100

150

200

250

300

350

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(120583m

ol T

E100

g)A

ntio

xida

nt ac

tivity

(b)

Figure 1 Effect of the ultrasound extraction on the antioxidant activity of green cactus pear seed oil (a) ABTS (b) DPPH

121

109

133145

157

169181

157

169

193

169

181

205

193

205

217

217

205

229

217

229

241

229

241

253

241

253

253

265

265

265

265

277

277

277

265

289

DPPH

5650

5650

557555005425

572558005875

5950

6025

6100

6175

6250

5950

6025

63256400

6175

6250

6250

6325

6475

6325

64006475

6400

6550

6475

6550

6550

6625

6625

6625

6700

6700

6700

6775

6775

6775

6700

6700

6625

6550

6475

6625

ABTS

Optimun condition

4

6

8

10

12

14

16

Tim

e (m

in)

80 82 84 86 88 90 9278Amplitude level ()

Figure 2 Optimal ultrasound extraction conditions of green cactuspear seed oil based on the highest antioxidant activity

oil Albeit the oil extracted by the Soxhlet method presentedhigher yield and antioxidant activity the ultrasound-assistedextraction may be enhanced if multiple extractions arecarried out in a time comparable to the required by theSoxhlet procedure (4ndash6 hrs)

36 Antimicrobial Activity Escherichia coli and Staphylo-coccus aureus are distributed in nature (water soil andvegetation) and are also part of the human intestinal

c

a

b

Ultrasound Soxhlet Maceration0

1

2

3

4

5

6

7

8Yi

eld

()

Figure 3 Cactus pear seed oil yield achieved by different extractionmethods abcDifferent letters mean significant differences betweenmethods (p lt 005)

b a b

b

a

c

Ultrasound Soxhlet Maceration0

255075

100125150175200225250275300

DPPH (120583mol TE100 g)ABTS (mg AAE100 g)

Figure 4 Antioxidant activity by ABTS and DPPH of cactus pearseed oil extracted by different methods abcDifferent letters meansignificant differences between methods (p lt 005)

6 Journal of Food Quality

Table 4 Antimicrobial activity of cactus pear seed oil extracted by different methods

Diameter of inhibition zone (mm)Oillowast (+) control (minus) control

Staphylococcus aureus (Gram-positive)Ultrasound 917 plusmn 029a 1889 plusmn 154 NDSoxhlet 950 plusmn 087a 1878 plusmn 164 NDMaceration 978 plusmn 069a 1811 plusmn 117 NDEscherichia coli (Gram-negative)Ultrasound 778 plusmn 019a 1556 plusmn 212 NDSoxhlet 756 plusmn 019a 1533 plusmn 265 NDMaceration 756 plusmn 038a 1400 plusmn 233 NDPseudomonas aeruginosa (Gram-negative)Ultrasound ND 1256 plusmn 038 NDSoxhlet ND 1222 plusmn 038 NDMaceration ND 1278 plusmn 038 NDlowastSeed oil 6667120583L (+) control ampicillin (disc 10 120583g Staphylococcus aureus and Escherichia coli) and streptomycin (disc 10 120583g Pseudomonas aeruginosa) (minus)control hexane ND not detected plusmn standard deviation a Same superscripts indicates that there is no significant difference (p gt 005)

microbiota [38] Pseudomonas aeruginosa besides beingpresent in the intestinalmicrobiota [39] is a bacteria found inthe soil fertilizers and water used for food production [40]and thus it can contaminate fresh or processed food whichis an indicator of inadequate sanitation or improper han-dling during food production [41] Table 4 summarizes theantimicrobial activity of green cactus pear seed oil Extractionmethod did not have a significant effect on the antimicrobialactivity against Staphylococcus aureus and Escherichia colibut the effect was lower than the positive controls Theseresults may be explained by the similar seed oil concentrationand combined action of compounds on the structure ofmicrobial cells [42 43] despite the extraction method Seedoil did not exhibit antimicrobial activity against Pseudomonasaeruginosa probably due to the oil chemical composition thetype of microorganism and the own characteristics of thebacteria [42ndash44]The antimicrobial activity of oils is generallymore effective against Gram-positive bacteria in comparisonto Gram-negative bacteria which are more resistant mainlybecause their outer membrane is less permeable [42 4345 46] The results suggest that Pseudomonas aeruginosawas more resistant than Escherichia coli probably due tothe lipopolysaccharides present in the outer membrane thatrestrict the diffusion of compounds making it less permeable[45]The resistance can also be caused by systems of exclusionpumps that eject antimicrobial compounds from the inside ofthe bacteria before they can cause damage [39 44]

37 Effect of Ultrasound on the Physical Structure Scanningelectron micrographs of the green cactus pear seeds powderbefore and after the ultrasound treatment at magnificationsfactors of 1000x and 500x are shown in Figure 5 Beforethe ultrasound treatment and despite the previous millingprocess in the control sample it was possible to identify intactstructures of the seeds cell as well as some starch granules

(Figure 5(a)) After the ultrasound treatment the cell struc-tural damage and the variations in the shape and size of theparticles were observed (Figure 5(b)) For instance starchgranules were not observed because sonication fragmentedthese particles while cavitation phenomenon disrupted thecell structures of the seeds [47 48]

4 Conclusions

This study demonstrated that response surface methodologyand a second-order polynomial model were effective tools todetermine the optimumprocessing conditions of ultrasound-assisted extraction based on the maximum values of antiox-idant activity The results demonstrated that cactus pearseed oil has good antioxidant and antimicrobial propertiesUltrasound-assisted extraction was comparable to macera-tion but a single ultrasound process yielded less oil andlower antioxidant activity than solvent extraction (Soxhlet)Ultrasound can be considered an alternative technology forthe extraction of seed oil but further research is required todetermine the uses of the seed oil and the technology withinthe food industry and the potential of several ultrasoundcycles at the optimized conditions

Conflicts of Interest

The authors declare that there are no conflicts of interest

Acknowledgments

This work was financially supported by Programa Integral deFortalecimiento Institucional (PIFI 2014-2015) The authorsacknowledge Mexican Association CoMeNTuna (HidalgoMexico) for providing the plant materials Marıa de losAngeles Ortega-Ortega participated in this research and she

Journal of Food Quality 7

(i) (ii)

A A

(a)

(i) (ii)

(b)

Figure 5 Scanning electron micrographs of green cactus pear seed powder before (a) and after (b) ultrasound treatment (i) 1000x (ii) 500xA The black circle shows a starch granule

received her Bachelorrsquos degree in nutrition in the Universi-dad Autonoma del Estado de Hidalgo Mexico (Act no 12872016)

References

[1] L Lozano ldquoEcofisiologıa de la tuna (Opuntia ficusmdashindica (L)Mill)rdquo Horticultura Argentina vol 30 no 72 pp 37ndash52 2011

[2] LMedina-Torres J A Gallegos-Infante R F Gonzalez-Laredoand N E Rocha-Guzman ldquoDrying kinetics of nopal (Opuntiaficusmdashindica) using three different methods and their effect ontheir mechanical propertiesrdquo LWTmdashFood Science and Technol-ogy vol 41 no 7 pp 1183ndash1188 2008

[3] J A Reyes-Aguero J R Aguirre-Rivera and H M HernandezldquoSystematic notes and a detailed description of Opuntia ficusindica (L)Mill (Cactaceae)rdquoAgrociencia vol 39 no 4 pp 395ndash408 2005

[4] H I Jun M N Cha E I Yang D G Choi and Y S KimldquoPhysicochemical properties and antioxidant activity of Koreancactus (Opuntia humifusa) cladodesrdquoHorticulture Environmentand Biotechnology vol 54 no 3 pp 288ndash295 2013

[5] A Rabhi H Falleh F Limam R Ksouri C Abdelly and ARaies ldquoUpshot of the ripening time on biological activitiesphenol content and fatty acid composition of Tunisian Opuntiaficus-indica fruitrdquo African Journal of Biotechnology vol 12 no40 pp 5875ndash5885 2013

[6] M Kaur A Kaur and R Sharma ldquoPharmacological actions ofOpuntia ficus indica a reviewrdquo Journal of Applied Pharmaceuti-cal Science vol 2 no 7 pp 15ndash18 2012

[7] M R Bhatt and P S Nagar ldquoEvaluation of physicochemicalproperty and fatty acid composition ofOpuntia elatior seed oilrdquoJournal of the Professional Association for Cactus Developmentvol 15 pp 13ndash19 2013

[8] M Ennouri H Fetoui E Bourret N Zeghal F Guermazi andH Attia ldquoEvaluation of some biological parameters of Opuntiaficus indica 2 Influence of seed supplemented diet on ratsrdquo Bio-resource Technology vol 97 no 16 pp 2136ndash2140 2006

[9] SAGARPA Secretarıa de Agricultura Ganaderıa DesarrolloRural Pesca y Alimentacion Pliegos de condiciones para eluso de la marca oficial Mexico calidad suprema en tuna 2005httpwwwmexicocalidadsupremaorgassetsgaleriaPC 0462005 Tunapdf

[10] M F Ramadan and J-TMorsel ldquoOil cactus pear (Opuntia ficus-indica L)rdquo Food Chemistry vol 82 no 3 pp 339ndash345 2003

[11] K El-Mostafa Y Kharrassi A Badreddine et al ldquoNopal Cactus(Opuntia ficus-indica) as a source of bioactive compounds fornutrition health and diseaserdquo Molecules vol 19 no 9 pp14879ndash14901 2014

[12] Z Ghazi M Ramdai M L Fauconnier B El Mahi and RCheikh ldquoFatty acids sterols and Vitamin E composition of seedoil of Opuntia ficus indica and Opuntia dilenii from MoroccordquoJournal of Materials and Environmental Science vol 4 no 6 pp967ndash972 2013

[13] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extrac of Laururs nobillis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

8 Journal of Food Quality

[14] A Nawirska-Olszanska A Kita A Biesiada A Sokol-Łętowska and A Z Kucharska ldquoCharacteristics of antioxidantactivity and composition of pumpkin seed oils in 12 cultivarsrdquoFood Chemistry vol 139 no 1ndash4 pp 155ndash161 2013

[15] V Cervantes-Cardoza N E Rocha-Guzman J A Gallego-Infante M Rosales-Castro L Medina-Torres and R FGonzalez-Laredo ldquoActividad antioxidante de extractos desemilla de tres variedades de manzana (Malus domestica Borkh-Rosaceae-)rdquo Boletın Latinoamericano y del Caribe de PlantasMedicinales y Aromaticas vol 9 no 6 pp 446ndash456 2010

[16] M K M Nair P Vasudevan and K Venkitanarayanan ldquoAnti-bacterial effect of black seed oil onListeriamonocytogenesrdquoFoodControl vol 16 no 5 pp 395ndash398 2005

[17] A I Hussain F Anwar S T H Sherazi and R PrzybylskildquoChemical composition antioxidant and antimicrobial activi-ties of basil (Ocimum basilicum) essential oils depends on sea-sonal variationsrdquo Food Chemistry vol 108 no 3 pp 986ndash9952008

[18] W Liu Y J Fu Y G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[19] M T Labuschagne and A Hugo ldquoOil content and fatty acidcomposition of cactus pear seed compared with cotton andgrape seedrdquo Journal of Food Biochemistry vol 34 no 1 pp 93ndash100 2010

[20] S Zine S Gharby and M El Hadek ldquoPhysicochemical char-acterization of Opuntia ficus-indica seed oil from MoroccordquoBiosciences Biotechnology Research Asia vol 10 no 1 pp 99ndash105 2013

[21] R Azuola and P Vargas ldquoExtraccion de sustancias asistida porultrasonido (EUA)rdquoTecnologıa enMarcha vol 20 no 4 pp 30ndash40 2007

[22] M Gao and C Z Liu ldquoComparison of techniques for theextraction of flavonoids fromcultured cells of SaussureamedusaMaximrdquo World Journal of Microbiology and Biotechnology vol21 no 8-9 pp 1461ndash1463 2005

[23] B Karki B P Lamsal S Jung et al ldquoEnhancing protein andsugar release from defatted soy flakes using ultrasound tech-nologyrdquo Journal of Food Engineering vol 96 no 2 pp 270ndash2782010

[24] F Adam M Abert-Vian G Peltier and F Chemat ldquolsquoSolvent-freersquo ultrasound-assisted extraction of lipids from freshmicroal-gae cells a green clean and scalable processrdquo BioresourceTechnology vol 114 pp 457ndash465 2012

[25] T Allaf V Tomao K Ruiz and F Chemat ldquoInstant controlledpressure drop technology and ultrasound assisted extraction forsequential extraction of essential oil and antioxidantsrdquo Ultra-sonics Sonochemistry vol 20 no 1 pp 239ndash246 2013

[26] Z S Zhang L J Wang D Li S S Jiao X D Chen and ZH Mao ldquoUltrasound-assisted extraction of oil from flaxseedrdquoSeparation and Purification Technology vol 62 no 1 pp 192ndash198 2008

[27] T Zhang Z Wang and X Chen ldquoUltrasound-associatedextraction of seed oil of Korean pinerdquo Journal of Forest Researchvol 16 no 2 pp 140ndash142 2005

[28] A M Goula ldquoUltrasound-assisted extraction of pomegranateseed oilmdashkinetic modelingrdquo Journal of Food Engineering vol117 no 4 pp 492ndash498 2013

[29] Q Y Zafra-Rojas N S Cruz-Cansino A Quintero-Lira etal ldquoApplication of ultrasound in a closed system optimum

condition for antioxidants extraction of blackberry (Rubusfructicosus) residuesrdquoMolecules vol 21 no 7 p 950 2016

[30] AOAC Official Methods of Analysis AOAC InternationalGaithersburg Md USA 18th edition 2005

[31] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[32] EM Kuskoski A G Asuero AM Troncoso J Mancini-Filhoand R Fett ldquoAplicacion de diversos metodos quımicos paradeterminar actividad antioxidante en pulpa de frutosrdquo Cienciae Tecnologia de Alimentos vol 25 no 4 pp 726ndash732 2005

[33] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[34] Y Tian Z Xu B Zheng and Y Martin Lo ldquoOptimization ofultrasonic-assisted extraction of pomegranate (Punica grana-tum L) seed oilrdquo Ultrasonics Sonochemistry vol 20 no 1 pp202ndash208 2013

[35] M L Agudo ldquoTecnicas para la determinacion de compuestosantioxidantes en alimentosrdquo 2010 httpwwwanpebadajozesautodidactaautodidacta archivosnumero 9 archivosl amedinapdf

[36] S K Ho C P Tan Y Y Thoo F Abas and C W HoldquoUltrasound-assisted extraction of antioxidants inMisai Kucing(Orthosiphon stamineus)rdquo Molecules vol 19 no 8 pp 12640ndash12659 2014

[37] S R Kirk R Sawyer and H Egan ldquoMetodos quımicos gen-eralesrdquo inComposicion y Analisis de Alimentos pp 25ndash29 Com-panıa editorial continental Ciudad de Mexico Mexico 2002

[38] S Vazquez S OrsquoNeill and M Legnani ldquoImportancia de loscoliformes en los alimentosrdquo 2013 httpwwwmontevideogubuysitesdefaultfilesimportancia de los coliformes en losalimentospdf

[39] C A Gomez-Alvarez A L Leal-Castro M J Perez de Gonza-lez and M L Navarrete-Jimenez ldquoMecanismos de resistenciaen Pseudomonas aeruginosa entendiendo a un peligroso ene-migordquo Revista de la Facultad de Medicina de la UniversidadNacional de Colombia vol 53 no 1 pp 27ndash34 2005

[40] S D Kominos C E Copeland B Grosiak and B Postic ldquoIntro-duction of Pseudomonas aeruginosa in to a hospital via vegeta-blesrdquo Applied Microbiology vol 24 no 4 pp 567ndash570 1972

[41] NOM Norma Oficial Mexicana NOM-210-SSA1-2014 Pro-ductos y servicios Metodos de prueba microbiologicosDeterminacion de microorganismos indicadores Determina-cion de microorganismos patogenos 2014 httpdofgobmxnota detallephpcodigo=539868ampfecha=26062015

[42] F Reyes-Jurado E Palou and A Lopez-Malo ldquoMetodos deevaluacion de la actividad antimicrobiana y de determinacionde los componentes quımicas de los aceites esencialesrdquo TemasSelectos de Ingenierıa de Alimentos vol 8 pp 68ndash78 2014

[43] D Zekaria ldquoLos aceites esenciales una alternativa a los antimi-crobianosrdquo 2015 httpwwwwpsa-aecaesaeca imgs docswpsa1182855355apdf

[44] DM Livermore ldquoMultiplemechanisms of antimicrobial resist-ance in Pseudomonas aeruginosa our worst nightmarerdquo Clini-cal Infectious Diseases vol 34 no 5 pp 634ndash640 2002

[45] M Viuda-Martos M A Mohamady J Fernandez-Lopez et alldquoIn vitro antioxidant and antibacterial activities of essentials oilsobtained from Egyptian aromatic plantsrdquo Food Control vol 22no 11 pp 1715ndash1722 2011

Journal of Food Quality 9

[46] X Feas L M Estevinho C Salinero et al ldquoTriacylglyc-eride antioxidant and antimicrobial features of virgin camelliaoleiferaC reticulata andC sasanqua oilsrdquoMolecules vol 18 no4 pp 4573ndash4587 2013

[47] R G Earnshaw ldquoUltrasound a new opportunity for foodpreservationrdquo in Ultrasound in Food Processing M J W PoveyandT JMason Eds pp 183ndash192 Editorial BlackAcademic andProfessional New York NY USA 1998

[48] M Vinatoru ldquoAn overview of the ultrasonically assisted extrac-tion of bioactive principles from herbsrdquo Ultrasonics Sonochem-istry vol 8 no 3 pp 303ndash313 2001

Research ArticleAntioxidant and Antimicrobial Properties of CactusPear (Opuntia) Seed Oils

Esther Ramiacuterez-Moreno1 Raquel Carintildeo-Corteacutes2 Nelly del Socorro Cruz-Cansino1

Luis Delgado-Olivares1 Joseacute Alberto Ariza-Ortega1 Vanessa Yelina Montantildeez-Izquierdo3

Mariacutea Manuela Hernaacutendez-Herrero3 and Tomaacutes Filardo-Kerstupp4

1Academic Area of Nutrition Health Sciences Institute Autonomous University of Hidalgo State 42160 Pachuca HGO Mexico2Academic Area of Medicine Autonomous University of Hidalgo State Eliseo Ramırez Ulloa 400 42090 Pachuca HGO Mexico3Department of Food Hygiene Faculty of Veterinary Autonomous University of Barcelona 08193 Bellaterra Spain4Academic Area of Chemistry Basic Science and Engineering Institute Autonomous University of Hidalgo StateCarretera Pachuca-Tulancingo Km 45 Mineral de la Reforma 42183 Pachuca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 23 January 2017 Accepted 5 April 2017 Published 26 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Esther Ramırez-Moreno et alThis is an open access article distributed under the Creative CommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Seed oils from two Mexican varieties of cactus pear (green Opuntia albicarpa and red Opuntia ficus indica) were extracted withdifferent solvents (hexane ethanol and ethyl acetate) to evaluate their antioxidant activity The seed oil with higher antioxidantactivitywas selected to evaluate antimicrobial activityThe fatty acid profilewas analyzed by gas chromatography-mass spectrometry(GC-MS) Oil from green cactus pear seeds obtained with ethanol and ethyl acetate exhibited higher antioxidant activity (119901 lt 005)of 323 and 316 120583mol TE20mg (p lt 005) respectively compared to red cactus pear seed oil (asymp274 and 247 120583mol TE20mgwith ethyl acetate and ethanol resp) The oil obtained with ethanol and higher antioxidant activity was used to determine theantimicrobial activity Both cactus pear oils produced a microbial inhibition zone in most of the microorganisms evaluatedparticularly Saccharomyces cerevisiae which had similar diameter (38ndash40mm) The oil fatty acids profiles of both varieties weresimilar and exhibited a high content of linoleic acid while two fatty acids (linolenic and behenic) found in red cactus pear were notobserved in the green variety

1 Introduction

A relatively untapped source of lipid and protein rawmaterialis the by-product of fruit-processing plants Millions ofpounds of fruit seeds are discarded yearly causing disposalproblems while proper utilization of these waste productscould lead to an important new source of oil and meal [1]Seeds of fruits collect at least some cytoplasmic lipid bodies asmajor storage reserve for lipid accumulation [2] Fruit seedsoils are of great interest because they are edible oils with highdegree of unsaturation antioxidant radical scavenging prop-erties [3ndash8] and a broad spectrum of antimicrobial activity[9ndash15] Therefore the oil from plants can be potentially usedby the food industry for the manufacturing of ldquonaturalrdquo orldquogreenrdquo safe foods [16] and extend shelf-life [17 18]

The oil from cactus pear seed has been found to havean appreciable amount of oil with high levels of unsaturatedfatty acids [19] with antioxidant [20 21] and antimicrobialactivity [22] as well as cardioprotective antithrombotic anti-inflammatory antiarrhythmic hypolipidemic and antihy-perglycemic effect [23 24] These properties are of interestfor the pharmaceutical and food industry However theconcentration and effectiveness of these oils may vary amongcultivars or varieties crop environmental factors (eg lighttemperature and type of soil nutrients) or methods andsolvents used for their extraction Therefore the purpose ofthis research was to determine the antioxidant and antimi-crobial activity and fatty acid profile of the oil obtained fromtwo Mexican varieties of cactus pear (Opuntia albicarpa andOpuntia ficus indica) seeds extracted with different solvents

HindawiJournal of Food QualityVolume 2017 Article ID 3075907 8 pageshttpsdoiorg10115520173075907

2 Journal of Food Quality

2 Materials and Methods

21 Plant Material Two Mexican varieties of cactus pear(Opuntia albicarpa and Opuntia ficus indica) fruit green (cvReyna) and red (cv Rojo Pelon) respectively were providedby theMexican association CoMeNTuna (ConsejoMexicanodel Nopal y la Tuna AC Actopan Hidalgo Mexico) Fruitsfree of external injuries were selected washed and manuallypeeled Cactus pear seeds were obtained after juice wasextracted stirring the pulpwith an industrial blender (38BL52LBC10 Waring Comercial USA) and passing it through aconventional strainer The seeds retained were washed in thestrainer with water until pulp residues were removed

22 Powder Seed and Oil Extraction Green cactus pear seeds(GCPS) and red cactus pear seeds (RCPS)were sun-dried andthen grounded (Cyclotec 1093 Tecator Sweden) to a 1mmdiameter mesh and stored at minus32∘C until further analysisTheseed oil was extracted as follows 25 g of powdered seeds wasmixed with 500mL of solvents with varying polarities (hex-ane ethanol and ethyl acetate) and the obtained residue wasreextracted until extraction solvents become colourless Allthe extracts were filtered through filtration paper Whatmannumber 1 and the filtered extracts were collected for furtherdrying and removal of the remaining solvent at 50∘C using arotary evaporator (BUCHI R-200 Switzerland) All extractswere placed in plastic bottles and then stored at minus20∘C untilused The oils obtained were used to further analysis

23 Free Radical Scavenging Assay The free radical scaven-ging activity was measured using 11-diphenyl-2-picrylhy-drazyl (DPPH∙) radical as described byMorales and Jimenez-Perez [25] A volume of 500 120583L of ethanolic DPPH∙ solution(74mg100mL) was added to a sample aliquot of 100 120583Lplaced in vialsThemixturewas left to sit at room temperaturefor 1 h and then was vortexed and centrifuged at 3000 rpm for10 minutesThe absorbance of the supernatant was measuredat 520 nm in amicroplate reader (PowerWave XSUV-Bioteksoftware KC Junior USA) and 120583mol of Trolox equivalentsper 20 milligram (120583mol TE20mg) of sample was obtainedOil samples with best antioxidant capacity obtained from thedifferent solvents were used for the antimicrobial analysis

24 Antimicrobial Activity Eight standard freeze-dried cul-tures of bacteria Candida albicans (ATCC 10231) Escherichiacoli O58H21 (ATCC 10536) Escherichia coli O157H7(CCUG 44857) Staphylococcus aureus (ATCC 13565) Liste-ria monocytogenes (CCUG 15526) Pseudomonas aeruginosa(ATCC 15442) Saccharomyces cerevisiae (CECT 1942) andSalmonella Typhi (CCUG 29478) were obtained in ther-mosealed vials from the Spanish Type Culture Collection(Autonomous University of Barcelona Barcelona Spain)Freeze-dried cultures were rehydrated in tryptone soy brothat 37∘C for 18 h and then were used to inoculate tryptone soyagar and malt extract agar plates all microorganisms wereincubated at 37∘CexceptCandida albicans and Saccharomycescerevisiae which were incubated at 25∘C Individual colonies

were maintained on specific agar slants stored at 4∘C andsubcultured every 15 days

Disc Diffusion Assay Antimicrobial activity of oil extractedfromGCPS andRCPSwas carried out using the disc diffusionmethod [26] Petri plates were filled with sim20mL of steriletryptone soy agar for bacteria and malt extract agar for fungiThe test cultures were swabbed on the top of the solidifiedmedia and allowed to dry for 10 minutes Serial dilutions(10ndash50 120583gmL) of the seed oil from a stock solution (1mgmL)were prepared in 20 DMSO and 10 120583L loaded onto thesterile blank discs (BBL Sensi-Disc) of 6 millimetersof diameter On the media surface the loaded disks wereplaced and left for 30 minutes at room temperature toallow compound diffusion The seed oil was serially dilutedin MuellerndashHinton broth medium and duplicate tubes ofeach dilution (10ndash100 120583gmL) were inoculated with 5 times106 cells of the test bacteria strain and culturesThe antibioticagents Sensi-Disc streptomycin ampicillin and sulfamethox-azoletrimethoprim (BBL Sensi-Disc) were used as positivecontrols at the same concentration level After plates wereincubated at 37∘C for 24 h the diameters of the inhibitionzones were recorded in millimeters Three independentrepetitions were performed and tests were made in triplicate

25 GC-MS Analysis The GC-MS analysis was performedwith a GC-MS HP-5890 (Hewlett-Packard Company PaloAlto California USA) equipped with a Flame IonizationDetector (FID) and a ZB-WAX fused silica capillary column(60m times 025mm id times 025mm film thickness) packedwith 5 phenylmethylpolysiloxane (Phenomenex TorranceCA) To obtain the methyl esters the cactus pear seed oilswere saponified and derivatized using KOH 1N (IUPAC1969) Changes in the fatty acids of the oils samples werecompared against a standard mixture of 37 components offatty acids methyl esters (FAMEs) (Food Industry FAMEsMix Restek) comprised by methyl esters with chains C40C60 C80 C100 C110 C120 C130 C140 C141 C150C151 C160 C161 C170 C171 C180 C181n9c C181n9tC182n6c C182n6t C183n6 C183n3 C200 C201n9 C202C203n6 C203n3 C204n6 C205n3 C210 C220 C221n9C222 C226n3 C230 C240 and C241n9 The samplevolume injected was of 2 120583L (split ratio 20 2) at an injectorand detector temperatures of 225 and 225∘C respectively N2was used as carrier gas at a flow rate of 12mLsdotminminus1 Fattyacids were calculated as percentage of total FAMEs

26 Statistical Analysis All values were obtained by triplicateand expressed as means plusmn standard deviations (SD) Datawere analyzed using the SPSS V15 software (SPSS InstituteInc Cary NC) An ANOVA was carried out to determinedifferences between oils extracted as well as its antimicrobialactivity that were significant at the 5 level of probability anda Tukey test was used for comparison of data

3 Results and Discussion

31 Yield Comparison between Extraction Solvents Hexaneethanol and ethyl acetate were used to extract the oil from

Journal of Food Quality 3

1183

669

1013

511

106

381

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

2

4

6

8

10

12

14

Oil

yiel

d (

)

Figure 1 Oil yields () extracted from GCPS and RCPS withhexane ethanol and ethyl acetate

cactus pear seeds The extraction yields are compared inFigure 1 which shows that the higher amount of oil () wasobtained from the green cultivar and that yield depended onthe solvent used Oil extraction with hexane was higher forboth fruit varieties (1183 for GCPS and 689 for RCPS)followed by ethanol which reached the same yield as ethylacetate for GCPS (asymp10) Ethyl acetate was the least effectivesolvent for RCPS The extraction yields were similar to thosereported (asymp7 to 11) for several varieties of Opuntia ficusindica [27ndash29] This extraction yields will vary depending onseveral factors as fruit variety harvest period maturationgeographic region percentage of oil in the seed and chemicalcompounds found in the source and by the extractionmethod[30] Researchers have determined that solvent extractioncombinedwith othermethods could increase oil yield as highpressure or supercritical fluid combined with solvent reacheda yield of 933 from tobacco seeds (Nicotiana tabacum L)while sonication and Soxhlet reached a 775 and 1372respectively [31]

32 Free Radical Scavenging Activity Solvent extraction isusually used for isolation of antioxidants the extractiondepends on the solvent selected based on the different antiox-idant compounds with varying polarity [32 33] DPPH is astable free radical that accepts an electron or hydrogen radicalto become a stable diamagnetic molecule [34 35]The DPPHassay has also been used to predict the oxidative stability ofedible oils [36 37] The antioxidant activity determined byDPPH of the oil extracted from RCPS and GCPS is shownin Figure 2 Oil from the GCPS extracted with ethanol andethyl acetate exhibited the higher antioxidant activity (119901 lt005) of 323 and 316 120583mol TE20mg extract respectivelyfollowed by RCPS oil extracted with ethyl acetate (274120583molTE20mg extract) and ethanol (247 120583mol TE20mg extract)These results demonstrate that the extraction solvent hada significant effect on the free radical scavenging capacityof the oil where the hexane had the lower values In ourstudy the green variety exhibited a higher antioxidant activityregardless of solvent Different results may depend mainly

e

d

a

c

ab

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

50

100

150

200

250

300

350

휇m

ol T

E20

mg

extr

act

Figure 2 Antioxidant activity of GCPS and RCPS oils extractedwith different solvents andashdDifferent letters above bars indicate thatsamples are significantly different (119901 lt 005)

on the content and concentration of bioactive compounds inthe oil but other factors such as solvent polarity solubilityof the extracts in different testing systems stereoselectivityof the radicals [38] and strong synergism between fattyacids [6] may affect antioxidant activities Other studies havealso reported diverse antioxidant activity among oils fromdifferent Opuntia varieties [20 39 40]

33 Antibacterial and Antifungal Activity The most recom-mended way to prevent or inhibit microbial growth in foodsis the use of food preservatives Essential oils are secondarymetabolites of plants that have wide applications in thefood flavoring and preservative industry [41] Six differentbacterium and two fungi species were used to screen theantimicrobial potential of the oils extracted from the twovarieties of cactus pear seeds Oil extracted with ethanolexhibited the highest antioxidant activity and therefore itwas used to evaluate the antibacterial and antifungal activityFigure 3 shows the results from the microbial assay wheremost microorganisms showed an inhibition zone whenexposed to GCPS and RCPS oils except Salmonella Typhiand Escherichia coli O157H7 (image not shown) From thesetwo microorganisms the first showed an inhibition zonein the presence of antibiotic agents streptomycin (S) ampi-cillin (AMP) and sulfamethoxazoletrimethoprim (STX) indiameters of 146 113 and 273mm respectively (Table 1)while Escherichia coli O157H7 was only inhibited by SXT(253mm) which agrees with other reports of multiantibi-otic resistance of E coli O157H7 due to the presence ofthe gene cluster AMR-SSuT [42] and production of beta-lactamase [43] On the other hand Saccharomyces cerevisiaewas highly inhibited (38ndash40mm) by the extracted oils butgrew in presence of the antimicrobial agents (Figure 3)Similar results were observed for Candida albicans althoughinhibition zones were smaller and similar for both oilsThese observations demonstrate that certain compounds inthe cactus pear seed oil have antimicrobial activity Otherresearchers also reported similar observations for cactus

4 Journal of Food Quality

Table 1 Diameters of growth inhibition zones (mm) in the presence of oil extracted from cactus pear seeds and conventional antimicrobialsA

Microbial cultures Extract Antimicrobial agentGCPS RCPS S AMP SXT

Saccharomyces cerevisiae (CECT1942) 383 plusmn 42a 403 plusmn 45a ND ND NDEscherichia coli O58H21 (ATCC 10536) 119 plusmn 07d 114 plusmn 09d 195 plusmn 14b 178 plusmn 15c 299 plusmn 09a

Escherichia coli O157H7 (CCUG 44857) NDB ND ND ND 253 plusmn 10Staphylococcus aureus (ATCC 13565) 121 plusmn 10c 111 plusmn 11c 183 plusmn 09b 281 plusmn 15a 333 plusmn 19a

Listeria monocytogenes (CCUG15526) 133 plusmn 15c 114 plusmn 09d 213 plusmn 12a 173 plusmn 08c 376 plusmn 18a

Pseudomonas aeruginosa (ATCC15442) 164 plusmn 21c 151 plusmn 20c 201 plusmn 15b 241 plusmn 25a 366 plusmn 29a

Salmonella typhi (CCUG29478) ND ND 146 plusmn 04b 113 plusmn 18c 273 plusmn 08a

Candida albicans (ATCC 10231) 111 plusmn 10a 110 plusmn 18a ND ND NDAInhibition zone diameters for oil and reference antibiotics are means plusmn SE of three replicas GCPS green cactus pear seed oil extract RCPS red cactus pearseed oil extract S streptomycin (10120583gdisc) AMP ampicillin (10 120583gdisc) and SXT sulfamethoxazoletrimethoprim (10120583gdisc) BND not detected activityandashdDifferent letters in the same row indicate significant differences

RG

SXT

S

AMP

(a)

RG

SXT

S

AMP

(b)

R G

SXTS

AMP

(c)

RG

SXTS

AMP

(d)

RG

SXT

S

AMP

(e)

R G

SXT

S

AMP

(f)

Figure 3 Antimicrobial activity of oil extracted from green cactus pear (G) oil extracted from red cactus pear seeds (R) streptomycin(S) ampicillin (AMP) and sulfamethoxazoletrimethoprim (SXT) Candida albicans (ATCC 10231) (a) Escherichia coli O58H21 (ATCC10536) (b) Staphylococcus aureus (ATCC 13565) (c) Listeria monocytogenes (CCUG15526) (d) Pseudomonas aeruginosa (ATCC15442) (e)Saccharomyces cerevisiae (CECT1942) (f)

pear fruit cv Opuntia stricta [44] and for other plants asfennel (Foeniculum vulgare L) and chamomile (Matricariachamomilla L) [5] Differences in the levels of antimicrobialactivity may be partially attributed to variable chemicalcomposition of the oils [45] Mnayer et al [46] suggestedthat oil compounds can act on different bacterial structureswhile Gill et al [47] mentioned that whole oils have a greater

antibacterial activity than the major component mixed sothat minor components are critical for the activity and exerta synergistic effect [16 48 49]

In the present study the antimicrobial activity of cactuspear seed oil was more effective against fungi comparedto bacteria cultures These interesting results suggest thatthere is a link between the oil chemical contents and the

Journal of Food Quality 5

Table 2 Percentages of FAMEs in crude cactus pear seed oil extracts

FAMEs Green cactus pear seed oil extract Red cactus pear seed oil extractC140 0078 plusmn 000 0066 plusmn 001C160 12327 plusmn 009 12887 plusmn 002C161 0429 plusmn 002 0570 plusmn 001C162 0073 plusmn 000 0540 plusmn 000C170 0060 plusmn 001 0075 plusmn 000C180 3436 plusmn 001 3389 plusmn 007C181 16215 plusmn 003 17061 plusmn 001C182 67448 plusmn 008 65407 plusmn 001C183 Ni 0372 plusmn 001C220 Ni 0160 plusmn 001Means of 3 replicates plusmn SE Ni not identified

140

160

181

182

18017

016

116

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(a)14

0 161

162

170

180

181

182

183

220

160

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(b)

Figure 4 Chromatograms of FAMEs of cactus pear seed oil extract (a) Green cactus pear seed oil extract (b) red cactus pear seed oil extractIn both oils extracts were identified myristic (C140) palmitic (C160) palmitoleic (C161 cis-9) hexadecadienoic (C162 cis-9 12) margaric(C170) stearic (C180) oleic (C181 cis-9) linoleic (C182 cis-9 12) except linolenic (C183 cis-6 9 12) and behenic (C220) fatty acids thatwere identified only in red cactus pear seed

antimicrobial activity The membrane disruption could beone mechanism of action by inactivating microbial adhesionenzymes and proteins transport [15 46] RCPS and GCPSextracts inhibited most of the evaluated bacterial and fungispecies (Table 1) however antimicrobial activity was notdetected for Salmonella Typhi which is a gram-negative bac-terium In general gram-negative bacteria have an effectiveoutermembrane that restricts the penetration of amphipathiccompounds and has a mechanism to extrude toxins across[50]Thismay explain the apparent antimicrobial ineffective-ness of the oils against the permeability barrier in addition tothe presence of multidrug resistance encoding plasmids [51]

34 Fatty Acid Profile FAMEs chromatograms and percent-ages are shown in Figure 4 and Table 2 Cactus pear seed oilscontained saturated and unsaturated fatty acids the linoleicfatty acid being the predominant (674 and 654 in GCPSand RCPS oils resp) Minimal amounts of myristic (C140)palmitoleic (C161) hexadecadienoic (C162) and margaric(C170) fatty acids in both oils were also identified The fattyacids profiles of the two cactus pear varieties were similarhowever theGCPS had a slightly higher content of the linoleicacid (C182)while the fatty acids linolenic (C183) and behenic(C220) were in minimal amounts only in the RCPS

Different studies have established that factors as cultivartype temperature and harvest time have a strong influence inparameter as pH Brix vitamin C sugars and fat content [5253] Oumato et al [52] found differences in linoleic fatty acid(C182) content among cactus pear cultivars In other studythe oleic acid (C181) content was significantly influenced bythe cultivar and location interaction [53] providing uniquecharacteristics to the oil

In comparison with other plants oils the linoleic acid(C182) content of the cactus pear fruit was similar to thelevels reported for sunflower oil (62) [54] and higher thanwheat germ oil (5505) [55] and soybean oil (5270)[56] The contents of other FAMEs in cactus pear varietiessuch as palmitic (C160) oleic (C181) and stearic (C180)were similar to those reported for Castilla blackberry (Rubusglaucus Benth) with 1124 passion fruit (Passiflora edulis)with 1547 [57] and grape (Vitis vinifera) with 35 [58]

Other researchers have reported similar fatty acidsprofile to our findings for different plant materials andhave analyzed the antimicrobial effectiveness against dif-ferent microorganisms For instance fatty acids found inAllium cepa were found to effectively inhibit Staphylococcusaureus Bacillus subtilis Enterococcus faecalis Escherichia coliand Klebsiella pneumoniae [59] Oil extracted from SwieteniaMacrophylla king seed oil inhibited growth of S aureus

6 Journal of Food Quality

S Typhimurium and P aeruginosa [60] These studies de-monstrate that seed oil can inhibit fungi and bacteria buttheir efficacy would depend on their concentration levels andspecific pathogen [15]

4 Conclusions

Oil yield from the green cactus pearwas higher in comparisonto the red cultivar andwas also influenced by the solvent usedHexane exhibited high extraction yield while oils extractedwith ethanol had the better antioxidant activity The resultsdemonstrated that oil extracts from both varieties have anoticeable antimicrobial activity against gram-positive andgram-negative bacteria comparable to antimicrobial com-pounds such as ampicillin streptomycin and sulfamethoxa-zoletrimethoprimThis research provides further incentivesto develop additives for the food cosmetic and pharmaceu-tical sectors seeking natural compounds with antimicrobialactivity Further studies are needed to determine the specificcomponent responsible for the antimicrobial activity in cac-tus pear seeds oil and determine the optimum levels of oilextract and the antimicrobial effectiveness in the foodmatrix

Additional Points

Practical Application Our results suggest that the oilsextracted from cactus pear seeds have the potential to be usedas a natural antioxidant and antimicrobial agents by the foodcosmetic and pharmaceutical sectors

Conflicts of Interest

The authors have declared that no conflicts of interest exist

Acknowledgments

This study was possible thanks to the financial supportfrom the Programa Integral de Fortalecimiento Institucional(PIFI 2013ndash2015) Mexico This research project was partiallysupported by the Food Hygiene Department Faculty ofVeterinary from the Autonomous University of BarcelonaSpain The authors acknowledge the Mexican associationCoMeNTuna (Consejo Mexicano del Nopal y la TunaHidalgo Mexico) for providing the plant materials

References

[1] B S Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Acids in Foods and Their Health Implications pp 263ndash301 CRC Press 3rd edition 2007

[2] D J Murphy I Hernandez-Pinzon and K Patel ldquoRole oflipid bodies and lipid-body proteins in seeds and other tissuesrdquoJournal of Plant Physiology vol 158 no 4 pp 471ndash478 2001

[3] A Kedia B Prakash P KMishra andN K Dubey ldquoAntifungaland antiaflatoxigenic properties of Cuminum cyminum (L)seed essential oil and its efficacy as a preservative in storedcommoditiesrdquo International Journal of Food Microbiology vol168-169 pp 1ndash7 2014

[4] S Singh S S Das G Singh C SchuffM P de Lampasona andC A Catalan ldquoComposition in vitro antioxidant and antimi-crobial activities of essential oil and oleoresins obtained fromblack cumin seeds (Nigella sativa L)rdquo BioMed Research Inter-national vol 2014 Article ID 918209 10 pages 2014

[5] M H H Roby M A Sarhan K A-H Selim and K I KhalelldquoAntioxidant and antimicrobial activities of essential oil andextracts of fennel (Foeniculum vulgare L) and chamomile(Matricaria chamomilla L)rdquo Industrial Crops and Products vol44 pp 437ndash445 2013

[6] G Kavoosi A Tafsiry A A Ebdam and V Rowshan ldquoEvalua-tion of antioxidant and antimicrobial activities of essential oilsfrom carum copticum seed and ferula assafoetida latexrdquo Journalof Food Science vol 78 no 2 pp T356ndashT361 2013

[7] S Lalas O Gortzi V Athanasiadis J Tsaknis and I ChinouldquoDetermination of antimicrobial activity and resistance tooxidation of Moringa peregrina seed oilrdquoMolecules vol 17 no3 pp 2330ndash2334 2012

[8] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extract of Laurus nobilis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

[9] R S Bhat and S Al-daihan ldquoAntimicrobial activity of Litchichinensis and Nephelium lappaceum aqueous seed extractsagainst some pathogenic bacterial strainsrdquo Journal of King SaudUniversitymdashScience vol 26 no 1 pp 79ndash82 2014

[10] J M Silvan E Mingo M Hidalgo S de Pascual-Teresa A VCarrascosa and A J Martinez-Rodriguez ldquoAntibacterial activ-ity of a grape seed extract and its fractions against Campylobac-ter spprdquo Food Control vol 29 no 1 pp 25ndash31 2013

[11] K Rakholiya M Kaneria D Desai and S Chanda ldquoAntimi-crobial activity of decoction extracts of residual parts (seedand peels) ofMangifera indica L var Kesar against pathogenicand food spoilage microorganismrdquo in Microbial pathogens andstrategies for combating them science technology and educationA Mendez-Vilas Ed vol 2 pp 850ndash856 2013

[12] N A Hasan M Z Nawahwi and H Ab Malek ldquoAntimicrobialactivity ofNigella sativa seed extractrdquo Sains Malaysiana vol 42no 2 pp 143ndash147 2013

[13] Z I Sajid F Anwar G Shabir G Rasul KM Alkharfy and A-H Gilani ldquoAntioxidant antimicrobial properties and phenolicsof different solvent extracts from bark leaves and seeds ofPongamia pinnata (L) pierrerdquoMolecules vol 17 no 4 pp 3917ndash3932 2012

[14] M Khoobchandani B K Ojeswi N Ganesh et al ldquoAntimicro-bial properties and analytical profile of traditional Eruca sativaseed oil comparisonwith various aerial and root plant extractsrdquoFood Chemistry vol 120 no 1 pp 217ndash224 2010

[15] V Kesari A Das and L Rangan ldquoPhysico-chemical charac-terization and antimicrobial activity from seed oil of Pongamiapinnata a potential biofuel croprdquo Biomass and Bioenergy vol34 no 1 pp 108ndash115 2010

[16] K Carovic-Stanko S Orlic O Politeo et al ldquoComposition andantibacterial activities of essential oils of seven Ocimum taxardquoFood Chemistry vol 119 no 1 pp 196ndash201 2010

[17] MM Tajkarimi S A Ibrahim andDO Cliver ldquoAntimicrobialherb and spice compounds in foodrdquo Food Control vol 21 no 9pp 1199ndash1218 2010

[18] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

Journal of Food Quality 7

[19] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[20] W Liu Y-J Fu Y-G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[21] B Matthaus and M M Ozcan ldquoHabitat effects on yield fattyacid composition and tocopherol contents of prickly pear(Opuntia ficus-indica L) seed oilsrdquo Scientia Horticulturae vol131 pp 95ndash98 2011

[22] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research vol 27 no 14 pp 1305ndash1314 2013

[23] KMobraten TMHaug C R Kleiveland and T Lea ldquoOmega-3 and omega-6 PUFAs induce the same GPR120-mediatedsignalling events but with different kinetics and intensity inCaco-2 cellsrdquo Lipids in Health and Disease vol 12 no 1 ArticleID 101 2013

[24] A BerraaouanA ZiyyatHMekhfi et al ldquoEvaluation of antidi-abetic properties of cactus pear seed oil in ratsrdquo PharmaceuticalBiology vol 52 no 10 pp 1286ndash1290 2014

[25] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[26] P R Murray E J Baron M A Pfaller F C Tenover and R HYolkeManual of Clinical Microbiology 1995 Washington DCUSA

[27] M Ennouri H Fetoui E Bourret N Zeghal and H AttialdquoEvaluation of some biological parameters of Opuntia ficusindica 1 Influence of a seed oil supplemented diet on ratsrdquoBioresource Technology vol 97 no 12 pp 1382ndash1386 2006

[28] Y Habibi L Heux M Mahrouz and M R Vignon ldquoMorpho-logical and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruitsrdquo Carbohydrate Polymers vol 72 no 1pp 102ndash112 2008

[29] MMoudenM Boujnah S Salmaoui S Zantar and A DouiraldquoEffect of two extraction methods and harvest period andperformance there statement of fatty oils of figs pear seedrdquoInternational Journal of Pure amp Applied Bioscience vol 4 no1 pp 1ndash8 2016

[30] A El Finti M Belayadi R El Boullani F Msanda and A ElMousadik ldquoAssessment of some agro-technological parametersof cactus pear fruit (Opuntia ficus-indica Mill) in Moroccocultivarsrdquo Journal of Medicinal Plants Research no 7 pp 2574ndash2583 2013

[31] S Majdi M Barzegar A Jabbari and M Agha AlikhanildquoSupercritical fluid extraction of tobacco seed oil and itscomparison with solvent extraction methodsrdquo Journal of Agri-cultural Science and Technology vol 14 no 5 pp 1043ndash10512012

[32] E M Marinova and N V Yanishlieva ldquoAntioxidative activity ofextracts from selected species of the family Lamiaceae insunflower oilrdquo Food Chemistry vol 58 no 3 pp 245ndash248 1997

[33] Y-Y Soong and P J Barlow ldquoAntioxidant activity and phenoliccontent of selected fruit seedsrdquo Food Chemistry vol 88 no 3pp 411ndash417 2004

[34] J R Soares T C P Dinis A P Cunha and L M AlmeidaldquoAntioxidant activities of some extracts of Thymus zygisrdquo FreeRadical Research vol 26 no 5 pp 469ndash478 1997

[35] I GulcinMOktay E Kirecci and O I Kufrevioglu ldquoScreeningof antioxidant and antimicrobial activities of anise (Pimpinellaanisum L) seed extractsrdquo Food Chemistry vol 83 pp 371ndash3822003

[36] J Lee H Chung P-S Chang and J Lee ldquoDevelopment of amethod predicting the oxidative stability of edible oils using 22-diphenyl-1-picrylhydrazyl (DPPH)rdquo Food Chemistry vol 103no 2 pp 662ndash669 2007

[37] A Fazio P Plastina J Meijerink R F Witkamp and BGabriele ldquoComparative analyses of seeds of wild fruits ofRubus and Sambucus species from Southern Italy fatty acidcomposition of the oil total phenolic content antioxidant andanti-inflammatory properties of the methanolic extractsrdquo FoodChemistry vol 140 no 4 pp 817ndash824 2013

[38] R L Prior X Wu and K Schaich ldquoStandardized methods forthe determination of antioxidant capacity and phenolics infoods and dietary supplementsrdquo Journal of Agricultural andFood Chemistry vol 53 no 10 pp 4290ndash4302 2005

[39] A Cardador-Martınez C Jimenez-Martınez and G SandovalldquoRevalorization of cactus pear (Opuntia spp) wastes as a sourceof antioxidantsrdquo Ciencia e Tecnologia de Alimentos vol 31 no3 pp 782ndash788 2011

[40] Z Ghazi M Ramdani M Tahri et al ldquoChemical compositionand antioxidant activity of seeds oils and fruit juicerdquo Journalof Materials and Environmental Science vol 6 no 8 pp 2338ndash2345 2015

[41] V K Bajpai K-H Baek and S C Kang ldquoControl of Salmonellain foods by using essential oils a reviewrdquo Food ResearchInternational vol 45 no 2 pp 722ndash734 2012

[42] K Ziebell R P Johnson A M Kropinski et al ldquoGenecluster conferring streptomycin sulfonamide and tetracyclineresistance in Escherichia coli O157H7 phage types 23 45 and67rdquo Applied and Environmental Microbiology vol 77 no 5 pp1900ndash1903 2011

[43] O Chandra K J Putra and I Wayan ldquoAntibiotic resistanceprofiles of Escherichia coli O157H7 in cattle at Suth-KutaBadung Regency Bali Indonesiardquo Global Veterinaria vol 15no 5 pp 480ndash484 2015

[44] E Moosazadeh M R Akhgar and A Kariminik ldquoChemicalcomposition and antimicrobial activity of Opuntia stricta Fessential oilrdquo Journal of Biodiversity and Environmental Sciencesvol 4 pp 94ndash101 2014

[45] S Burt ldquoEssential oils their antibacterial properties and poten-tial applications in foods - a reviewrdquo International Journal ofFood Microbiology vol 94 no 3 pp 223ndash253 2004

[46] D Mnayer A-S Fabiano-Tixier E Petitcolas et al ldquoChemicalcomposition antibacterial and antioxidant activities of sixessentials oils from the Alliaceae familyrdquo Molecules vol 19 no12 pp 20034ndash20053 2014

[47] A O Gill P Delaquis P Russo and R A Holley ldquoEvaluationof antilisterial action of cilantro oil on vacuum packed hamrdquoInternational Journal of FoodMicrobiology vol 73 no 1 pp 83ndash92 2002

[48] M Turgis K D Vu C Dupont and M Lacroix ldquoCombinedantimicrobial effect of essential oils and bacteriocins againstfoodborne pathogens and food spoilage bacteriardquoFoodResearchInternational vol 48 no 2 pp 696ndash702 2012

[49] H Zengin and A H Baysal ldquoAntibacterial and antioxi-dant activity of essential oil terpenes against pathogenic andspoilage-forming bacteria and cell structure-activity relation-ships evaluated by SEM microscopyrdquo Molecules vol 19 no 11pp 17773ndash17798 2014

8 Journal of Food Quality

[50] G Tegos F R Stermitz O Lomovskaya and K Lewis ldquoMul-tidrug pump inhibitors uncover remarkable activity of plantantimicrobialsrdquo Antimicrobial Agents and Chemotherapy vol46 no 10 pp 3133ndash3141 2002

[51] M Baltazar A Ngandjio K E Holt et al ldquoMultidrug-resistantSalmonella enterica serotype typhi Gulf of Guinea RegionAfricardquo Emerging Infectious Diseases vol 21 no 4 pp 655ndash6592015

[52] J Oumato S ZriraM Boujnah andB Saidi ldquoEffect ofmaturitystage onmorphological and chemical characteristics ofOpuntiaficus indica from Moroccordquo International Journal of Innovationand Applied Studies vol 20 no 1 pp 400ndash410 2017

[53] M deWit A Hugo N Shongwe and R van derMerwe ldquoEffectof cultivar season and locality on lipid content and fatty acidcomposition of cactus pear seed oilrdquo South African Journal ofPlant and Soil no 33 pp 279ndash288 2016

[54] Australian Oilseeds Federation Incorporated 2015 Section 1ldquoQuality standards technical information amp typical analysisrdquono 14 pp 31ndash40 2016 (Accessed 1 November 2015)

[55] A Awad A Adel A A M Nady and AAE ldquoWheat germ anoverview on nutritional value antioxidant potential andantibacterial characteristicsrdquo Food and Nutrition Sciences vol6 no 2 pp 265ndash277 2015

[56] P Pumrojana S Terapuntuwat and P Pakdee ldquoInfluence offatty acid composition of soybean oil vs beef tallow on egg yolkfatty acid profiles of laying hensrdquo Pakistan Journal of Nutritionvol 14 no 7 pp 383ndash387 2015

[57] A F Ceron M O Osorio and B A Hurtado ldquoIdentificacionde acidos grasos contenidos en los aceites extraıdos a partir desemillas de tres diferentes especies de frutasrdquo Acta Agronomicavol 61 no 2 pp 126ndash132 2012

[58] J Orsavova L Misurcova J Vavra Ambrozova R Vicha andJ Mlcek ldquoFatty acids composition of vegetable oils and itscontribution to dietary energy intake and dependence of car-diovascular mortality on dietary intake of fatty acidsrdquo Interna-tional Journal of Molecular Sciences vol 16 no 6 pp 12871ndash12890 2015

[59] M Derbali A Elaissi I Cheraief and M Aouni ldquoFatty acidcomposition and antimicrobial activity against sensitive andmulti-drug resistant bacteria of Tunisian Allium cepa seedextractrdquo Research amp Reviews Journal of Hospital and ClinicalPharmacy vol 2 no 2 pp 30ndash34 2016

[60] M B Suliman A H Nour M M Yusoff P Kuppusamy A RYuvaraj and S A Mazza ldquoFatty acid composition and antibac-terial activity of Swietenia macrophylla king seed oilrdquo AfricanJournal of Plant Science vol 7 no 7 pp 300ndash303 2013

Page 6: Natural Preservatives to Improve Food Quality and Safety

Contents

Natural Preservatives to Improve Food Quality and SafetyMoreno Bondi Andrea Laukovaacute Simona de Niederhausern Patrizia Messi and Chrissanthy PapadopoulouVolume 2017 Article ID 1090932 3 pages

Natural Food Additives and Preservatives for Fish-Paste Products A Review of the Past Present andFuture States of ResearchKhawaja Muhammad Imran Bashir Jin-Soo Kim Jeong Hyeon An Jae Hak Sohn and Jae-Suk ChoiVolume 2017 Article ID 9675469 31 pages

Development of a Chemically Defined Medium for Better Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31Wenli Liu Lanwei Zhang and Huaxi YiVolume 2017 Article ID 9017452 8 pages

Lipid Oxidation Color Changes and Microbiological Quality of Frozen Beef Burgers Incorporatedwith ShiraziThyme Cinnamon and Rosemary ExtractsHadi Hashemi Gahruie Seyed Mohammad Hashem HosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan ShadVolume 2017 Article ID 6350156 9 pages

Optimization of Ultrasound Extraction of Cactus Pear (Opuntia ficus indica) Seed Oil Based onAntioxidant Activity and Evaluation of Its Antimicrobial ActivityMariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-Cansino Ernesto Alaniacutes-GarciacuteaLuis Delgado-Olivares Joseacute Alberto Ariza-Ortega Esther Ramiacuterez-Morenoand Joseacute de Jesuacutes Manriacutequez-TorresVolume 2017 Article ID 9315360 9 pages

Antioxidant and Antimicrobial Properties of Cactus Pear (Opuntia) Seed OilsEsther Ramiacuterez-Moreno Raquel Carintildeo-Corteacutes Nelly del Socorro Cruz-Cansino Luis Delgado-OlivaresJoseacute Alberto Ariza-Ortega Vanessa Yelina Montantildeez-Izquierdo Mariacutea Manuela Hernaacutendez-Herreroand Tomaacutes Filardo-KerstuppVolume 2017 Article ID 3075907 8 pages

EditorialNatural Preservatives to Improve Food Quality and Safety

Moreno Bondi1 Andrea Laukovaacute2 Simona de Niederhausern1

Patrizia Messi1 and Chrissanthy Papadopoulou3

1Department of Life Sciences University of Modena and Reggio Emilia Via G Campi 287 Modena Italy2Institute of Animal Physiology Slovak Academy of Sciences Soltesovej 4-6 040 01 Kosice Slovakia3Microbiology Department Faculty of Medicine School of Health Sciences University of Ioannina Ioannina Greece

Correspondence should be addressed to Moreno Bondi morenobondiunimoreit

Received 12 October 2017 Accepted 12 October 2017 Published 12 December 2017

Copyright copy 2017 Moreno Bondi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Food products can be contaminated by a variety of path-ogenic and spoilage microbiota the former causing food-borne diseases and the latter causing significant economiclosses for the food industry due to undesirable effects onthe food properties According to the Centers for DiseaseControl and Prevention (CDC) each year in the UnitedStates 48 million people get sick 128000 are hospitalizedand 3000 die because of foodborne infections Howeveralthough foodborne outbreaks are well recorded sporadiccases are not because not all patients visit the doctor orenter the hospital and the causative agent is not alwaysidentified A considerable number of foodborne pathogens ofgreat public health importance (eg VTEC E coli serotypesCampylobacter jejuni Listeria monocytogenes and Yersiniaenterocolitica) have emerged during the recent two decadescausing severe illness and foodborne outbreaks worldwide

Microbial food spoilage is also an area of immenseconcern for the food industry It is estimated that as much as25 of all food produced is lost after harvest due to microbialactivity While the growth of spoilage microbiota in foodsis not harmful for the human health it has negative impacton the shelf-life textural characteristics and overall qualityof the finished products affects the consumer choices andresults in significant commercial losses Thus prevention orinhibition of microbial growth in foods is of outmost impor-tance for the current globalized food production Hencethere is still the need for new processing methods to be usedeither alone or in combination with the already existing onesable to reduce or eliminate foodborne pathogens and spoilagebacteria

Chemical additives have been extensively used to preventthe survival and proliferation of microorganisms but their

safety and impact on human health are under discussionSince the reduction or elimination of pathogens and spoilagemicroorganisms in food is the foremost priority the currenttrends in food processing are focusing on the use of naturalcompounds which are considered as safe alternatives andsatisfy the consumer preferences for more ldquogreen foodsrdquoHence the increased awareness on the safety of food additivesand preservatives and the consumerrsquos trend to avoid foodscontaining chemicals which in the long-term may haveadverse impact on their health have generated a significantnumber of studies and publications on the potential useof various natural substances recognized as GRAS (Gener-ally Recognized as Safe) to be used as food preservativesChemical compounds added to foods as antioxidant agentsare also of concern particularly when important proteinsources (eg burgers steaks) are involved in the daily diet ofwesternized consumer living in the developed countries [1 2]Synthetic antioxidants such as BHT TBHQ and BHA havedemonstrated various adverse effects on the human healthincluding allergy headache asthma and dermatitis Recentstudies on the utilization of natural antioxidants (eg herbalessential oils and extracts) indicate their capacity and safety[3 4] Also the antimicrobial properties of natural substancessuch as plant essential oils and extracts have been extensivelystudied with promising results [5] The proper recycling anduse of fruit-processing plants by-products like fruit seedsor skins discarded and piling up in huge amounts everyyear are of great interest for the food industry particularlytheir potential to be a useful source of oil and meal [6]Additionally the oil from plant seeds can be used by thefood industry for manufacturing more ldquonaturalrdquo or ldquogreenrdquofoods and also can sufficiently extend the shelf-life of the

HindawiJournal of Food QualityVolume 2017 Article ID 1090932 3 pageshttpsdoiorg10115520171090932

2 Journal of Food Quality

food product [7] The oils derived from fruit seeds oils mayalso have some more useful properties beyond being justldquoediblerdquoThe oil derived from the seed extract of twoMexicanvarieties of cactus pear (Opuntia albicarpa and Opuntia ficusindica) has been found to have sufficient antioxidant andantimicrobial properties [8] Furthermore some biologicalactive compounds produced by microorganisms are widelyused in the food industry as well A good alternative toconventional chemically synthesized food preservatives is theuse of natural antimicrobials such as bacteriocins producedby lactic acid bacteria (LAB) with Nisin being officiallyemployed by the food industry and thus the most widelyused Bacteriocins are peptides actually microbial toxinsproduced from various microorganisms and so far someof them (eg enterocins produced mostly by enterococci)have shown remarkable antimicrobial potential and theirapplication as a natural barrier against pathogens and foodspoilage has been proven to be very efficient when used inthe form of purified or semipurified extracts or as protectivecultures [9 10] Therefore as the developments in foodpreservation are focusing on the implementation of naturalantimicrobials and antioxidants this special issue exploresthe potential of alternatives to currently used preserva-tives through the publication of five high-quality articleswhich aim to address recent advancements in the field ofnatural food preservatives and antioxidants The prospectto replace synthetic preservatives with natural substanceshas been demonstrated by comparing the effects of Shirazithyme cinnamon and rosemary extracts (denoted as naturalantioxidants) with those of the synthetic antioxidant BHT onprotein and lipid oxidations physicochemical microbial andsensory characteristics of frozen beef burgers during storageSpecifically the oxidative stability of the beef burgers contain-ing Shirazi thyme cinnamon and rosemary extracts was welldemonstrated and the antibacterial activitywas documentedas the total microbial counts of the tested burgers were wellbelow the maximum allowed limit Besides the evaluationof the antimicrobial and antioxidant properties of naturalsubstances it is important to optimize their recovery Withregard to bacteriocins to enhance Enterocin Y31 productionand simplify the steps of separation and purification a propersimplified and defined medium (SDM) has been developedfor the Enterococcus faecium Y31 growth and enhancementof the Enterocin Y31 production The bacterial growth didnot result in Enterocin Y31 production in MRS medium andtherefore both the growth rate and the EnterocinY31 produc-tion were set as the goal for the investigation Single omissionexperiments revealed that 5 gL NaCl five vitamins twonucleic acid bases MgSO4sdot7H2O MnSO4sdot4H2O KH2PO4K2HPO4 CH3COONa fourteen amino acids and glucosewere essential for the adequate strain growth and EnterocinY31 production As a result a novel simplified and definedmedium (SDM) was formulated containing 30 ingredientsin which the Enterocin Y31 production yield was higherwhen compared to either MRS or CDM The developmentof the SDM improved the Enterocin Y31 production andsimplified the steps of purification (only two steps) whichis very promising and increases its potential applicationsReferring to seedsrsquo oils the optimization of the extraction

conditions of cactus pear seed oil has been obtained usingultrasound in a closed system based on the antioxidantactivity and using response surface methodology The yieldextraction and antioxidant and antimicrobial activity werecompared with those obtained using both conventional andunconventional methods such as Soxhlet and macerationusing heat agitation or long extraction times microwavesupercritical fluids and ultrasound-assisted extraction inan open and in a closed system The results have shownthat ultrasound exhibited lower oil yield and antioxidantactivity but had the potential to achieve comparable resultsif multiple ultrasound extractions are performed in the timeneeded by conventional methods Seed oils showed similarantimicrobial activity despite the extraction method and canbe an alternative extraction method of seed oils from fruitssuch as cactus pear Lastly the replacement of chemicaladditives with natural compounds has been addressed for fishfoods as well Fish-paste products also known as fish cakes orsurimi-based products are worldwide favorites Surimi a wetprotein concentrate of fish muscle is used as an intermediateraw material to produce surimi seafood The flavor texturetaste shelf-life and market value of surimi-based productsdepend on several factors including the additives used toprepare the surimi While preparing surimi with chemicaladditives several problems have been observed such as alack of unique characteristics inferior acceptability and poorfunctionality In this context a systematic review of fish-paste products prepared using natural food additives (eganimal seafood and plant source additives herbs and orientalmedicines grains and roots and functional food materials)has been performed which summarizes the existing relevantknowledge in the production of new value-added foodstuffsof interest for the surimi industry

In conclusion this special issue offers to the readers thechance to be informed on the recent advancements relatedto the antimicrobial and antioxidant properties of naturalsubstances that are of interest for the contemporary foodindustry Their prospective use in the food production hasthe potential to lead towards the production of safer andhealthier foods not excluding their contribution to a moreefficient preservation of the environment when chemicalswill be replaced with natural substances

Moreno BondiAndrea Laukova

Simona de NiederhausernPatrizia Messi

Chrissanthy Papadopoulou

References

[1] G Comi E Tirloni D AndyantoMManzano and L IacuminldquoUse of bio-protective cultures to improve the shelf-life andthe sensorial characteristics of commercial hamburgersrdquo LWT -Food Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[2] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWT - FoodScience and Technology vol 68 pp 385ndash390 2016

Journal of Food Quality 3

[3] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[4] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[5] H Sakkas P Gousia V Economou V Sakkas S Petsios and CPapadopoulou ldquoIn vitro antimicrobial activity of five essentialoils on multidrug resistant Gram-negative clinical isolatesrdquoJournal of Intercultural Ethnopharmacology vol 5 no 3 pp212ndash218 2016

[6] B Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Fatty Acids in Foods and their Health ImplicationsThirdEdition vol 20073230 of Food Science and Technology pp 263ndash301 CRC Press 3rd Edition edition 2007

[7] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

[8] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research (Formerly Natural Product Letters)vol 27 no 14 pp 1305ndash1314 2013

[9] R Iseppi F Pilati M Marini et al ldquoAnti-listerial activity of apolymeric film coated with hybrid coatings doped with Ente-rocin 416K1 for use as bioactive food packagingrdquo InternationalJournal of Food Microbiology vol 123 no 3 pp 281ndash287 2008

[10] A Laukova and P Turek ldquoEffect of enterocin 4231 in Slovak fer-mented salami puchov after its experimental inoculation withListeria Innocua Lirdquo ACTA Scientiarum Polonorum TechnologiaAlimentaria vol 10 no 4 pp 423ndash431 2011

Review ArticleNatural Food Additives and Preservatives forFish-Paste Products A Review of the Past Present andFuture States of Research

Khawaja Muhammad Imran Bashir1 Jin-Soo Kim2 Jeong Hyeon An1

Jae Hak Sohn13 and Jae-Suk Choi13

1Seafood Research Center IACF Silla University 606 Advanced Seafood Processing Complex Wonyang-roAmnam-dong Seo-gu Busan 49277 Republic of Korea2Department of Seafood and Aquaculture Science Gyeongsang National University 38 Cheondaegukchi-gilTongyeong-si Gyeongsangnam-do 53064 Republic of Korea3Food Biotechnology Division of Bioindustry College of Medical and Life Sciences Silla University 140 Baegyang-daero700 beon-gil Sasang-gu Busan 46958 Republic of Korea

Correspondence should be addressed to Jae-Suk Choi jsc1008sillaackr

Received 9 June 2017 Revised 15 August 2017 Accepted 17 September 2017 Published 27 November 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Khawaja Muhammad Imran Bashir et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Fish-paste products also known as fish cakes or surimi-based products are worldwide favorites Surimi a wet protein concentrateof fish muscle is used as an intermediate raw material to produce surimi seafood The flavor texture taste shelf-life and marketvalue of surimi-based products depend on the source of the fish meat type of applied heat treatment and additives used toprepare the surimi While preparing surimi with chemical additives several problems have been observed such as a lack of uniquecharacteristics inferior acceptability and poor functionality Various types of fish-paste products have been developed by usingdifferent ingredients (eg vegetables seafood herbs and oriental medicines grains and roots including carrots and functionalfood materials) However a systematic review of fish-paste products prepared using natural food additives has not yet beenperformedTherefore the quality characteristics of fish-paste products and their functionalities were elucidated in this study Withthe increasing demand for surimi seafood products the functional properties physiochemical properties and shelf-life of surimi-based products need to be improved This review will aid the preparation of new value-added products in the surimi industry

1 Introduction

Fish-paste products popularly known as fish cakes areproduced from frozen surimi (ie they are a kind of surimi-based product) and are popular in Korea and Japan [1] Inthe Korean Food Standards Codex fish cakes are known asa processed marine product comprising salt-soluble proteinsisolated from fish meat [2] Fish muscle is mechanicallydeboned washed with water and blended with cryoprotec-tants to prepare a wet concentrate of proteins called surimiSurimi is a Japanese term that is also known as washed fishmince It is a refined fish myofibrillar protein manufacturedthrough numerous step-by-step processes including headinggutting filleting deboning (mincing) washing dewatering

refining mixing with cryoprotectants freezing and metaldetection for HACCP [3] The myofibrillar proteins make itan excellent ingredient for developing food products It hasexcellent gelling properties and forms strong and elastic gelsupon heating [4]

The setting and deformation are important to preparesurimi and surimi-based products Setting also known asldquosuwarirdquo in Japanese is a very important process which hasa significant influence on the physiological and rheologicalproperties of surimi-based products Setting is a vital processin the quality estimation of surimi because it helps to improvethe water-holding capacity as well as the gel texture of surimi-based productsWhen fishmince paste (sol) is heated at a lowtemperature (up to 50∘C) a loose network (suwari) is formed

HindawiJournal of Food QualityVolume 2017 Article ID 9675469 31 pageshttpsdoiorg10115520179675469

2 Journal of Food Quality

from myosin and actomyosin molecules this process isreferred to as setting Setting is species dependent and occursover a range of temperatures (up to 50∘C) and to a varyingextent As the temperature is increased to around 70∘Csuwari is partially disrupted to form a broken net structure(modori) a phenomenon attributed to the dissociation ofmyosin from actin and the possible fragmentation of the actinfilament [5ndash7]

Most of the surimi-based products are different types offish-paste products while less than 10 include fish burgersfish ham and fish sausages [3] Surimi-based products areprepared by mixing the raw or frozen surimi with saltsand other ingredients molded and heated to form the finalproduct in the specified shape and texture and pasteurizedbefore packaging The kind of heat treatment depends on theflavor texture and appearance of the desired final productand may include broiling steaming deep-fat frying andboiling [8] while fish-paste products in South Korea aremostly prepared by frying [9] Textural characteristics suchas gel strength are the major determinant of surimi priceand quality [10] Several studies have attempted to enhancethe textural quality of surimi or surimi-based products usingvarious protein additives [11ndash14]

Surimi quality and gelling property are mainly affectedby both intrinsic factors (effect of fish species seasonalitysexual maturity and freshness or rigor) and extrinsic fac-tors (harvesting handling water characteristics processingtime and temperature solubilization of myofibrillar proteinsduring processing the activity of the endogenous or addedprotein oxidants and proteolytic enzymes washing cyclessalinity and pH) [3 134] Surimi forms thermoirreversiblegels upon heating which do not deform with further changein the temperature This phenomenon of surimi and surimi-based products is similar to that observed in other proteinssuch as egg white milk-lactoglobulin and wheat glutenAdditionally surimi produces gels of very high deformabilityand strength This heat-induced gelation property of surimimakes it a very valuable food ingredient [134]

The gel-forming ability and capacity of surimi areadversely affected by the proteolytic degradation of myofib-rillar proteinsThe presence of indigenous proteinases causedgel softening in surimi made from fish species for examplethreadfin bream [135] arrow tooth flounder [136] Pacificwhiting [137] and lizard fish and bigeye snapper [20 59]Various active proteinases in fish muscle are responsible forsoftening of the surimi gels Nakamura and Ogawa and Anet al testified that cathepsins L and B were the most activecysteine proteinases in Pacific whiting surimi and fish filletsrespectively [7 138] The myofibril-associated proteinasesobserved in lizardfish surimi were serine proteinases andcysteine while a serine proteinase was reported in the bigeyesnapper surimi [20 59]

Seasonal analysis of the compositional properties ofAlaska pollock and Pacific whiting showed higher proteincontents in winter while the moisture contents were higherin summer [139 140] Surimi prepared from cold-water fishspecies with low thermostability of myofibrillar proteinsmakes setting easier Normally a myofibrillar protein withlow thermostability is optimum to do setting because its

reactivity is increased due to the loose internal structure bysodium chloride addition and heat denaturation In contrastthe myofibrillar protein of tropical fish species with high heatstability is difficult to denature and form the myofibrillarprotein network structure in surimi [3]

Several research groups have studied ways to enhance thequality of surimi-based products by investigating the changesin microbial content enzyme activity nutrient content andacceptability characteristics the use of raw materials thestandardization of the manufacturing process storage andmarketing Natural and chemical food-grade additives suchas konjac flour proteinase inhibitors egg white and hydro-colloids have been used to enhance the gelling properties ofsurimi [12 17 20 23 34 141ndash143] The trypsin inhibitor inegg white plays a major role in improving the gel strengthof surimi The addition of egg white inhibits the proteolyticactivity of the modori-inducing enzyme in fish meat andsuppresses the decrease of elasticity in surimi Serum pro-teins have strong inhibiting abilities against the action ofvarious proteases with different active centers such as SHgroups and serine groups In addition they also containtransglutaminases that accelerate the setting Egg white andserum proteins also play an important role in inhibiting theenzymatic activity of the parasites Apart from the use ofadditives gel strengthening can be achieved by treating thegels at low temperatures (0ndash40∘C) before cooking [144 145]Furthermore the gel quality of surimi and surimi-basedproducts can also be enhanced by using alternate fish speciesor by acid and alkali washing to increase the myofibrillarprotein concentrations [7 146 147]

Surimi production worldwide reached around800000MT by 2011-2012 [3] while South Korea alonecontributed approx 156000MT in 2013 Over the yearsthe size of the market for Korean fish-paste products hasgradually increased reaching sim350 million US dollars in2013 (based on the amount produced) [148] Howevermanufacturers have had several problems in producingsurimi-based products such as a lack of unique character-istics and inferior acceptability and functionality Thereforethere have been several attempts to develop new fish-pasteproducts with excellent acceptability and functionalityTo this end numerous types of fish-paste products havebeen developed using various natural ingredients such asvegetables seafood animals plants herbs and orientalmedicines seaweed and functional food materials It is ofworldwide interest to use these natural food preservativesinstead of chemical or synthetic ones However to date nosystematic review of fish-paste products supplemented withvarious food raw materials has been performed Thereforethe quality characteristics of fish-paste products and theirfunctionalities were elucidated in this study

2 Improvement of the Gel Properties ofFish-Paste Products

Various food additives derived from animals (eg beefswine and chicken) seafood (eg fish invertebrates) plants(eg legumes cereals) sugars polyols and functional mate-rials used in fish-paste products to improve their gelling

Journal of Food Quality 3

capabilities and strength are listed in Table 1 and describedbelow

21 Animal Source Additives Various food-grade proteaseinhibitors from animal sources are used to enhance thephysical properties of surimi-based products as well to pre-vent the protein degradation The ability of beef plasma andother food-grade additives in surimi and fishmince preparedfrom Pacific whiting (Merluccius productus) was studied byMorrissey et al [12] The strongest proteolytic inhibitionwas observed with beef plasma protein at a concentrationas low as 1 Reppond and Babbitt reported the increase ingel strength of gels prepared by arrow tooth flounder at aconcentration of 2 with a yellow hue color [16] Weeras-inghe et al characterized the inhibitory activity of these food-grade inhibitors and reported that the inhibitory activity wasmainly because of specific serine proteinase inhibitors [17]The addition of 2 dried bovine plasma to steamed fish-pasteslightly increased the chewiness and hardness but it showeda negative effect on the gel strength [18] Duangmal andTaluengphol reported that the higher levels of beef plasmaprotein unfavorably affected gel characteristics of red tilapiasurimi gels [19]

The effect of porcine plasmaprotein on the bigeye snapper(Priacanthus tayenus) surimi gel characteristics was investi-gated by Benjakul et al [14]The gels supplemented with 05porcine plasma protein had the highest level of deformationand breaking force Benjakul and colleagues later reportedthe effect of porcine plasma protein on the gel characteristicsof surimi from bigeye croaker (Pennahia macrophthalmus)bigeye snapper (P tayenus) barracuda (Sphyraena jello)and threadfin bream (Nemipterus bleekeri) [20] The porcineplasma protein was effective in increasing the deformationand breaking force of kamaboko gels Higher breaking forcesand levels of deformation occurred when chicken plasmaprotein was supplemented to sardine kamaboko gels at levelsup to 2 [21] The inhibitory activities of cysteine proteinaseinhibitor fraction from chicken plasma on Pacific whitingand arrow tooth flounder mince were reported by Rawdkuenet al [22] Furthermore similar results were observed intheir extended study onPacificwhiting surimi where chickenplasma at a level of 2 inhibited the degradation of myosinheavy chain proteins [23]

Ovomucoid is a mucoprotein obtained from egg whitethat has been tested for its potential as a gel-degradationinhibitor [24 25] The addition of 2 ovomucoid couldincrease the breaking strength and gel deformation [28]The autolytic activities of lizardfish (Saurida tumbil) surimiand mince under the application of protease inhibitors wereinvestigated by Yongsawatdigul and Piyadhammaviboon[26] At all preincubation conditions egg white enhancedthe gel-forming capability of S tumbil surimi to a greaterextent than did whey protein concentrateThe addition of 1egg white and preincubation at 25∘C increased the breakingforce by twofold Campo-Deano and Tovar [27] reportedthat the addition of egg albumen at 15 and 2 for Alaskapollock and Pacific whiting surimi respectively enhancedthe gel strength of crab sticks According to Hunt et al theincorporation of 2-3 special dried egg white improved

the gel textural characteristics of Alaska pollock and Pacificwhiting surimi [28]

Whey is the complete set of proteins isolated fromthe watery portion of milk Whey protein is comprisedof 20 milk protein and 80 casein [149] Whey proteinconcentrates have generally been used as an emulsifierfiller water binder protein supplement foam stabilizer andthickener as well as gelling agent [150] Rawdkuen andBenjakul investigated the effect of whey protein concentrateon the gelling characteristics of surimi prepared fromgoatfish(Mulloidichthys vanicolensis) bigeye snapper (P tayenus)lizardfish (S tumbil) and threadfin bream (N bleekeri) [29]All the tested surimi supplemented with 3 whey proteinconcentrate displayed inhibitory activity against autolysis andsignificantly reduced gel whiteness However better water-holding capacity was obtained by increasing concentrationsof whey protein concentrate

Plasma proteins produced from pig cow and chickenbyproducts are relatively affordable and easily collectiblesources [143 151 152] However outbreaks of foot-and-mouthdisease avian influenza andmad cow disease as well as a banonproteins frompig bone and skin in some states for religiouscauses have made it essential to search alternative sources[153 154] Various fish plasma proteins have been testedincluding those from rainbow trout and salmon [31 35 36]

22 Seafood Additives The effects of shrimp head proteinhydrolysate fromdifferent shrimp namely black tiger shrimp(Penaeus monodon) northern pink shrimp (Pandalus eous)and endeavour shrimp (Metapenaeus endeavouri) on thegelling properties of lizardfish (Saurida spp) surimi wereinvestigated by Ruttanapornvareesakul et al [30] It wasreported that the freeze-induced denaturation of lizardfishmuscle protein could be reduced by the supplementation ofshrimp head protein hydrolysate at a concentration of 5resulting in higher Ca-ATPase activity and gel strength Theeffects of rainbow trout plasma proteins on the gelling prop-erties of surimi prepared by Alaska pollock were investigatedby Li et al [31] Gel degradation deformation the breakingforce water-holding capacity and whiteness enhanced withincreasing amounts of rainbow trout plasma protein anddecreased at higher concentrationsThe rainbow trout plasmaprotein at a concentration of 075mgg could be used asa potential protease inhibitor to inhibit gel weakening inAlaska pollock surimi Li et al reported the higher inhibitoryactivities of the recombinant chum salmon cystatin againstautolysis of Alaska pollock surimi [155]

Fish gelatin is extracted from the collagen of fish skinand it is used as a food additive Hernandez-Briones et alstudied the functional and mechanical properties of Alaskapollock surimi gels while using fish gelatin as an additive[32] The increasing concentration of gelatin affected thewhiteness but the sensory panelists were unable to detect itThese results showed that fish gelatin was not effective as afunctional additive in Alaska pollock surimi Nevertheless itcould be added at up to 10 gkg without negatively affectingthe mechanical properties of surimi Yin et al reported asignificant improvement in the endogenous transglutaminaseactivity of Alaska pollock surimi prepared with nanoscaled

4 Journal of Food Quality

Table1Naturalfood

additiv

esused

toim

provethe

gelpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Animalsource

additiv

es

Beefplasma

hydrolysate

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Atlanticmenhaden

(Brevoortia

tyrann

us)

Alaskap

ollock

(Theragra

chalcogram

ma)

Moistu

recontentproteincontent

cook

inglossw

ater-holding

capacitytexturetorsio

ntest

05

ndash15

[15]

Bovine

plasma

Bostaurus

Heatedin

awater

bath

Powder

Arrow

toothflo

under

(Atheresthessto

mias)

Walleye

pollo

ck

Moistu

recontentpu

nchtorsion

colortest

2[16]

Beefplasma

protein

Bostaurus

mdashPo

wder

Pacific

whitin

g(M

erlucciusp

rodu

ctus)

Proteincontentinhibitory

assay

4[17]

Drie

dbo

vine

plasma

Bostaurus

Steaming

Powder

Alaskap

ollock

(Tchalco

gram

ma)

Nutrie

ntcontentpH

water-holding

capacitytexture

and

sensoryevaluatio

n2

[18]

Beefplasma

protein

Bostaurus

Heatedin

awater

bath

Drie

dpo

wder

Redtilapia

(Oniloticus

xO

placidus)

Colortextureexpressiblewater

protein

totalsulfhydrylcon

tent

2gkg

[19]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Bigeye

snapper

(Pria

canthu

stayenus)

Expressib

ledrip

amou

ntcolor

texturesetting

cond

ition

s05

[14]

Porcinep

lasm

aprotein

Susscrofadomesticus

Heatedin

awater

bath

Drie

dpo

wder

Threadfin

bream

(Nem

ipterus

bleekeri)Bigeyes

napp

er(Ptayenus)

Baracuda

(Sphyraena

jello)and

Bigeye

croaker

(Penna

hiamacrophthalmus)

Trichloroacetic

acid-solub

lepeptidescolortextureprotein

content

05

[20]

Chickenplasma

protein

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Sardine

(Sardinella

gibbosa)

Colortextureexpressiblemoistu

re

proteincontentautolysis

activ

ity2

[21]

Cyste

inep

roteinase

inhibitorfrom

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Arrow

toothflo

under

(Astomias)Pacific

whitin

g(M

produ

ctus)

Autolysis

andinhibitory

activ

ity

pHprotein

content

3[22]

Chickenplasma

Gallusgallusd

omesticus

Heatedin

awater

bath

Drie

dpo

wder

Pacific

whitin

g(M

produ

ctus)

Torsionandfracture

test

dynamic

rheologicalattribute

2[23]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[24]

Ovomucoid

Gallusgallusd

omesticus

Heatedin

awater

bath

Ovomucoid

solutio

nAlaskap

ollock

Puncture

test

texturalandsensory

attributes

2[25]

Eggwhite(EW)

Gallusgallusd

omesticus

Heatedin

awater

bath

Powder

Lizardfish(Saurid

atumbil)

mince

andsurim

iAu

tolytic

activ

itytexturalattributes

EW1

[26]

Eggalbu

min

Gallusgallusd

omesticus

Heatedin

thec

ooking

roller

Eggwhite

itself

Surim

i-based

crab

sticksfrom

Alaskap

ollock

(AP)

Pacific

whitin

g(PW)

(Mprodu

ctus)

Transie

nttest

streng

thtest

texture

dynamicrheologicaland

physical

attributes

AP

15

PW2

[27]

Journal of Food Quality 5

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Regu

lard

riedegg

white(REW

)speciald

riedegg

white(SEW

)liq

uideggwhite

(LEW

)

Gallusgallusd

omesticus

Heatedin

awater

bath

Spray-dried

powder

Pacific

whitin

g(M

produ

ctus)

Totalsulfhydrylgroup

sfracture

test

dynamicrheologicalattribute

SEW2-3

[28]

Wheyprotein

concentrate

Bostaurus

Heatedin

awater

bath

Wheyprotein

concentrate

Bigeye

snapper(Ptayenu

s)Goatfish

(Mulloidich

thys

vanicolen

sis)

Threadfin

bream

(Nblee

keri)

and

Lizardfish(Stum

bil)

Water-holding

capacitycolor

autolytic

activ

ity3

[29]

Seafoo

dadditiv

esSh

rimphead

proteinhydrolysate

from

northern

pink

shrim

pendeavou

rshrim

pand

blacktig

ershrim

p

Pand

alus

eous

Metapenaeus

endeavouri

Pena

eusm

onodon

Heatedin

awater

bath

Drie

dmatter

Lizardfish

(Saurid

aspp)

Gelstr

engthcolorgel-forming

abilityC

a-AT

Pase

activ

ity5

[30]

Rainbo

wtro

utplasmap

rotein

Oncorhynchu

smykiss

Heatedin

awater

bath

Freeze-drie

dplasma

Alaskap

ollock

Proxim

atea

nalysisw

ater-holding

capacitycolortextureprotein

content

075

mgg

[31]

Fish

gelatin

Com

mercialfishgelatin

(Gelatin

Rousselot)

Heatedin

awater

bath

Powder

Alaskap

ollock

Colorm

echanicalfunctio

nal

sensoryattributes

10gkg

[32]

Nanoscaled

fish-bo

neof

Pacific

whitin

gMprodu

ctus

Heatedin

awater

bath

Powder

Alaskap

ollock

Texturescanning

electron

microscop

y1g10

0g[33]

Nanoscaled

fish-bo

ne(N

FB)+

driedeggwhite

(DEW

)

Mprodu

ctusGallus

gallu

sdom

esticus

Heatedin

awater

bath

Powder

Pacific

whitin

g(M

produ

ctus)

Rheologicaland

texturalattributes

DEW

1+

10mgNFB

Cag

surim

ipaste

[34]

Salm

onbloo

dplasma

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)

Scanning

electronmicroscop

yproteincontentdynamic

rheologicalattributes

1g10

0g[35]

6 Journal of Food QualityTa

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Freeze-drie

dchinoo

ksalm

onplasma(

FSP)

and

concentrate

salm

onplasma

(CSP

)

Oncorhynchu

stsh

awytscha

Ohm

icheating

Freeze-drie

dplasma

Pacific

whitin

g(M

produ

ctus)surim

iand

Salm

onmince

Proteolytic

inhibitio

nautolysis

proteincontent

Salm

onminceC

SPgt

FSP

Pacific

whitin

gsurim

iFSP

[36]

Partially

purifi

edtrypsin

inhibitor

from

ther

oeof

yello

wfin

tuna

fish

Thun

nusa

lbacares

Heatedin

awater

bath

Freeze-drie

dBigeye

snapper

(Pria

canthu

smacracanthu

s)Proteolysis

colorw

ater-holding

capacitygellin

gprop

ertie

s3g

100g

[37]

Squidink

tyrosin

ase(SIT)

+tann

icacid

(TA)

Todarodesp

acificus

Heatedin

awater

bath

Mixture

Sardine

(Sardinella

albella)

Tyrosin

asea

ctivityinvitro

oxidationassaycolortexturaland

sensoryattributes

SIT

500U

gprotein+

TA1

[38]

Plantsou

rcea

dditives

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soybean

protein

Wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[39]

Soyprotein

eggwhite(EW)

wheyprotein

concentrate

(WPC

)La

ctalbumin

(LA)

milk

proteiniso

late

(MPI)

Glycinem

ax

Gallusgallusd

omesticus

Bostaurus

Coo

kedin

aste

amcooker

Powder

AlaskaP

ollock

(Tchalco

gram

ma)

Textureexpressib

lemoistu

recontentwater

retentionprop

ertie

sEW

andMPI

[4041]

Legu

mes

eed

extractfrom

blackcowpea

whitecowpea

soybeanseeds

Mun

gbean

peanut

Vignaun

guicu

lata

Glycinem

axVignaradiata

Arachish

ypogaea

mdash

Freeze-drie

dproteinase

inhibitor

extracts

Threadfin

bream

(Nem

ipterid

ae)

ThermalstabilitypHprotein

contentproteinase

inhibitory

assay

Blackcowpea

soybeanseeds

30mgg

[42]

Legu

mes

eed

extractfrom

Cow

pea

pigeon

pea

bambara

grou

ndnu

ts

Vignaun

guicu

lata

Cajanu

scajan

Vo

andzeia

subterranea

mdashPartially

purifi

edTrypsin

Threadfin

bream

(Nem

ipterid

ae)

Sarcop

lasm

icmod

ori-ind

ucing

proteinase

activ

itycolor

30ku

nits

g[43]

bambara

grou

ndnu

tprotein

isolate

Vignasubterranea

Heatedin

awater

bath

Powder

Threadfin

bream

(Nblee

keri)

Colorautolysis

025

g100g

[44]

Soyproteiniso

late

Glycinem

axHeatedin

awater

bath

Com

mercial

soyprotein

isolate

(JinQ

ui1200)

Alaskap

ollock

(Tchalco

gram

ma)

Com

mon

carp

(Cyprin

uscarpio)

Totaln

itrogen

andmoistu

recontentgelstre

ngthcolor

10

[45]

Journal of Food Quality 7Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Soybeanprotein

wheatgluten

Glycinem

ax

Triticum

aestivum

Heatedin

awater

bath

Soyprotein

wheatgluten

Alaskap

ollock

(Tchalco

gram

ma)

Expressib

lewaterm

oistu

recontent

gelstre

ngthphysic

alattributes

5[46]

Dietary

fiber

(DF)

from

peaa

ndchicory+

microbial

transglutaminase

(MTG

ase)

Cichorium

intybu

sPisum

sativ

umHeatedin

awater

bath

Powder

Hake(Mcapensis)

Gilthead

seabream

(Sparusa

urata)

Seab

ass(Dice

ntrarchu

slabrax)

Meagre(Argyrosomus

regius)

Dyn

amicrheologicalattributes

MTG

ase100U

g[47]

Proteiniso

lates

from

Mun

gbean

(MBP

I)black

bean

(BBP

I)bam

bara

grou

ndnu

t(BG

PI)

Phaseolusa

ureus

Phaseolusv

ulgarisV

igna

subterranea

mdashFreeze-drie

dpo

wder

mdash

Scanning

electronmicroscop

yproteolytic

autolyticandtrypsin

inhibitory

activ

ityassaycolor

texturetrichloroacetic

acid-solub

lepeptidec

ontent

1g10

0g[48]

Partially

purifi

edtrypsin

inhibitor

from

adzukibean

Vignaangularis

Heatedin

awater

bath

Freeze-drie

dpo

wder

Threadfin

bream

(Nblee

keri)

Proteincontenttexturecolor

trypsin

inhibitory

activ

ityautolytic

activ

ityassay

3g10

0g[49]

Amylose(A)a

ndam

ylop

ectin

(AP)

mdashHeatedin

awater

bath

Powder

Walleye

pollo

ck(T

chalcogram

ma)

Gelationandbreaking

strength

Amylose70+

Amylop

ectin

4

[50]

Wheatsta

rch

Triticum

aestivum

Heatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Com

pressio

ntest

dynamic

viscoelasticityscann

ingele

ctron

microscop

y

Starch10g

+Surim

i10g

[51]

Natives

weetp

otato

starch(N

SPS)

and

Mod

ified

sweet

potato

starch

(MSP

S)

Ipom

oeabatatas

Heatedon

acontrolled

stress

rheometer

Powder

Alaskap

ollock

(T

chalcogram

ma)

Dyn

amicrheologicalattributes

5[52]

Potato

starch

Solanu

mtuberosum

Heatedin

the

Krehalon

ecasin

gfilm

Powder

Pacific

sand

lance(Am

modytes

personatus

Gira

rd)

Proxim

atea

nalysis

protein

compo

sition

colorfoldingtext

texturalandsensoryattributes

8[53]

Rice

flour

Oryza

sativa

Fried

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorrheologicaland

sensoryattributes

10ndash15

[54]

Rice

flour

Oryza

sativa

Fried

Powder

Threadfin

bream

(Nem

ipterid

ae)

Moistu

recontentpH

color

texturalandsensoryattributes

50

[55]

Rice

flour

Oryza

sativa

Fried

Powder

Goldenthreadfin

bream

(Nem

ipterusv

irgatus)

Gelstr

engthsensoryattributes

14

[56]

Cryoprotectantsa

ndhu

mectants

Xanthan(X)

locustbean

(LB)

gumsa

loneX

LB

ratio

Ceratoniasiliqua

Heatedin

awater

bath

Powder

Silver

carp

(Hypophthalm

ichthys

molitrix)

Torsiontest

gel-formingability

mechanicalattributes

XLB

025075

[57]

Pectin

gum

(HM

LM)+

CaCl2

mdashHeatedin

awater

bath

Gum

and

powder

Silver

carp

(Hm

olitrix)

Water-holding

capacitym

echanical

andtexturalattributes

Pectin

gum1+

CaCl202

[58]

8 Journal of Food Quality

Table1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Chito

san7B

from

praw

nshell

Not

mentio

ned

Heatedin

awater

bath

Not

mentio

ned

Barred

garfish

(Hem

iramphus

far)

ProteincontentSE

Mtextural

attributes

1[59]

Konjac

glucom

annan

aqueou

sdisp

ersio

nAm

orphophallu

skonjac

Heatedin

awater

bath

Aqueou

sdispersio

n

Giant

squid(D

osidicu

sgigas)

Alaskap

ollock

(T

chalcogram

ma)

ProteinsolubilitypH

texturaland

viscoelasticrheologicalattributes

1[60]

Carrageenan+

NaC

lorK

Clmdash

Heatedin

awater

bath

Hydrocollo

idAlaskap

ollock

(T

chalcogram

ma)

Gelstr

engthcolorcompressio

ntest

Carrageenan1+

KCl15

[61]

Amorphophallu

skonjac

flour

(AKF

)Am

orphophallu

skonjac

Heatedin

awater

bath

Flou

rGiant

squid(D

gigas)

Water

retentionabilitycolor

texturalandsensoryattributes

10

[62]

NaC

l+high

hydrostatic

pressure

(HHP)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Proxim

atea

nalysis

FTIR

SEM

colormechanicalrheologicaland

sensoryattributes

HHP

300MPa

+NaC

l03

[63]

Sodium

chlorid

esugarspolyols

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Larim

ichthys

polya

ctis)

Water

activ

ityV

BNcolor

moistu

recontent

Sodium

chlorid

e4

Glucose10

Glycerin

10

[64]

Starchglycine

sodium

lactate

mdashHeatedin

awater

bath

Powdera

ndliq

uid

Yello

wcorvina(

Lpolya

ctis)

Water

activ

ityV

BNcolorm

oistu

recontent

Sodium

lactate75

[65]

Glycerol

mdashSteamed

Liqu

idMackerel(Scom

berjaponicu

s)andBrazilian

sand

perch

(Pseud

opercis

semifa

sciata)

Water

activ

itytexturaland

sensory

attributes

20

[66]

Naa

ndCa

salts

ofpo

lyuron

ides

and

carboxym

ethyl

cellu

lose

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gel-

streng

theningeffects

2ndash6

[67]

L-ascorbicacid

(AsA

)and

dehydro-L-

ascorbicacid

(DAs

A)

mdashHeatedin

awater

bath

Powder

Alaskap

ollock

(T

chalcogram

ma)

Gelstr

engthanalysis

DAsA

10120583

gg

[68]

Sodium

-L-

ascorbate

(SA)

mdash

Steamed

inNojax

cellu

lose

casin

g

Powder

Alaskap

ollock

(T

chalcogram

ma)

pHtexturaland

sensoryattributes

02

[69]

120596-3

fatty

acids

from

algae

Not

mentio

ned

Heatedin

awater

bath

Oil

Cod

(Gadus

morhu

a)TB

ARS

fattyacid

contentcolor

500m

g85

g[70]

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)

Microscop

icob

servation

viscosity

gel-formingability

10

[71]

Journal of Food Quality 9Ta

ble1Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atmentcon

ditio

nRe

ferences

Eicosapentaeno

icacid

docosahexaenoic

acid

mdashHeatedin

awater

bath

Oil

Walleye

pollo

ck(T

chalcogram

ma)Th

readfin

bream

(Nem

ipterid

ae)White

croaker(Ge

nyonem

uslin

eatus)

andJapanese

jack

mackerel(Trachu

rus

japonicus)

Proxim

atea

nalysis

color

water-holding

capacityphysic

alattributes

5ndash30

[72]

120596-3

PUFA

s-ric

hoils

Flaxseedalgae

menhaden

krillblend

(flaxseed

algae

krill

811)

Heatedin

awater

bath

Oil

Alaskap

ollock

(T

chalcogram

ma)

Torsiontest

andrheological

attributes

9g10

0g[73]

Ethano

licKiam

woo

dextract

(EKW

E)+

commercialtann

in(C

T)

Hopea

sp

Heatedin

awater

bath

Overdrie

dpo

wder

Strip

edcatfish

(Pangasiu

shypophthalmus)

pHV

BNT

BARS

color

TCA-

solublep

eptid

emoistu

re

proteincontents

texturalattributes

EKWE

008

CT002

ndash004

[74]

Cocon

uthu

skextractw

ithethano

l60(C

HE-E6

0)

80(C

HE-E8

0)

Cocosn

ucifera

Heatedin

awater

bath

Freeze-drie

dpo

wder

Sardine

(Salbella)

Totalpheno

licexpressible

moistu

reT

CA-solub

lepeptideand

proteincontents

colortextual

rheologicalandsensoryattributes

CHE-E6

00125

[75]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Solutio

nMackerel

(Rastre

lligerk

anagurta)

SEMexpressiblemoistu

reprotein

contentcolortexturalandsensory

attributes

OFA

040

OTA

050

OCF

050

OCT

010

[76]

Oxidizedph

enolic

compo

unds

ferulic

acid

(OFA

)tann

icacid

(OTA

)catechin

(OCT

)caffeicacid

(OCF

)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Bigeye

snapper

(Ptayenus)

SEMexpressiblemoistu

reprotein

andfre

eaminoacid

contentcolor

texturalandsensoryattributes

OFA

020

OTA

005

OCF

015

OCT

005

[77]

Eggwhitepo

wder

(EW)whey

protein

concentrate(WPC

)

Gallusgallusd

omesticus

Triticum

aestivum

Heatedin

awater

bath

Powdera

ndconcentrate

Lizardfish

(Stum

bil)mince

andsurim

i

Autolytic

activ

ityT

CA-solub

leoligop

eptid

esprotein

content

texturalattributes

EW4

WPC

4

[26]

Zinc

sulfate

(ZnS

O4)sodium

tripolypho

sphate

(STP

P)

mdash

Heatedin

awater

bath

inpo

lyvinyli-

dene

casin

g

Powder

Yello

wstr

ipetrevally

(Sela

roideslep

tolep

is)

Expressib

lemoistu

relipid

phosph

olipidand

proteincontent

Ca-ATP

asea

ctivitycolortextural

attributes

ZnSO460120583

molkg+

STPP

05

[78]

SEMscann

ingelectro

nmicroscop

yFT

IRFou

rier-transfo

rminfrared

spectro

scop

yVBN

volatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stancesT

CAtric

hloroacetic

acid

10 Journal of Food Quality

fish bones [33] Furthermore a study on the rheologicaland textural attributes of Pacific whiting surimi showedthat slow heating and the addition of nanoscaled fish bonessignificantly enhanced gel strength [34]

Fowler and Park reported an enhanced gelling strengthand effectively inhibited proteinase activity in Pacific whitingsurimi gels heated ohmically [35] Fowler and Park laterstudied the effects of salmon plasma from Chinook salmonon proteolytic inhibition of surimi [36] Salmon plasmaeffectively inhibited both serine and cysteine proteases as wellas proteases isolated from Pacific whiting Salmon plasmaconcentrated by ultrafiltration performed slightly better thanfreeze-dried salmon plasma at inhibiting autolysis in salmonmince

Klomklao et al reported inhibitory activity of a par-tially purified trypsin inhibitor (TIYTR) from yellowfintuna (Thunnus albacores) on the gelling characteristics ofbigeye snapper (Priacanthus macracanthus) surimi [37] Theincorporation of TIYTR with a level of 30 g100 g resultedin the enhanced deformation and breaking force of surimigels suggesting that the TIYTR could be employed as anaffordable and alternative proteinase inhibitor to enhance thegel strength of surimi prepared by bigeye snapper

Vate and Benjakul investigated the effects of squid inktyrosinase mixtures of tannic acid and protein on the gellingcharacteristics of sardine surimi [38] The highest deforma-tion and breaking force were obtained when surimi gels wereallowed to react for 90min while being supplemented with1 tannic acid and 500Ug squid ink tyrosinase proteinHowever gels with an added squid ink tyrosinasetannicacid mixture were whiter than the control The surimi gelssupplemented with squid ink tyrosinasetannic acid mixtureshowed the maximum overall acceptance scores suggestingthat it could be used as an additive to increase the surimi gelproperties

23 Plant Source Additives The chicken plasma proteinegg white and beef plasma protein are considered as themost effective protease inhibitors for surimi [17 22 23156] However the use of chicken plasma and beef plasmaprotein has been forbidden because of the occurrence of avianinfluenza and mad cow disease respectively In additionhigher concentrations of beef plasma proteins have also beenassociated with off-flavors while egg white is expensive andhas an unwanted egg-like odor [29 156] Additionally veg-etarians would not want to consume surimi-based productsprepared with additives from animal or even seafood sourcesTherefore alternate food-grade additives are still desired toenhance the gel strength of surimi without affecting thecustomer demandVarious natural additives derived from theplant sources have been briefly described below

231 Legumes Theeffects of vegetable protein contentmois-ture heating and setting conditions on the physical attributesof kamaboko were examined by Yamashita [39] A firm gelwas obtained at 60∘C for kamaboko with soybean proteinand at 80∘C with wheat gluten When the kamaboko gelswere supplemented with 5 vegetable protein the changes injelly strength softness and expressiblewater of the kamaboko

with wheat gluten were somewhat greater than those of thekamaboko with soybean protein According to the results ofChung and Lee the addition of plant proteins including soyprotein isolate lactoalbumin and wheat gluten remarkablylessened the strength of non-animal protein-incorporatedsurimi gels [40] The textural and sensory attributes offiberized surimi gel products were categorized as an increasein overall textural desirability and an increase in gel strengthIn another study egg white and milk protein isolate showedhigher water retention ability than whey protein concentratesoy protein isolate and lactoalbumin [41]

Protein isolates from legume seeds can be used as alter-nate protein additives for the quality improvement of surimigels Legume seed isolates comprise trypsin inhibitors andhave been used as the protease inhibitor in the prepara-tion of surimi and surimi-based products [42 43] Ben-jakul et al reported higher protease inhibitory activities ofinhibitor extracts from soybean and black cowpea seeds[42] A reduced gel-degradation activity (modori) and ahigh thermal stability were reported In another study theyreported inhibitory effects of proteinase inhibitor extractsfrom Bambara groundnuts (Voandzeia subterranea) pigeonpea (Cajanus cajan) and cowpea (Vigna unguiculata) onautolysis and gel-degradation activity (modori) of threadfinbream surimi [43] The whiteness of surimi gels reducedslightly with the addition of proteinase inhibitor Similarresults were obtained by Oujifard and colleagues [44] TheBambara groundnut protein extracts at a level of 025 g100 gshowed improved autolytic inhibition deformation andbreaking force in surimi prepared by threadfin bream (Nbleekeri) [44] However a slight reduction in whiteness wasobserved at increasing levels of Bambara groundnut proteinisolates These studies show that the addition of Bambaragroundnut protein extracts at a suitable level could serve asan alternative food inhibitor to enhance the gelling propertiesof surimi

Plant protein isolates mainly soy protein isolates havebeen used in the surimi industry because of their safety andrational price [45] Luo et al indicated the legumin andvicilin two main legume seed storage proteins as bindersand cogelling agents in surimi gels [45] Protease inhibitorsisolated from legume seeds not only can help to reduce thegel-degradation process in surimi but can also improve thesurimi gel properties by acting as filler or binder Luo etal reported higher breaking force and quality characteristicsof silver carp surimi when supplemented at a ratio of 10soy protein isolate [46] Cardoso et al studied the effects ofdietary fiber and microbial transglutaminase from chicoryand pea on the rheological properties of protein paste fromgilthead sea bream hake meagre and seabass [47] It wasfound that a high degree of protein denaturation boosted gelhardness while a low degree of protein denaturation createdgels with high deformability It shows that the addition ofmicrobial transglutaminase could serve as a possible additivefor gels of those species having lesser protein unfoldingability

Kudre et al studied the effects of black bean (Phaseolusvulgaris) and mung bean (Phaseolus aureus) protein isolateson gelling properties and proteolysis of sardines (Sardinella

Journal of Food Quality 11

albella) surimi [48] An increase in deformation breakingforce and water-holding capacity as well as a lower levelof degradation was observed while the whiteness of kam-aboko gels reduced slightly Therefore mung bean or blackbean protein isolates could be effectively used to retardthe proteolysis in sardine surimi leading to improved gelstrength Klomklao and Benjakul studied the effects of thepartially purified trypsin inhibitor from adzuki bean on thegelling properties and proteolysis of threadfin bream (Nbleekeri) surimi [49] An increase in autolysis and inhibitoryactivity against sarcoplasmic proteinases aswell as an increasein deformation and breaking force of kamaboko gel wasobserved at increasing levels of trypsin inhibitor while gelwhiteness decreased slightly

232 Starch Starch is widely used to make fish-paste prod-ucts as it enhances elasticity and increases the weight ofthe products In attempts to control thermal stability stick-iness andor wetness under different serving and storageconditions the functional characteristics of surimi seafoodproducts have been widely studied using modified starchesStarch is the second most abundantly used ingredient in themanufacturing of fish-paste products because of its higherwater-holding ability and capacity to replace fish proteinspartially while preserving the desired gel features at a reducedcost [69 157ndash161]

Kim et al reported a positive correlation between theamount of added starch and the quality of the food products[162] Konoo et al studied the effects of adding starch andamylose to amylopectin contents of starch on the gela-tion properties of frozen walleye pollack surimi [50] Thebreaking strength of gel was not affected by the changein amylose amylopectin ratio However it increased as thecontent of amylose increased in pregelatinized starch [51]A lower packing effect was observed at 90∘C which hypoth-esized that the gelatinization of starch in fish meat can beprevented at this temperature A strong correlation betweenthe amylose to amylopectin contents and the textural andrheological properties of starch-containing surimi gels wasalso reported by Lanier et al [134]

The addition of normal and modified potato or sweetpotato starch resulted in reductions in the characteristicstorage modulus of surimi sols during heating [52] Surimigels supplemented with potato starch showed the highestfirmness and cohesiveness Yoo reported the best texturalproperties of the sand lance (Ammodytes personatus) fish-paste products at a level of 8 potato starch [53] Thesestudies show that potato or sweet potato starch can also beused as a potent food additive for the production of surimi

233 RiceRice Flour Fish meat and wheat flour are themajor ingredients used for the production of surimi-basedproducts Rice flour however can be an important ingredientto enhance the rheological properties of surimi-based prod-ucts Several attempts have been made to evaluate the poten-tial of rice flour as an alternate of wheat flour in the prepara-tion of surimi products [41] The effect of rice flour additionmethods and milling types on the sensory and rheologicalattributes of surimi products were studied by Cho et al [54]

Roll-mil rice at a concentration of 10ndash15 displayed highergel strength and sensory properties which show that roll-millrice had strong potential for replacing wheat flourThe surimiproducts containing rice flour showed similar rheological andsensory characteristics to those of a finest commercial surimiproduct Hence rice flour might be an effective alternative towheat flour for high-quality surimi products

To replace wheat flour Kwon and Lee examined thequality characteristics of fried fish cakes containing rice flour[55] The total content of corn starch and rice flour was2883 of the total content of fish cake doughThere were nonoteworthy differences in the pHmoisture level appearancecolor flavor taste and overall acceptance as compared tothe control group The addition of 50 rice flour to surimi-based products could be an effective way to increase thecontent of rice flour without decreasing texture acceptabilityYoon et al optimized the content of water and rice flourin surimi-based products [56] The surimi-based productsmanufactured under optimal environment were comparablein gel strength to the commercial products However highersensory evaluation scores were observed compared to thoseof the commercial products These studies advocate that therice flour not only can be employed as an alternative to wheatflour but can also be used to enhance the quality of surimiand surimi-based products

234 Potato Powder The food additives extracted frompotato and potato protease inhibitors used in the preparationof fish-paste products are discussed in Sections 21 232 and244

24 Cryoprotectants and Humectants To inhibit denatura-tion and to lessen the damage of gel quality during coldstorage cryoprotectants are usually added to surimi productsPolyunsaturated fatty acids protein additives polyols sugarsamino acids salts and plant extracts are frequently usedas cryoprotectants and humectants to avoid fluctuationsin myofibrillar proteins promoted by freezing storage orthawing [163] Mechanical properties of surimi gels can beimproved by the addition of numerous hydrocolloids such askonjac carrageenan locust bean xanthan gum and differentmicrobial transglutaminases during the preparation of surimiproducts [57 164ndash166] In contrast the addition of alginateshas been reported to weaken surimi gels [69]

241 Saccharides Xanthan is a nongelling polysaccharideproduced by the aerobic fermentation of Xanthomonascampestris [167] The property of xanthan to form highlyviscous and stable solution at low levels makes it acceptablein the food industry [168] Xanthan displays quite remarkablesynergistic interactions with other nongelling polysaccha-rides of the galactomannan family leading to increases in gelformation and viscosity [168 169] The three commerciallyavailable galactomannans are tara gum locust bean gum andguar gum

The impact of low methoxyl pectin on the mechanicalproperties of silver carp surimi gels was studied by Barreraet al [58] An increase in hardness shear stress and water-holding capacity of the surimi gel was observed while no

12 Journal of Food Quality

significant improvement in the mechanical properties wasobserved as compared to the control Benjakul et al reportedthe effects of prawn-shell chitosan on surimi prepared bybarred garfish (Hemiramphus far) [59] Prawn-shell chitosanat a level of 1 of the surimi gel showed an increase in gel-enhancing effect on the heat-induced gelation of myofib-rillar proteins The addition of microbial transglutaminasegenerally increases the deformation and breaking force ofsurimi gel However this effect was significantly retardedin the presence of prawn-shell chitosan resulting in lowermagnitudes of deformation and breaking force

The viscoelastic properties and the thermal stability oflow-grade squid (Dosidicus gigas) surimi were investigated byIglesias-Otero et al [60] The konjac glucomannan aqueousdispersion at a level of 1 expressed the best rheologicalproperties suggesting that the konjac glucomannan aqueousdispersion may be used to enhance the quality characteristicsof low-grade squid surimi gel Ramırez et al evaluated theeffect of protein-hydrochlorides on the gel-forming ability ofmyofibrillar proteins [142] The xanthanlocust bean gum ata ratio of 025075 showed a positive improvement in themechanical attributes of surimi gels Eom et al investigatedthe impact of carrageenan on the gelation property of salt-based Alaska pollock surimi [61] The addition of 15KCl rather than 2 NaCl significantly enhanced the gellingproperty of 120581-carrageenan-induced surimi gel and showedincreased gel strength breaking force and whiteness values

242 Salts Salts help in protein-protein interaction and theaddition of salt is critical during the processing of fish-pasteproducts However the high levels of sodium in foods andconsequently human consumption of sodium have becomea global issue The prime harmful effects of excess sodiumintake are hypertension and increased blood pressure Sub-sequently these conditions lead to cardiovascular diseasesincluding instances of stroke heart attack and relateddiseases as well as gastric cancer and osteoporosis [170ndash172] Therefore to reduce sodium intake levels in fish-pasteproducts Hwang et al prepared the sodium-reduced friedfish cakes containing potassium as a substitute for sodium [1]The quality characteristics of 30 sodium-reduced fried fishcakes were not notably different from those of full-sodiumfried fish cakes however the addition of potassium changedthe color and reduced consumer acceptance To increase theconsumer preference for sodium-reduced fried fish cakes theuse of different food additives might be advantageous

The weak gel-forming ability and the strong fishy smellof the giant squid (D gigas) make it undesirable for themanufacturing of surimi-based products To overcome theseproblems Choi and Kim used Amorphophallus konjac flourto enhance the quality characteristics of giant-squid surimiproducts [62]The increasing levels ofA konjac flour showedincreases in gel texture and water retention ability while areduction in color and taste was observed as compared tothe commercial surimi products The incorporation of theseasoning ingredients such as sweeteners might be helpfulin removing the fishy smell of D gigas ultimately improvingthe gel properties of giant-squid surimi Cando et al reportedthat the sensory and mechanical properties of surimi gels

with reduced-NaCl contents can be improved by the appli-cation of 300Mpa high hydrostatic pressures [63] The gelsmade with lower-NaCl contents revealed stronger and stablenetworks as showed by the ones with higher-NaCl contents

243 Water Activity It has been reported that humectantshad the greatest effect on lowering water activity (119886

119908) with

the efficiency of the reduction in 119886119908value decreasing in the

order of NaCl sodium lactate glycerin propylene glycoland sorbitol when each of them was combined with otherhumectants [173] Kim and Park reported the impact ofhumectants such as sodium chloride sugars and polyols tolower the water activity (119886

119908) of various model kamaboko gels

[64]The effect of sodium chloride on lowering water activity(119886119908) was the highest among all of the examined treatments

while glucose caused browning reaction on the surface ofkamaboko In another study they examined the effect ofstarch glycine and sodium lactate in lowering the wateractivity (119886

119908) of model kamaboko gels [65] Sanchez Pascua et

al reported that glycerol (15ndash50) was effective in reducingthe water activity (119886

119908) in Brazilian sand perch (Pseudopercis

semifasciata) and mackerel (Scomber japonicus marplatensis)[66] Among the tested humectants the efficiency of thereduction in water activity (119886

119908) was observed decreasing in

the order of sodium lactate glycine and starch

244 Polyuronides The effect of sodium and calcium salts ofcarboxymethyl and polyuronides cellulose on the strength-ening of kamaboko gels was investigated by Niwa et al [67]It was reported that the calcium salts of pectinic acid pecticacid alginic acid and carboxymethyl cellulose enhancedthe breaking force of Alaska pollock surimi whereas theirsodium salts except Na-pectinate failed to increase the break-ing force The increase in the breaking force induced by cal-cium carboxymethyl cellulose vanished upon increasing thedegree of substitution of hydroxyl groups to carboxymethylgroups Furthermore fine cellulose particles enhanced thebreaking strain and breaking force and reduced the amount ofexpressible water but were unsuccessful in the case of coarserparticlesThe addition of potato starch can increase the effec-tiveness even in the presence of coarse particles of cellulose

245 Ascorbic Acid The addition of dehydro-L-ascorbicacid and L-ascorbic acid to Alaska pollock surimi increasedthe gel strength [68] It was suggested that the positiveeffect of L-ascorbic acid on gel formation might be due tothe oxidation of sulfhydryl groups in fish proteins Lee etal studied the effects of sodium-L-ascorbate on the gel-forming abilities of surimi prepared by Alaska pollock [69]Sodium-L-ascorbate remarkably enhanced the gel firmnesscohesiveness strength and sensory properties of the fiber-ized products at a level of 02 It directly influenced thesurimi quality regardless of vacuum treatment indicatingthat airborne oxygen was not important Freeze-syneresisstimulated by ascorbate during frozen storage was lessenedby the application of hydroxypropylated-modified starch

246 Unsaturated Fatty Acids The addition of nutritionallybeneficial 120596-3 fatty acids during surimi preparation could

Journal of Food Quality 13

enhance the gel strength and stability [70] For the effectiveuse of highly unsaturated fatty acids such as docosahexaenoicacid (DHA) and eicosapentaenoic acid (EPA) in surimi-basedproducts Okazaki et al studied the gel-forming properties offrozen walleye pollock surimi containing DHA and EPA [71]They reported that to achieve a good quality product thevigorous agitation of surimi with fish oil is essential to allowthe heat-induced gelation of its emulsified product throughthe formation of fine oil droplets

Fukushima et al investigated changes in the physi-cal properties of heat-treated surimi gels prepared fromthreadfin breamwalleye pollock Japanese jackmackerel andwhite croaker [72] The breaking strain breaking strengthand water-holding capacity of the heat-treated gels becamegreater as the amount of fish oil increased Furthermoresurimi seafood was nutritionally enhanced with 120596-3 polyun-saturated fatty acid- (PUFA-) rich oils isolated from natu-ral sources such as algae flaxseed menhaden blend andkrill [73] The Alaska pollock surimi supplemented with120596-3 PUFA-rich oils showed improved protein fundamentaltextural properties heat-induced gelation and endothermaltransitions These studies show that the interaction of unsat-urated fatty acids and surimi proteins could contribute to theimprovement in gel properties without altering the texturalattributes

247 Plant Ethanol Extracts The effect of commercial tan-nin and ethanolic Kiam wood extract on the gelling char-acteristics of ice stored mackerel (Rastrelliger kanagurta)surimi was investigated by Balange et al [74] During12 d of iced storage pH TBARS TCA-soluble peptide andtrimethylamine (TMA) contents as well as total volatilebase (TVB) of mackerel mince increased while gel-formingability myosin heavy chain band intensity and whitenessdecreased consistently Deterioration lipid oxidation andprotein degradation proceeded as storage time increasedAn increase in deformation and breaking force of surimigel was observed with the addition of 030 commercialtannin or 015 ethanolic Kiam wood extract during the first6 d of storage Therefore commercial tannin and ethanolicKiam wood extract had not shown a gel-enhancing effecton mackerel surimi Furthermore Buamard and Benjakulinvestigated the effects of coconut husk ethanolic isolateson the gel-forming ability of sardine (S albella) surimi [75]Breaking force increasedwith the increasing levels of coconuthusk ethanolic isolates while a decrease in whiteness and nodetrimental effect on the sensory attributes of surimi gel wasobserved It was concluded that the addition of coconut huskextracts at a suitable concentration could enhance the gelstrength of sardine surimi with increased acceptability

25 Compound Additives The effect of different oxidizedphenolic compounds such as tannic acid OTA ferulic acidOFA caffeic acid OCF and catechin OCT on the gellingattributes of mackerel (R kanagurta) surimi was studied byBalange and Benjakul [76] Gels supplemented with 050OTA 040 OFA 010 OCT or 050 OCF showedincreases in deformation and breaking forces while a decreasein the expressible moisture content and myosin heavy chain

band intensity was observed In another study they inves-tigated the effects of oxidized phenolic compounds on thegel-forming abilities of bigeye snapper (P tayenus) surimi[77] An increase in breaking force and deformation witha decrease in expressible moisture contents was observedGels supplemented with the oxidized phenolic compoundshad a finer matrix with smaller strandsThe physicochemicalcharacteristics of natural actomyosin advocate that oxidizedphenolics could trigger the induction of disulfide bondformation or the conformational changes and cross-linkingthrough amino groups Therefore the addition of oxidizedphenolic compounds at an optimum concentration couldenhance the strength of surimi gel

Yongsawatdigul and Piyadhammaviboon reported aninhibition in autolysis of surimi and mince preparedby lizardfish (S tumbil) caused by p-tosyl-L-phenylalanylchloromethyl ketone and phenylmethanesulfonyl fluorideindicating the involvement of myofibrillar-associated serineproteinase Tropomyosin and myosin heavy chain proteinswere mainly hydrolyzed resulting in poor textural prop-erties [26] Arfat and Benjakul investigated the effect ofzinc chloride (ZnCl

2) and zinc sulfate (ZnSO

4) on the gel-

forming abilities of surimi produced by yellow stripe trevally(Selaroides leptolepis) [78] The kamaboko gels with ZnSO

4

added up to levels of 60120583molkg showed increased deforma-tion whiteness and breaking force as well as highly denserand interconnected gels Therefore ZnSO

4at a suitable

concentration could enhance gel strength and whiteness ofdark-fleshed fish surimi

3 Improvement in Quality andFunctionality of Fish-Paste Products

Various food additives from seafood (eg fish invertebratesand seaweed) plants (eg vegetables fruits and herbalmedicines) mushrooms animal sources and functionalmaterials used to improve the quality and functionality offish-paste products are listed in (Table 2) and describedbelow

31 Seafood Additives It has been reported that various typesof seafood namely fish including dried anchovy (Engraulisjaponicus) powder [79 80] pufferfish (Lagocephalus lunaris)powder [88] and skate (Raja kenojei) powder [81 82] andinvertebrates including warty sea squirt (Styela clava) groundflesh [83] its freeze-dried tunic powder [84] omandungi(Styela plicata) ground flesh [85] shrimp (Acetes japonicus)powder [86] and seaweed such as green laver (Ulva spp) [87]have been used to enhance the quality and functionality offish-paste

The boiled and dried Japanese anchovy (E japonicus)is a popular fisheries product in Korea and Japan As theflesh can be eaten together with bone boiled and driedanchovy products are regarded as good sources of calcium[174] Bae and Lee evaluated the properties of fried fish-paste with added anchovy (E japonicus) powder containinga high amount of calcium [79]The fish-paste containing 10anchovy powder displayed the highest values of adhesivenesshardness and strength In the overall acceptance of sensory

14 Journal of Food QualityTa

ble2Naturalfood

additiv

esused

toim

provethe

functio

nalpropertieso

ffish-pasteprod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Seafoo

dadditiv

es

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

1-2

[79]

Ancho

vyEn

grau

lisjaponicus

Fried

Drie

dpo

wder

Seab

ream

Calcium

contentcolortextural

andsensoryattributes

5[80]

Skate

Rajakenojei

Fried

Hot

wind-dried

skin

and

cartilage

(64)p

owder

Seab

ream

Moistu

recontentcolortextural

andsensoryattributes

3[81]

Skate

Rajakenojei

Steamed

Ferm

ented

flesh

Nemipterusv

irgatus

Aminoacidand

moistu

recontentcolortexturaland

sensoryattributes

20

[82]

Wartyseas

quirt

Styelacla

vaFried

Groun

dflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

5[83]

Wartyseas

quirt

Styelacla

vaFried

Freeze-drie

dtunicp

owder

Frozen

Itoyori

Colortexturaland

sensory

attributes

1[84]

Pleatedseas

quirt

Styelaplica

taFried

Grin

dedflesh

Him

eji

(Frozenyello

wtentacle)

Colortexturaland

sensory

attributes

15

[85]

Shrim

pAc

etesjaponicus

Fried

Powder

Frozen

seab

ream

surim

iMoistu

recontentcolortextural

andsensoryattributes

5[86]

Green

laver

Ulva

spp

Fried

Powder

Frozen

seab

ream

surim

iColorsensory

attributes

5[87]

Pufferfish

Lagocephalus

luna

risFried

Powder

Nemipterusspp

Moistu

recrude

protein

lipid

colortexturalandsensory

attributes

5[88]

Maesaengi

Capsosiphon

fulve

scens

Fried

Freeze-drie

dpo

wder

Frozen

seab

ream

surim

iColortexturaland

sensory

attributes

5[89]

Redsnow

crab

Chionoecetes

japonicus

Fried

Leg-meat

powder

Frozen

Alaskap

ollock

(Tchalco

gram

ma)

Physiochem

icalandsensory

attributes

6[90]

Plantsou

rcea

dditives

Mulberryleaf

Morus

alba

Fried

Powder

Seab

ream

Colortexturesensory

attributes

05

[91]

Onion

Alliu

mcepa

Fried

Ethano

lextract

Cutla

ssfishpaste

Moistu

recontentTB

CVBN

colorsensoryattributes

3[70]

Lotusleaf

Nelumbo

nucifera

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

05

[92]

Beetroot

andSpinach

Beta

vulga

risand

Spinaciaoleracea

Microwave

inkamaboko

shape

mold

Freshbeet

rootspinach

dish

Not

mentio

ned

Moistu

retexture

analysis

Beetroot10

Spinach15

[93]

Citrus

fruits

Citru

slim

onC

junosC

unshiu

Fortun

ellajaponica

varmargarita

Steamed

Groun

dflesh

pulpwith

out

seeds

Min

Daegu

flesh

Colortexturaland

sensory

attributes

Cumqu

at[94]

Journal of Food Quality 15

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Oatbran

+SiO2

Avenasativa

Boiled

Powder

Frozen

Alaskap

ollock

surim

iColortexturaland

physiochem

icalattributes

6gOatbran10

0gSiO2

[95]

Yam

Dioscorea

japonica

Fried

Powder

Pollo

cksqu

idshrim

pFo

ldingtest

colortexturaland

sensoryattributes

2[96]

WolfberryC

hinese

Goji

Fructuslycii

Fried

Powder

Seab

ream

Texturalandsensoryattributes

3[97]

Redginseng

Pana

xginsengCA

Meyer

Fried

Powder

Not

describ

edColorlipid

oxidation

sensory

attributes

1[98]

Korean

angelicar

oot

Angelicae

gigantis

Radix

Fried

Powder

Seab

ream

Texturalandsensoryattributes

05

[99]

Turm

eric

Curcum

alongaL

Fried

Powder

Pollo

cksqu

idshrim

pColorrheologicalandsensory

attributes

3[100]

Wasabi

Wasabiajaponica

Fried

Freeze-drie

dpo

wder

Silver

pomfre

t(Pam

pusa

rgenteus)

ColorT

BCviablec

ellcou

nt

texturalandsensoryattributes

18

[101]

Wolfip

oriaextensa

Poria

cocos

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

3[102]

Mushroo

madditiv

es

Butto

nmushroo

mAg

aricu

sbisp

orus

Fried

Chop

ped

fresh

Argyrosomus

argentatus

Texturalandsensoryattributes

10

[103]

Enok

imushroo

mFlam

mulina

velutip

esFried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

5[104]

Shiitakem

ushroo

mLentinus

edodes

Fried

Chop

ped

fresh

Aargentatus

Texturalandsensoryattributes

10

[105]

King

oyste

rmushroo

mPleurotuseryngii

Fried

Paste

Silver

whitecroaker(Penn

ahiaargentata)

Texturalandsensoryattributes

10

[106]

King

oyste

rmushroo

mPleurotuseryngii

Steamed

Paste

Cuttlefish

(Sepiaesculen

ta)

Texturalphysio

chem

ical

sensoryattributes

40

[107]

Animalsource

additiv

es

Poultrychicken

Gallusgallus

domesticus

Fried

Breastmeat

batte

r

Itoyori

Japanese

threadfin

bream(Ne

mipterus

japonicus)

Chem

icalcompo

sition

color

fatty

acid

compo

sition

TBARS

sensoryattributes

746

or1493

[108]

Functio

nalfoo

dadditiv

es

Long

-chain

cellu

lose

mdashBo

iled

Powdered

cellu

lose

Alaskap

ollock

surim

iTexturalandrheological

attributes

6[109]

Dietary

fiber

from

ascidian

tunic

Halocynthiaroretzi

Boiled

Refin

eddietaryfib

erAlaskap

ollock

surim

iColortexturalph

ysiological

andsensoryattributes

5[110]

16 Journal of Food Quality

Table2Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Fibera

nd120596-3

oil

mdashHeatedin

awater

bath

Powdered

fiber120596

-3oil

Alaskap

ollock

surim

iTexturalandrheological

attributes

Fiber6ndash

10g

and120596-3100

g[111]

Flaxseed

orsalm

onoil

Not

describ

edCoo

kedin

awater

bath

Oil

Frozen

Alaskap

ollock

surim

i(Tchalco

gram

ma)

TBARS

colortexturaland

sensoryattributes

2g10

0gfranks

[112]

Soybeanoil

Glycinem

axHeatedin

awater

bath

Oil

Frozen

silverc

arpsurim

iColortexturalattributes

Soybeanoilgt3

[113]

Calcium

powdero

fcuttlefish

bone

treated

with

aceticacid

Sepiaesculen

taHeatin

gin

awater

bath

Calcium

powder

Alaskap

ollock

surim

iMoistu

recontentcolortextural

andsensoryattributes

009

[114]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Alaskap

ollock

meatp

aste

Colortexturaland

sensory

attributes

017

[115]

Prop

olis

mdashFried

Alcoh

olextract

(100)

Sand

lance

(Hypoptychus

dybowskii)

Acid

andperoxide

valueVBN

sensoryattributes

02

[116]

Cheong

gukjang

Ferm

entedGlycine

max

byBa

cillussp

Fried

Powder

Seab

ream

Colortexturaland

sensory

attributes

2[117]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 17

evaluation small and large size fish-paste with 1 and 2respectively of added anchovy powder was preferred Thesimilar increasing trend of calcium intensity was observedby Bae et al [80] However the fried fish-paste productscontaining 20 anchovy powder displayed the highest valuesof adhesiveness hardness and strength Regarding overallacceptance in the sensory evaluation the fried fish-pastecontaining 5 anchovy was preferred The optimal amountsof added anchovy in the results from Bae and Lee and Bae etal were different which might have been due to the differentdrying methods and sizes of the anchovies used in each study[79 80] Despite the differences in the two studies the resultssuggest that anchovy powder could be applied to fried fish-paste products to achieve high calcium contents

Skate contains many essential fatty acids includinglinolenic acid linoleic acid arachidonic acid DHA andEPA [175] Skate skin contains high percentages of collagenprotein and calcium [176] while its cartilage is rich inchondroitin sulfate [177] To improve quality and nutrientlevels Cho and Kim prepared fried fish-paste with skate (Rkenojei) powder (hot wind-dried skin and cartilage powder[6 4]) [81] According to Park et al preference testingusing steamed fish-paste product with different levels ofadded 14-day-fermented flesh of skate showed significantincreases in brownness smoothness and skate flavor scores[82] The amino acid contents of fish cake samples with20 skate added had the highest overall preference scoresConsequently the addition of 20 skate powder was optimalfor the steamed fish cake to improve its quality characteristicswith higher protein contents

Warty sea squirt (S clava) aquaculture in the Masanarea of Korearsquos south coast contains abundant unsaturatedfatty acids and essential amino acids in its flesh [178] andglycosaminoglycan in its tunic [179] Warty sea squirt has aunique taste and distinct antioxidant and anticancer activities[180] Fried fish-paste supplemented with 20 warty seasquirt (Korean name miduduk) displayed improved qualityand functionality [83] Choi et al reported a fried fish-paste containing freeze-dried byproduct of warty sea squirt(S clava tunic) [84] The hardness and strength of fish-paste increased with increasing amounts of tunic powderFor overall acceptance in sensory evaluation a fish-pastesupplemented with 1 S clava tunic obtained a relativelyhigher score The results suggested that S clava flesh andtunic could be used for fish-paste products to improve theirquality and functionality Park et al reported improvementin the functional properties of fish-paste by adding S plicata(Korean name omandungi) [85] Fried fish-paste containing20 S plicata indicated the highest values of adhesivenesshardness and strength For overall acceptance in sensoryevaluation a fish-paste containing 15 S plicata obtained thehighest score

Seo and Cho reported the preparation of fish-paste withadded shrimp (A japonicus) powder [86] The hardnessspringiness and cohesiveness increased with the increasingconcentration of shrimp powder However the brittlenessand gumminess reduced In the sensory evaluation the fish-paste prepared with 5 shrimp powder was most preferredCho and Kim reported the preparation of fish-paste with

added green laver (Ulva spp) powder [87] The hardnessspringiness and cohesiveness increased with the increasingconcentration of green laver powder However the brittlenessand gumminess decreased upon the addition of green laverpowder In the sensory evaluation a fish-paste prepared with5 green laver powder was preferred over other fish-pastesThese results suggest that green laver powder could be appliedto fish-paste to improve its quality and functionality

Pufferfish containing taurine hydroxyproline lysine andglycine impart a characteristic taste to food [181] To improvethe taste of fish-paste products Park prepared a fish-pasteby adding green rough-backed pufferfish (L lunaris) pow-der [88] The hardness strength gumminess springinessand chewiness of the fish-paste increased depending onpufferfish powder contentThe preparation of fish-paste withadded Capsosiphon fulvescens powder was reported by Park[89] The hardness springiness strength and cohesivenessincreased with the increasing concentrations of C fulvescenspowder However the brittleness and gumminess reducedwith the addition of C fulvescens powder In the sensoryevaluation overall the fish-pastes prepared with 5 Cfulvescens powderwere preferred over other fish-pastesThusthe results show that C fulvescens powder could be used tocreate fish-paste products with high quality and functionality

Kim et al reported the changes in the sensory and physic-ochemical properties of a fish-paste containing red snow crab(Chionoecetes japonicus) leg-meat powder [90] Hardnessgumminess springiness and cohesiveness increased withincreasing levels of red snow crab leg-meat powder Based onthe sensory evaluation it was concluded that the addition ofred snow crab leg-meat powder at a level of 6 could improvethe quality characteristics of fish-paste products

32 Plant Source Additives It has been reported that variousplant sources namely vegetables (eg mulberry beetrootand spinach) fruits (eg citrus) and herbal medicines (egChinese matrimony vine Korean Angelica root) have asignificant effect in improving the quality and functionalityof fish-paste products

Mulberry (Morus alba) leaf has been used traditionallyto treat a disease symptomized by thirst and stroke [182]Ever since mulberry leaf was included as a food material inthe Food Codex in 1988 by the Ministry of Food and DrugSafety (MFDS Osong Chungju South Korea) Mulberry leafpowder has been used in various processed food productsand health functional foods Shin and Park reported theuse of mulberry leaf powder in the preparation of fish-pasteproducts [91] In a texture meter test the hardness increasedbut the cohesiveness springiness gumminess and brittlenessdecreased with increasing levels of mulberry leaf powder Insensory evaluation the fish-paste with 05 mulberry leafpowder revealed the highest acceptance scores in terms offlavor texture and overall quality

Garden onion (bulb onion Allium cepa) is a perennialplant belonging to Liliaceae and is widely used as a spice andseasoning vegetable in both the East and the West Park etal investigated the quality characteristics of fried fish-pastesupplemented with flavonol-rich ethanol extract of onion[183] In the sensory evaluation as the amount of ethanol

18 Journal of Food Quality

extract of onion increased so did the favorability in termsof flavor and taste Notably 3 ethanol extract of onion hadthe best score in overall acceptance The results indicate thatethanol extract of onion can be used to prepare fried fish-paste products with high quality and functionality

Shin reported the production of fish-paste with addedlotus (Nelumbo nucifera) leaf powder [92] The flavor adhe-siveness and hardness increased with the increasing levels oflotus leaf powder The fish-paste with 05 lotus leaf powderdisplayed the highest acceptance scores in terms of springi-ness pleasant taste appearance texture flavor and overallquality Thorat et al prepared kamaboko containing greenchili coriander ginger garlic spice mixture and groundbeetroot or a spinach dish and then subjected the preparationto microwave cooking [93] Kamaboko prepared with 10beetroot and a 15 spinach dish was found to be superior tothe others

Yang and Cho developed a steamed fish cake with added5 ground citrus fruits with skin [94] The addition of citrusfruits did not disturb the flexibility of surimi The pH ofsurimi samples increased in the following order lemon (Cit-rus limon) citron (Citrus junos) tangerine (Citrus unshiu)kumquat (Fortunella japonica var margarita) and controlThe hardness of surimi was highest for lemon followed bycitron tangerine kumquat and control surimi In the sensoryevaluation surimi containing kumquat demonstrated higherscores in terms of color taste and textural properties Theseresults suggest that surimi could be prepared by adding citrusfruits to improve the quality and functionality

Oat bran is a gluten-free dietary fiber that may decreasethe risk of diabetes and heart diseases The physicochemicalproperties of surimi gels supplemented with oat bran werestudied by Alakhrash et al [95] The oat bran and SiO

2

incorporation (6 g100 g) greatly improved water-holdingcapacity and gel texture while a reduction in whiteness wasobserved Kim and Byun conducted tests on the sensoryand physicochemical characteristics of fish-paste with addedyam (Dioscorea japonica) powder [96] The addition of yampowder increased gumminess strength springiness andcohesiveness In the sensory evaluation the addition of 2yam powder had the best scores in terms of taste color andoverall preference

Fructus lycii is a fruit produced by Lycium barbarumL that has been used for nourishment tonicity and nour-ishment of the blood it has antibacterial anticancer andantioxidant properties [182ndash186] Shin et al prepared friedfish-paste containing dried F lycii powder [97] In the texturalanalysis cohesiveness increased while brittleness and gum-miness decreased with increasing levels of F lycii powderThe 3 F lycii powder sample had the highest acceptancescores in terms of appearance texture taste flavor andoverall acceptability

Red ginseng-based fried fish-pastes containing differentsizes and amounts of red ginseng powder were preparedand their biological properties including lipid oxidation toimprove fish-paste quality were investigated [98] The fish-paste products containing red ginseng powder showed asignificant increase in hardness and chewiness Furthermorean inhibitory effect on lipid oxidation and reduced number

of total microbes during storage were observedThese resultssuggest that high-quality fish-pastes could be achieved withthe addition of 1 red ginseng powder which effectivelyimproved both sensory evaluation and physicochemicalproperties

Angelicae Gigantis Radix (the dried root ofAngelica gigasNikai) more popularly known as Korean Angelica is one ofthe widely used herbal medications [187] It has been usedin Korean medicine as an important medication for anemiaand blood circulatory disorders It has also been used formenstrual pains and postmenopausal syndromes Shin et alreported the development of fish-paste with A gigas powder[99] In a texture test hardness chewiness and brittlenessincreasedwith increasing concentrations of AngelicaeGigan-tis powderHowever cohesiveness and springiness decreasedIn the sensory evaluation the fish-paste with 05 AngelicaeGigantis powder showed the highest acceptance scores forappearance flavor taste texture and overall quality

Turmeric (Curcuma longa) has been used in Ayurvedicmedicine from ancient times as a treatment for inflammatoryconditions It has been reportedly used for its various bio-logical activities including antibacterial antiviral antifungalantioxidative and antiatherogenic effects [188] Turmeric hasbeen grown as a special crop in the central and southern areasaround Jindo in South Korea [189] Choi et al investigatedthe sensory and rheological properties of fish-paste preparedwith turmeric powder [84] In terms of textural attributesthe addition of C longa powder decreased springiness andimproved strength In the sensory evaluation the addition of3 C longa powder was associated with the best scores fortaste and overall preference

Wasabi (Wasabia japonica) has various beneficialhealth properties including antioxidative antimicrobialand antimutagenic activities [190 191] Jang et al reporteda high-quality fried fish-paste product made with silverpomfret (Pampus argenteus) which is one of the savorysoft and delicious types of fish prepared by adding wasabipowder [101] Notably hardness gumminess and chewinessincreased significantly with the addition of wasabi powderIn the sensory evaluation 18 wasabi powder showed thebest score in overall acceptability These results show thatwasabi could be used as a food additive or preservative infish-paste products

White Poria cocos wolf is the inner white part of P cocosa parasite found on Pinus densiflora It is used to treat edemachronic gastritis gastric atony nephrosis acute gastroentericcatarrh emesis dizziness and vomiting [192 193] Shin et alprepared a fried fish cake with added white P cocos powderand studied the textural and sensory characteristics [102]In texture tests brittleness was observed to increase whilespringiness decreased with increasing concentrations of Pcocos powder The fish-paste product containing 3 whitePoria cocos powder showed the highest acceptance scores forflavor appearance texture taste and overall quality

Milk-vetch root is one of the most produced herbalmedicines in Korea It is a peeled and dried root of the herba-ceous perennial herb known as Astragalus membranaceuswhich belongs to the Fabaceae family [194] It has been

Journal of Food Quality 19

reported that milk-vetch root exerts diuretic tonic anti-hypertensive hypoglycemic immune-enhancing antitumorand antiviral effects [195] Kim investigated the sensoryand physicochemical properties of fish-paste prepared withmilk-vetch root powder [196] The strength cohesivenessbrittleness and gumminess of the fish-paste increased whileits springiness decreased with an increasing amount of milk-vetch root powder In the sensory evaluation the addition of10 milk-vetch root powder indicated best scores for tastetexture color and overall preference

33 Mushroom Additives Mushroom is a nutritional andfunctional food as well as a vital source of physiologicallybeneficial medicines Mushrooms have been used as tradi-tional medicines in Korea Japan China and other Asiancountries for curing various diseases including lymphaticdisease gastroenteric disorder oral ulcer and various can-cers [197] It has been reported that edible mushrooms inKorea number approximately 350 species [198] Several ediblemushrooms that are highly preferred have been added to fish-paste to enhance their quality and functionality

Ha et al prepared a fried fish-paste product with addedAgaricus bisporus which is a product described as having aracy flavor and taste [103]The elasticity hardness brittlenessand gumminess of fish-paste with the added mushroomincreased however no significant difference in strengthwas observed Regarding overall acceptance in a sensoryevaluation a fish-paste supplemented with 10 A bisporusmushroom showed the highest scores

Enoki mushroom (Flammulina velutipes) is well knownfor its anticarcinogenic and blood pressure-reducing prop-erties To utilize its functional properties enoki mushroomwas added to fried fish cake [104] The sample containing15 mushroom received the highest values for strengthgumminess and brittleness In the sensory evaluation thefish cakes with 5 mushroom obtained favorable scores foroverall acceptance

Shiitake mushroom (Lentinus edodes) is known for itshigh level of 120573-glucans Son et al investigated the effectsof shiitake mushroom on the textural properties of friedfish cake [105] The fish cake containing shiitake mushroomreceived the highest values for strength hardness gummi-ness and brittleness In the sensory evaluation the fish cakeswith 10 shiitake mushroom sample obtained the best scorefor overall acceptance

Kim et al prepared a fried fish cake using cultured kingoyster mushroom (Pleurotus eryngii) and silver white croaker(Pennahia argentata) surimi to enhance its physiologicaleffects [106] In assessing its quality properties fish cake towhich 10 mushroom was added received the highest valuesfor strength hardness gumminess and brittlenessThe effectof king oyster mushroom on the textural and physicochem-ical properties of steamed cuttlefish (Sepia esculenta) fishcake was investigated by Chung et al [107] The fish-pastewith added king oyster mushroom paste revealed significantdecreases in gumminess cohesiveness and hardness whilethe springiness increased with increasing concentrations ofking oystermushroompasteOn the sensory evaluation basisthe cuttlefish-paste supplemented with 30ndash50 king oyster

mushroom showed higher overall acceptability In the studiesby Kim et al and Chung et al the optimal amounts of kingoyster mushroom differed which might have been due tothe different cooking methods and surimi used in each study[106 107]

34 Animal Source Additives Jin et al investigated the effectof chicken meat on the quality characteristics of Itoyori(Japanese threadfin bream Nemipterus japonicus) surimi[108] The physicochemical properties such as fatty acidcomposition shear force and gel characteristics were affectedby substitution with spent laying hen meat batter Howeversensory characteristics were less affected by this substitutionA huge amount of waste in the processing of grass carp isdiscarded To deal with this waste Gao et al studied theprocessing technology used for fish and mushroom pastewith salted fish cubes mushroom soybean and fermentedsoybeans [199]

35 Functional Food Additives Functional food additivesincluding dietary fiber 120596-3-rich oil calcium additives andpropolis have been used in the preparation of fish-pasteproducts to increase their quality and functionality Westernpopulations have an inadequate quantity of health beneficialdietary fiber in their diets Besides fiber most Western pop-ulations also consume an insufficient amount of 120596-3 PUFAswhile their sodiumconsumption greatly surpasses the recom-mended maximum Debusca et al prepared Alaska pollocksurimi fortified with commercial long-chain cellulose as asource of dietary fiber [109] Fiber fortification up to a level of6 improved both texture and color a slight decline in thesevalues was observed at levels of 8 fiber An increase in gelelasticity and thermal gelation of the fish cake was observed

Yook et al prepared a fish-paste by adding dietaryfiber extracted from ascidian (Halocynthia roretzi) tunic toenhance its physiological properties [110] The hardnessgumminess adhesiveness shear force and chewiness of thefish-paste improved with the incorporation of the ascidiandietary fiber The fish-paste with 5 ascidian dietary fiberscored the highest and was generally preferred by sensorypanels Tolasa et al reported that the oxidative stability andthe uniform dispersion of 120596-3 unsaturated fatty acids can beattained in a highly consistent surimi gel system without theuse of antioxidants [200]

Surimi and surimi-based products are famous through-out the world In fact US consumption increased in the1980s while the rate leveled off thereafter The nutrificationof food products with 120596-3 PUFAs increases the health ben-efits of food consequently increasing their market demandPietrowski et al prepared surimi seafood products nutrition-ally enhanced with 120596-3 PUFAs [201] Although the nutrifica-tion of 120596-3 PUFAs indicated an increase in lipid oxidationit was within limits acceptable to consumers The color ofsurimi seafood nutrified with 120596-3 PUFAs generally improvedbut no effect on textural characteristics was observed

Debusca et al reported that the fortification of Alaskapollock surimi with either 120596-3 oil or dietary fiber alone orin combination improved both the textural and rheologicalproperties [111]The120596-3 oil and fiber in combination revealed

20 Journal of Food Quality

greater gelation of surimi and a slight reduction in color prop-erties indicating their interaction with myofibrillar proteinsThus it was suggested that the 120596-3 oils and fiber could beeffectively used as a fortifying agent to prepare high-qualitysurimi products with nutritional benefits Sell et al preparedsurimi franks fortified with salmon oil or flaxseed [112]The textural properties showed differences between franktypes with the flaxseed franks being cohesive less gummysofter and chewy while the sensory evaluation showed nosignificant differences

Chang et al determined the effects of soybean oil andmoisture contents on the physical properties of surimi gels[113] The increasing levels of soybean oil and moisturecontents resulted in an increase in whiteness and reductionin the chewiness hardness and breaking force Setting incombination with soybean oil improved the textural andcolor parameters of surimi gels indicating that soybean oilcould be used to improve the color and textural properties ofsurimi seafood products

Kim et al prepared boiled fish cake using acetic acid-treated cuttlefish bone as a calcium additive agent [114] Theresults of sensory evaluation of texture and whiteness weresimilar to those without this supplementation In the mineralcontent analysis of heat-induced surimi gel calcium contentincreased depending on the increasing concentration ofacetic acid-treated cuttlefish bone powder while phosphoruscontent did not change The optimal concentration of aceticacid-treated cuttlefish bone powder for the preparation ofhigh-quality heat-induced surimi gel was 009

Kim et al prepared Alaska pollock fried fish-pastesupplemented with propolis [115] The addition of propolisenhanced the antispoiling and antioxidative ability as well asgel strength of fried fish-paste In the sensory evaluation theaddition of 017 propolis showed the best score in overallacceptability In another study Kim et al later studied sand-lance (Hypoptychus dybowskii) meat paste prepared withpropolis [116] Similar to the previous report the addition ofpropolis on the fried fish-paste showed higher antioxidativeand antispoiling activities The fried sand-lance meat pasteprepared with 02 added propolis was the most acceptableFurthermore the bitter taste of the sand-lancemeat paste wasreduced by adding 2 sweet amber powder

Cheonggukjang is an ancient Korean food prepared byfermented soybean It contains high levels of dietary fiberoligosaccharides isoflavones saponin lecithin phytic acidand phenolic compounds among others Its many benefi-cial properties have been reported such as thrombolyticanticancer antimicrobial hepatoprotective antioxidant andcholesterol-lowering effects [202] Park et al reported theuse of fish-paste containing cheonggukjang powder [117]Theincreasing concentrations of cheonggukjang resulted in anincreased value of springiness cohesiveness and hardnesshowever a reduction in brittleness and gumminess values offish-paste was observed

4 Shelf-Life Extension of Fish-Paste Products

Fish-paste products may easily spoil due to residualmicrobes that are not removed by sterilization during the

manufacturing process or by contamination in packagingor the distribution process For such reasons even vacuum-packed fried fish-paste products have a shelf-life of fewerthan 10 days during cold storage which is relatively short[121 122] Various efforts have been made to develop long-term storage solutions for fish-paste products via physicaland chemical methods [118ndash122] Although these methodswere found to be very effective for the long-term storageof fish-paste products they require sensitive and complexmanipulation and are costly

The addition of appropriate food additives to fish-pasteproducts as an effective preservation protocol is anotherstrategy Potassium sorbate is a typical synthetic food preser-vative and is commonly used in processed foods includingfish-paste productsThis material is effective in inhibiting thegrowth of variousmicroorganisms as it has a slight sterilizingeffectThe use of this material is permitted to a concentrationof less than 20 gkg in processed fish meat products (FoodCode Ministry of Food and Drug Safety Republic of Korea)According to the results of Walker sorbates and sorbic acidexert a very low level of mammalian toxicity even in chronicstudies as up to 10 of the diet did not show any carcinogenicactivity [203] In addition Thakur and Patel summarizedthe application of sorbates in the shelf-life extension of fishand fish-based products [204] The physical and chemicalmethods along with natural food preservatives for the long-term storage of fish-paste products are listed in Table 3 andbriefly described below

41 Physical and Chemical Methods Various efforts havebeen focused on developing long-term storage solutions forfish-paste products via physical methods including highpressurization [118] microwave pasteurization [93] highhydrostatic pressure treatment [119] and even irradiation[118 121] In addition it has also been reported that treatmentwith chlorine dioxide solution at an appropriate concentra-tion which is harmless to humans could be used to preventspoilage and to extend the shelf-life [122]

High hydrostatic pressure technology has graduallygained popularity in the food industry over the last twodecades [205] In 2013 the worldwide market for highhydrostatic pressure equipment was estimated to be $350million and it is expected to grow Besides high hydrostaticpressure technologies several types of radiation have alsobeen tested including ultraviolet microwaves and gammairradiation treatments Radiation is generally used to controlbiological hazards in the production of fish-paste productsand to prolong the shelf-life of such products [206 207]Gamma radiation exerts potent antimicrobial effects whereasultraviolet rays are effective for the surface but not interiorsterilization of porous dried fish products (eg fish-pasteproducts) However gamma irradiation treatment demandslarge-scale facilities and higher costs [207 208]

Miyao et al reported that growth of the majority of thepathogenic microorganisms present in surimi was inhibitedat a high pressure of between 300 and 400Mpa [118] Severalpressure-resistant strains were isolated from surimi and wereidentified as Moraxella sp Acinetobacter sp Streptococcusfaecalis and Corynebacterium sp It was suggested that

Journal of Food Quality 21

Table3Naturalfood

additiv

esandph

ysicochemicalmetho

dsused

toim

provethe

shelf-life

offish-paste

prod

ucts

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Physicalandchem

icalmetho

ds

Highhydrostatic

pressure

mdash

High-pressure

treatmento

rheattre

atment

insampletub

ewith

vacuum

packaging

mdashFrozen

Alaskap

ollock

Microbialactiv

ity40

0MPa

[118]

Highhydrostatic

pressure

mdashNot

cooked

mdash

Tuna

fishpaste

Mackerelp

astewith

paprika

mackerelp

astewith

garlic

mackerelp

astealon

eand

salm

onpaste

Microbialactiv

ity200M

Pa[119]

Co-60

Gam

mar

ays

mdashGrilled

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

texturalsensorym

icrobial

physiochem

icalattributes

75kG

y[120]

Co-60

Gam

mar

ays

mdashFried

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

TBC

pHtexturalmicrobial

physiochem

icalattributes

3kGy

[121]

Chlorin

edioxide

(ClO2)

mdashSteamed

mdashCom

merciallyavailablefi

shmeat

paste

prod

ucts

VBN

TBA

RSpHm

icrobial

physicochemicalsensory

attributes

50pp

m[122]

Naturalfood

additiv

esRe

dpepp

erethano

lextract(RP

EE)

andchop

pedfre

shredpepp

er(C

FRP)

Capsicu

mannu

umFried

Ethano

lextract

andchop

ped

fresh

one

Frozen

Alaskap

ollock

TBC

sensoryattributes

RPEE

10

CF

RP5

[123]

Ethano

lextract(EE)

andwater

extract

(WE)

Phellodendron

amurense

Eugenia

caryophyllu

sPinu

srigida

Bletillastr

iata

andPa

eonia

albiflora

mdashmdash

mdashAntim

icrobialattributes

onpu

trefactiveisolatesfrom

fish

meatp

asteprod

ucts

EE2000

ppm

[124]

Eggwhitelysozyme

(EWL)

andor

sodium

hexametapho

sphate

(SHMP)sod

ium

pyroph

osph

ate(SP

P)

Gallusgallus

domesticus

Fried

Powder

Frozen

Alaskap

ollock

Viablecellcoun

tpH

VBN

biochemicalattributes

EWL5

+SP

P05

+SH

MP

01

[125]

Grapefruitseed

extract

Citru

sparadisi

mdashSolutio

nCom

merciallyavailablefi

shmeat

paste

prod

ucts

Proxim

atec

ompo

sition

textural

biochemicalrheologicalsensory

attributes

1000

ppm

[126]

22 Journal of Food Quality

Table3Con

tinued

Com

mon

name

Species

Coo

king

metho

dUsedas

Fish

source

forsurim

iMetric

sOptim

umam

ount

ortre

atment

cond

ition

References

Cinn

amon

bark

extract

Cinn

amom

umcassia

Fried

Extracted

solutio

nFrozen

Alaskap

ollock

Antim

icrobialactiv

itySprayeddiluted

extract(11)

[127]

Alginicacid

hydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Relativev

iscositypHcolor

rheologicalattributes

03

[128]

Chito

sanhydrolysate

mdashBo

iled

Hydrolysate

solutio

nFrozen

Alaskap

ollock

Viablecellcoun

tsrheological

sensoryattributes

03

[129]

Nisin(N

)and

or

sucrosefattyacid

esters(SFE

)mdash

Steamed

Powdera

ndsolutio

nFrozen

Alaskap

ollock

Viablecellcoun

tantim

icrobial

activ

ityN125120583

gg+

SFE10mg

[130]

Piscicolin

KH1

Carnobacteriu

mmaltalomaticu

mSteamed

Solutio

nCod

fish

Inhibitory

assayproteincontent

antim

icrobialactiv

ity50

AUg

[131]

Zein

andsoyprotein

isolate(SPI)fi

lms

containing

greentea

extract(GTE

)

Zeamays

Glycinem

axCa

melliasin

ensis

Fried

Ediblefilm

(GC-WPI)w

ithGTE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

TBARS

colorm

icrobial

physicalattributes

GTE

1

[132]

Gelidium

corneum

(GC)

-Wheyprotein

isolate(G

C-WPI)

blendfilm

containing

grapefruitseed

extract(GSE

)

Gelidium

corneum

Citru

sparadisiBo

staurus

Not

mentio

ned

Ediblefilm

(GC-WPI)w

ithGSE

Com

merciallyavailablefi

shmeat

paste

prod

ucts

Water

vapo

rpermeability

microbiologicalanalysis

sensory

attributes

GSE

01

[133]

TBC

totalbacteria

lcou

ntV

BNvolatile

basic

nitro

gen

TBARS

thiob

arbituric

acid

reactiv

esub

stances

Journal of Food Quality 23

damage to the cell membrane and degradation of ribonucleicacids occurred in the high-pressure-treated cells Malickiet al investigated the use of high hydrostatic pressure toprolong the shelf-life of traditionallymanufactured fish-pastestored under refrigeration (4∘C) for 6 weeks [119] Neitherbacteria nor molds or yeasts were detected in the highhydrostatic pressure-treated fish-paste samples at any timepoint analyzed irrespective of the pressurization conditionsIn conclusion these studies revealed the effectiveness of highhydrostatic pressure to prolong the shelf-life of traditionallymanufactured fish-paste stored under refrigerated conditionsfor up to 6 weeks

Kim et al reported a reduction in the total aerobicbacterial counts in the grilled fish-paste stored at 5∘C andirradiated by gamma rays at a level of 25 kGy or more[120] Additionally the treatment of gamma rays at a levelof 75 KGy at 30∘C showed a significant inhibition in aerobicbacterial growth Cho et al investigated the effect of Co-60 gamma irradiation on fried fish-paste and studied thephysicochemical properties of fish-paste products stored atlow temperature (3 plusmn 1∘C) and room temperature (10ndash20∘C)[121] There was no obvious difference between the vacuum-and air-packed groupsThe irradiation of 3 KGy extended theshelf-life of fish-paste up to 2 times at room temperature and3-4 times at low temperature In both studies the irradiationtreatment caused very little textural degradation and no effecton the sensory characteristics of the samples was observed

Shin et al investigated the effects of chlorine dioxide(ClO2) treatment on the physiochemical andmicrobial prop-

erties of fish-paste products [122] After ClO2treatment

fish-paste samples were individually packed and stored at4∘C The pH and VBN values of fish-paste decreased withincreasing ClO

2concentration ClO

2treatment significantly

reduced the populations of total bacteria yeast and moldduring storage In particular treatment with 50 ppm ClO

2

significantly decreased the total bacterial count the mostamong all ClO

2-treated fish-pastes showing that 50 ppm

chlorine dioxide was the optimum concentration to prolongthe shelf-life of fish-paste products

42 Natural FoodAdditives Theuse of natural food preserva-tives rather than chemical and synthetic food preservatives isofworldwide interest It has been reported that several naturalfood additives could extend the shelf-life of cooked fish andfish products Some examples include onion ethanol extract[183] egg white lysozyme [125] grapefruit seed extract [126]chitosan hydrolysate [129] cinnamon bark extract [127] andred pepper extract [123] as well as mixtures of lysozymessodium hexametaphosphate and sodium pyrophosphate

The shelf-life of fried fish-paste products prepared byadding red pepper ethanol extract was estimated by Yoonet al [123] The shelf-life of the fried fish-paste with added10 red pepper ethanol extract and 5 chopped fresh redpepper was 2 to 3 days longer than that of the commercialfish-paste product thus demonstrating the most effectivepreservation effects According to Ahn et al the extractsof Eugenia caryophyllus Pinus rigida Bletilla striata andPaeonia albiflora exerted strong inhibitory effects on thegrowth of microorganisms isolated from putrefied fish-paste

[124] Notably the ethanol extract was more effective thanwater extract in all tested microorganisms The inhibitionlevel of each extract was evident at 2000 ppm ethanol in thefish-paste

Kim et al investigated the inhibitory effects of lysozymesmixtures of lysozymes and other antibacterial substancessuch as sodium pyrophosphate and sodium hexametaphos-phate on bacterial growth in surimi products [125] Thelysozymes inhibited growth in most of the tested isolatesand themixture of antibacterial substances showed increasedeffects compared with those when they were used individ-ually A mixture of 05 sodium hexametaphosphate 05sodium pyrophosphate and 005 lysozyme in imitationcrab and kamaboko showed the highest inhibitory activ-ity

The stabilizing effects of grapefruit seed extract on fish-paste products were investigated by Cho et al [126] Texturalproperties decreased with increasing storage period Thetreatment of fish products with grapefruit seed extract pro-longed the deterioration of fish-paste product proteins duringstorage up to 4-5 daysThe chemical sensory and rheologicalevaluation revealed that the grapefruit seed extract could beused as an effective additive to extend the shelf-life of fish-paste products

The predominant bacterium in most of the isolatedmicroorganisms from packed and unpacked spoiled fish-paste products is Bacillus sp [127] Notably yeast andmolds are not reported in the vacuum-packed products Ahydrolysate of alginic acid has antimicrobial activity but ithas not been used at industrial scale The alginic acid ata concentration of 03 prolonged shelf-life of fish-pasteproducts by 4 days at 15∘Cand inhibited the growth ofBacillussp isolated from fish-paste products [128] According to theresults of Cho et al the chitosan hydrolysate made withchitosanase from Aspergillus oryzae ATCC 22787 revealedthe strongest antimicrobial activity and inhibited the growthof Bacillus sp isolated from fish-paste products [129] Theaddition of chitosan hydrolysate at a concentration of 03resulted in extended shelf-life of up to 6 days at 15∘C Jeonget al reported that spraying cinnamon bark extract on thesurface of the fried fish-paste products could inhibit thegrowth of spoilage bacteria and mold at room temperatureand resulted in prolonged shelf-life [127]

Yamazaki et al investigated the effects of nisin andsucrose fatty acid esters on the growth of spoilage bacteria infish-paste products [130] Nisin exerted antibacterial activityagainst Bacillus subtilis and Bacillus licheniformis in a liquidmedium at 20∘C and resulted in a longer shelf-life forfish-paste products It was concluded that the addition ofnisin could be used as a potential alternative method toprevent spoilage caused by spore-forming bacteria in fish-paste productsThe bacteriocin produced byCarnobacteriummaltalomaticum had the ability to inhibit both Enterococcussp and Leuconostoc sp which reduce the shelf-life of fish-paste products during preservation [131] The results showedthat the purified bacteriocin piscicolin KH1 andor nisin sig-nificantly inhibited the growth of Leuconostoc mesenteroidesand Enterococcus faecium and could be used as a food-gradepreservative for kamaboko gels

24 Journal of Food Quality

Sakai and Yamaguchi examined the possibility of inhibit-ing lipid oxidation in boiled fish-paste by adding yuzu skinto the surimi [209] The heat-treated control kamabokoand yuzu skin-added kamaboko (citron kamaboko) wererefrigerated at 0∘C for 2 days and after heating the surimithe malonaldehyde content in both kamabokos was reducedThese results suggest that the addition of citron skin sup-pressed lipid oxidation in fish-paste products

Various packing materials and wrapping techniques havealso been employed to keep fish-paste products fresh and freeof contaminants for a longer period of time Lee et al investi-gated the processing conditions and quality stability of retortpouched fried-mackerel fish-paste during storage [210] Themackerel fish-paste was ground with added ingredients friedin soybean oil cooled vacuum-packed in a laminated plasticfilm and finally sterilized at 120∘C for 20min in a hotwater circulating retortThe reported method showed a goodpreservation for 100 days at 25 plusmn 3∘CThe sensory evaluationshowed no significant differences between the prepared fish-paste products and that of products in the market Ha et alexamined the optimum storage conditions for maintainingthe quality of the fried fish-paste in retort pouches [211]Both hardness and gel strength increased with increasingsterilization temperature On the other hand no differenceswere observed in elasticity and water-holding capacity

Lee et al elucidated the antioxidative effects of soyandor zein protein films containing green tea extract on thephysiological properties of fish-paste products during storage[132]The soy protein films showed an increase in yellownesswhile a decrease in yellowness was observed with the zeinfilms The lipid oxidation was retarded at day 2 of storageby wrapping the fried fish-paste products with soy and zeinprotein films containing green tea extract Lim et al prepareda Gelidium corneum whey protein isolate (GC-WPI) blendfilm containing grapefruit seed extract and studied the effectof this film on pathogenic bacterial inhibition during storage[133]TheGC-WPI blend was effective in decreasing the pop-ulations of Salmonella typhimurium Listeria monocytogenesand Escherichia coli on films treated with 01 grapefruitseed extract These studies suggest that packaging fish-pasteproducts in plant-based protein films containing green tea orgrapefruit seed extract could be beneficial to prolong shelf-life

5 Conclusion

The production of surimi dates back to ancient times How-ever advancement in surimi processing technology startedin 1960 with the discovery of cryoprotectants which werehelpful in maintaining the gel quality and functionality offish-paste for relatively longer periods of frozen storage [3]As themarket share of quality-conscious consumers rises thedemand for the use of natural additives rather than chemicalingredients for surimi products will continue to increaseAccording to Park et al the worldwide production of surimi-related products reached around 800000MT by 2011-2012while the main fish sources for surimi products includePacificwhitingAlaska pollock jackmackerel Atkamackerelsouthern blue whiting northern blue whiting and hoki [3]

Surimi is subdivided into high-grade (FA SA and A) andlow-grade (KA KB and RA) types based on the quality ofthe raw fish sources Most of the high-grade surimi is soldin Japan for the production of kamaboko and other high-quality surimi products and in Korea for the production ofpremium crabsticks Low-grade surimi is sold in Europe andthe United States for the manufacturing of crab sticks andin Korea and Japan for the preparation of other fried fishproducts [3] With the technological advancements in thesurimi processing industry it has been possible to use low-grade surimi for the production of fish cakes fish balls andother surimi products

With increasing demand and new processing techniques(eg the pH-shift method) the use of other seafoodresources such as small pelagic species and giant squid forthe production of surimi and surimi products was possible[212] Notably the production of surimi products is cheaperinKorea than elsewhere but industry professionals are alwayssearching for the most inexpensive surimi seafood sourcesHence the production of surimi from aquaculture fish suchas catfish and carp is growing in demand

Food additives from animal and seafood sources suchas fish chicken beef plasma proteins and egg white areconsidered the most effective protease inhibitors for surimiHowever with the outbreak of avian influenza mad cow dis-ease undesirable resulting characteristics and some religiousconstraints there is limited use of these food additives Addi-tionally vegetarians in some parts of the world would notwish to consume surimi-based products containing additivesderived from animals or even from seafood sources Hencethere is a need to identify more effective and alternative food-grade ingredients (eg plant sources seaweed and microal-gae) to be used in the preparation of fish-paste products

Surimi is mainly used for human consumption As suchthe challenges of production cost composition nutritionalvalue and the shelf-life of surimi products can never beneglected This review has provided an overview of nat-ural and synthetic food additives and preservatives usedto enhance the quality functionality and shelf-life of fish-paste products In addition the improvements in the fish-paste product quality and functionality by various foodadditives from seafood plants mushrooms animal sourcesand functional materials were discussed

For decades surimi and surimi-based products have beenwell known in East Asian countries such as Japan and KoreaHowever with advancements in technology they are attract-ing attention in other Asian as well as European countriesWith the increasing consumption worldwide the manufac-turing and processing of fish-paste products may requirenew and improved additives to enhance their acceptability inthe market Continuous scientific innovations and improvedprocessing technology will aid in further advancements andimprovements in this area

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article and regarding thefunding received

Journal of Food Quality 25

Authorsrsquo Contributions

Khawaja Muhammad Imran Bashir and Jin-Soo Kim con-tributed equally to this work

Acknowledgments

This research was a part of the Project no PJT200885entitled ldquoDevelopment andCommercialization of TraditionalSeafood Products Based on the Korean Coastal MarineResourcesrdquo funded by the Ministry of Oceans and FisheriesSouth Korea

References

[1] H-J Hwang S-Y Choi and S-C Lee ldquoPreparation andquality analysis of sodium-reduced fried fish cakesrdquo PreventiveNutrition and Food Science vol 18 no 3 pp 222ndash225 2013

[2] KFDA Food code Article 1-5-12 Korea Food and Drug Admin-istration Seoul Korea 2012

[3] J W Park H Nozaki T Suzuki and J-L Beliveau ldquoHistoricalreview of surimi technology and market developmentsrdquo inSurimi and Surimi seafood J W Park Ed pp 3ndash24 CRC PressNew York NY USA 2013

[4] J A Ramırez R Dıaz-Sobac O G Morales and M VazquezldquoEvaluation of freeze-dried surimi from tilapia and fat sleeper asemulsifiers [Evaluacion de surimi liofilizado de tilapia y dormi-dor como emulsificantes evaluacion de surimi liofilizado detilapia e dormidor como emulsificantes]rdquo Ciencia y TechnologiaAlimentaria vol 2 no 4 pp 210ndash214 1999

[5] J M Aguilera and D W Stanley ldquoFood structuringrdquo inMicrostructural Principles of Food Processing and Engineeringvol 12 p 246 AN Aspen Publishers Gaithersburg MarylandUSA 1999

[6] A P Stone and D W Stanley ldquoMechanisms of fish muscle gela-tionrdquo Food Research International vol 25 no 5 pp 381ndash3881992

[7] S Nakamura and M Ogawa ldquoBiomolecular strategies forpreparation of high quality surimi-based productsrdquo PreventiveNutrition and Food Science vol 10 no 2 pp 191ndash197 2005

[8] M Okada ldquoHistory of surimi technology in Japanrdquo in Surimitechnology T C Lanier and C M Lee Eds pp 3ndash22 MarcelDekker Inc New York NY USA 1992

[9] MIFAFF ldquoStatistics of fisheries processingrdquo Ministry of FoodAgriculture Forestry and Fisheries Seoul Korea 2011

[10] T C Lanier ldquoMeasurement of surimi composition and junc-tional propertiesrdquo in Surimi technology T C Lanier and C MLee Eds pp 123ndash166 Marcel Dekker Inc New York NY USA1992

[11] K-H Chung and C-M Lee ldquoRelationships between physico-chemical properties of nonfish protein and textural propertiesof protein-incorporated surimi gelrdquo Journal of Food Science vol55 pp 972ndash975 1990

[12] M TMorrissey JWWuD Lin andHAn ldquoProtease inhibitoreffects on torsionmeasurements and autolysis of Pacific whitingsurimirdquo Journal of Food Science vol 58 no 5 pp 1050ndash10541993

[13] J W Park ldquoFunctional protein additives in surimi gelsrdquo Journalof Food Science vol 59 no 3 pp 525ndash527 1994

[14] S Benjakul W Visessanguan and C Srivilai ldquoGel propertiesof bigeye snapper (Priacanthus tayenus) surimi as affected by

setting and porcine plasma proteinsrdquo Journal of Food Qualityvol 24 no 5 pp 453ndash471 2001

[15] D D Hamann P M Amato M C Wu and E A FoegedingldquoInhibition of modori (gel weakening) in surimi by plasmahydrolysate and egg whiterdquo Journal of Food Science vol 55 pp665ndash669 1990

[16] K D Reppond and J K Babbitt ldquoProtease inhibitors affectphysical properties of arrowtooth flounder and walleye pollocksurimirdquo Journal of Food Science vol 58 pp 96ndash98 1993

[17] V C Weerasinghe M T Morrissey and H An ldquoCharacteriza-tion of active components in food-grade proteinase inhibitorsfor surimi manufacturerdquo Journal of Agricultural and FoodChemistry vol 44 no 9 pp 2584ndash2590 1996

[18] C-Y Yang ldquoEffect of the addition of bovine plasma on thequality properties of steamed fish pasterdquo The Korean Journal ofFood and Nutrition vol 21 pp 518ndash523 2008

[19] K Duangmal and A Taluengphol ldquoEffect of protein additivessodium ascorbate and microbial transglutaminase on the tex-ture and colour of red tilapia surimi gelrdquo International Journalof Food Science amp Technology vol 45 no 1 pp 48ndash55 2010

[20] S BenjakulW Visessanguan and C Chantarasuwan ldquoEffect ofporcine plasma protein and setting on gel properties of surimiproduced from fish caught inThailandrdquo LWT- Food Science andTechnology vol 37 no 2 pp 177ndash185 2004

[21] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoCysteine proteinase inhibitor from chicken plasma Fractiona-tion characterization and autolysis inhibition of fish myofibril-lar proteinsrdquo Food Chemistry vol 101 no 4 pp 1647ndash1657 2007

[22] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoEffect of chicken plasma protein and some protein additiveson proteolysis and gel-forming ability of sardine (SardinellaGibbosa) surimirdquo Journal of Food Processing and Preservationvol 31 no 4 pp 492ndash516 2007

[23] S Rawdkuen S Benjakul W Visessanguan and T C LanierldquoRheological and textural properties of pacific whiting surimigels as influenced by chicken plasmardquo International Journal ofFood Properties vol 11 no 4 pp 820ndash832 2008

[24] M Sugiyama T Mishiro Y Tsukamasa T Suzuki and KTakama ldquoPuncture properties of kamaboko with ovomucoidpasteurized at several temperaturesrdquo Nippon Suisan Gakkaishivol 64 no 1 pp 76ndash81 1998

[25] M Sugiyama T Mishiro Y Tsukamasa et al ldquoPhysical prop-erties of Kamaboko with ovomucoid pasteurized at severaltemperaturesrdquo Nippon Suisan Gakkaishi vol 64 no 1 pp 82ndash87 1998

[26] J Yongsawatdigul and P Piyadhammaviboon ldquoInhibition ofautolytic activity of lizardfish surimi by proteinase inhibitorsrdquoFood Chemistry vol 87 no 3 pp 447ndash455 2004

[27] L Campo-Deano and C Tovar ldquoThe effect of egg albumen onthe viscoelasticity of crab sticks made from Alaska pollock andPacific whiting surimirdquo Food Hydrocolloids vol 23 no 7 pp1641ndash1646 2009

[28] A Hunt J W Park and A Handa ldquoEffect of various types ofegg white on characteristics and gelation of fish myofibrillarproteinsrdquo Journal of Food Science vol 74 no 9 pp C683ndashC6922009

[29] S Rawdkuen and S Benjakul ldquoWhey protein concentrateAutolysis inhibition and effects on the gel properties of surimiprepared from tropical fishrdquo Food Chemistry vol 106 no 3 pp1077ndash1084 2008

26 Journal of Food Quality

[30] Y Ruttanapornvareesakul K Somjit A Otsuka et al ldquoCry-oprotective effects of shrimp head protein hydrolysate on gelforming ability and protein denaturation of lizardfish surimiduring frozen storagerdquo Fisheries Science vol 72 no 2 pp 421ndash428 2006

[31] D K Li H Lin and SM Kim ldquoEffect of rainbow trout (Oncor-hynchus mykiss) plasma protein on the gelation of Alaska pol-lock (Theragra chalcogramma) surimirdquo Journal of Food Sciencevol 73 no 4 pp C227ndashC234 2008

[32] A Hernandez-Briones G Velazquez M Vazquez and J ARamırez ldquoEffects of adding fish gelatin onAlaska pollock surimigelsrdquo Food Hydrocolloids vol 23 no 8 pp 2446ndash2449 2009

[33] T Yin Z H Reed and J W Park ldquoGelling properties of surimias affected by the particle size of fish bonerdquo LWT- Food Scienceand Technology vol 58 no 2 pp 412ndash416 2014

[34] T Yin and J W Park ldquoTextural and rheological properties ofPacific whiting surimi as affected by nano-scaled fish bone andheating ratesrdquo Food Chemistry vol 180 pp 42ndash47 2015

[35] M R Fowler and J W Park ldquoEffect of salmon plasma proteinon Pacific whiting surimi gelation under various ohmic heatingconditionsrdquo LWT- Food Science and Technology vol 61 no 2pp 309ndash315 2015

[36] M R Fowler and J W Park ldquoSalmon blood plasma Effectiveinhibitor of protease-laden Pacific whiting surimi and salmonmincerdquo Food Chemistry vol 176 pp 448ndash454 2015

[37] S Klomklao S Benjakul H Kishimura K Osako and BK Simpson ldquoTrypsin inhibitor from yellowfin tuna (Thunnusalbacores) roe Effects on gel properties of surimi from bigeyesnapper (Priacanthus macracanthus)rdquo LWT- Food Science andTechnology vol 65 pp 122ndash127 2016

[38] N K Vate and S Benjakul ldquoEffect of the mixtures of squid inktyrosinase and tannic acid on properties of sardine surimi gelrdquoJournal of Food Science and Technology vol 53 no 1 pp 411ndash420 2016

[39] T Yamashita ldquoEffects of commercial soybean protein andwheat gluten as subsidiary materials on physical properties ofkamabokordquo Nippon Shokuhin Kogyo Gakkaishi vol 38 no 12pp 883ndash890 1991

[40] K H Chung and C M Lee ldquoFunction of nonfish proteins insurimi-based gel productsrdquo Korean Journal of Society of FoodScience vol 10 pp 146ndash150 1994

[41] K-H Chung and C-M Lee ldquoEvaluation of wheat gluten andmodified starches for their texture-modifying and freeze-thawstabilizing effects on surimi based-productsrdquo Journal of FoodScience and Nutrition pp 190ndash195 1996

[42] S Benjakul S Karoon and A Suwanno ldquoInhibitory effects oflegume seed extracts on fish proteinasesrdquo Journal of the Scienceof Food and Agriculture vol 79 no 13 pp 1875ndash1881 1999

[43] S Benjakul W Visessanguan and P Thummaratwasik ldquoInhi-bition of gel weakening of threadfin bream surimi using Thailegume seed proteinase inhibitorsrdquo Journal of Food Biochem-istry vol 24 no 5 pp 363ndash380 2000

[44] A Oujifard S Benjakul M Ahmad and J Seyfabadi ldquoEffect ofbambara groundnut protein isolate on autolysis and gel prop-erties of surimi from threadfin bream (Nemipterus bleekeri)rdquoLWT- Food Science and Technology vol 47 no 2 pp 261ndash2662012

[45] Y Luo RKuwaharaMKaneniwa YMurata andMYokoyamaldquoEffect of soy protein isolate on gel properties of Alaska pollockand common carp surimi at different setting conditionsrdquoJournal of the Science of Food and Agriculture vol 84 no 7 pp663ndash671 2004

[46] Y Luo H Shen D Pan and G Bu ldquoGel properties of surimifrom silver carp (Hypophthalmichthys molitrix) as affected byheat treatment and soy protein isolaterdquo Food Hydrocolloids vol22 no 8 pp 1513ndash1519 2008

[47] C Cardoso B Ribeiro and R Mendes ldquoEffects of dietary fibreandmicrobial transglutaminase addition on the rheological andtextural properties of protein gels from different fish speciesrdquoJournal of Food Engineering vol 113 no 4 pp 520ndash526 2012

[48] T Kudre S Benjakul and H Kishimura ldquoEffects of proteinisolates from black bean and mungbean on proteolysis and gelproperties of surimi from sardine (Sardinella albella)rdquo LWT-Food Science and Technology vol 50 no 2 pp 511ndash518 2013

[49] S Klomklao and S Benjakul ldquoEffect of trypsin inhibitor inadzuki bean (Vigna angularis) on proteolysis and gel propertiesof threadfin bream (Nemipterus bleekeri)rdquo LWT- Food Scienceand Technology vol 63 no 2 pp 906ndash911 2015

[50] S Konoo H Ogawa and N Iso ldquoEffects of addition of amyloseand amylopectin on the breaking strength of fish meat gelrdquoNippon Suisan Gakkaishi vol 64 no 1 pp 69ndash75 1998

[51] C-S Kong H Ogawa and N Iso ldquoRheological analysis of theeffect of gelatinization of starch added to fish-meat gel based onvolume changesrdquo Fisheries Science vol 65 no 6 pp 930ndash9361999

[52] B-Y Kim W-W Kim and B Yoo ldquoEffect of native and acety-lated sweet potato starch on rheological properties of compositesurimi solrdquo Journal of Food Science and Nutrition vol 13 no 3pp 245ndash248 2008

[53] B-J Yoo ldquoThe effects of alkaline treatment and potato-starchcontent on the quality of fishmeat paste products prepared fromPacific sandlance Ammodytes personatus Girardrdquo Fisheries andAquatic Sciences vol 14 no 3 pp 161ndash167 2011

[54] S M Cho M S Yoon and S-B Kim ldquoEffects of rice flourmilling types and addition methods on rheological and sensoryproperties of surimi productsrdquo Korean Journal of Fisheries andAquatic Sciences vol 46 no 2 pp 139ndash146 2013

[55] Y-M Kwon and J-S Lee ldquoA study on the quality characteristicsof fish cakes containing rice flourrdquo Korean Journal of HumanEcology vol 22 no 1 pp 189ndash200 2013

[56] M Yoon J-S Kim D Kim J Jo and S Cho ldquoOptimization ofthe processing conditions for the preparation of surimi productscontaining rice flourrdquo Fisheries and Aquatic Sciences vol 17 no2 pp 167ndash173 2014

[57] J A Ramırez M Barrera O G Morales and M VazquezldquoEffect of xanthan and locust bean gums on the gelling prop-erties of myofibrillar proteinrdquo Food Hydrocolloids vol 16 no 1pp 11ndash16 2002

[58] A M Barrera J A Ramırez J J Gonzalez-Cabriales and MVazquez ldquoEffect of pectins on the gelling properties of surimifrom silver carprdquo Food Hydrocolloids vol 16 no 5 pp 441ndash4472002

[59] S Benjakul W Visessanguan S Phatchrat and M TanakaldquoChitosan affects transglutaminase-induced surimi gelationrdquoJournal of Food Biochemistry vol 27 no 1 pp 53ndash66 2003

[60] M A Iglesias-Otero J Borderıas and C A Tovar ldquoUse ofKonjac glucomannan as additive to reinforce the gels from low-quality squid surimirdquo Journal of Food Engineering vol 101 no3 pp 281ndash288 2010

[61] S-H Eom J-A Kim B-Y Son et al ldquoEffects of carrageenanon the gelatinization of salt-based surimi gelsrdquo Fisheries andAquatic Sciences vol 16 no 3 pp 143ndash147 2013

Journal of Food Quality 27

[62] S H Choi and S M Kim ldquoQuality properties of giant squid(Dosidicus gigas) surimi-based product manufactured withAmorphophallus konjac flourrdquo Korean Journal of Food Scienceand Technology vol 44 no 4 pp 422ndash427 2012

[63] D Cando B Herranz A J Borderıas and H M MorenoldquoEffect of high pressure on reduced sodium chloride surimigelsrdquo Food Hydrocolloids vol 51 pp 176ndash187 2015

[64] D-S Kim and Y-H Park ldquoEffect of food humectants onlowering water activity of casing kamaboko 1 Effect of loweringwater activity of sodium chloride sugars and polyolsrdquo Bulletinof the Korean Fisheries Society vol 14 pp 139ndash147 1981

[65] D-S Kim and Y-H Park ldquoEffect of food humectant on lower-ingwater activity of casing kamaboko 2 Effect of loweringwateractivity of starch glycine and sodium lactate and prediction ofthe water activity lowing ability of humectantsrdquo Bulletin of theKorean Fisheries Society vol 15 pp 74ndash82 1982

[66] G L Sanchez Pascua M R Casales and M I Yeannes ldquoInflu-ence of water and glycerol contents on the aw of fish pastesrdquoJournal of Aquatic Food Product Technology vol 10 no 1 pp89ndash100 2001

[67] E Niwa K Tsujimoto and S Kanoh ldquoKamaboko gel-strength-ening effect of polyuronides and other polysaccharidesrdquoNipponSuisan Gakkaishi vol 58 pp 85ndash88 1992

[68] R Yoshinaka M Shiraishi and S Ikeda ldquoEffect of AscorbicAcid on theGel Formation of FishMeatrdquoBulletin of the JapaneseSociety for the Science of Fish vol 38 no 5 pp 511ndash515 1972

[69] H G Lee C M Lee K H Chung and S A Lavey ldquoSodiumascorbate affects surimi gel-forming propertiesrdquo Journal of FoodScience vol 57 pp 1343ndash1347 1992

[70] Y Park S D Kelleher D J McClements and E A DeckerldquoIncorporation and stabilization of omega-3 fatty acids insurimi made from cod Gadus morhuardquo Journal of Agriculturaland Food Chemistry vol 52 no 3 pp 597ndash601 2004

[71] E Okazaki Y Yamashita and Y Omura ldquoEmulsification of fishoil in surimi by high-speed mixing and improvement of gel-forming abilityrdquo Nippon Suisan Gakkaishi vol 68 no 4 pp547ndash553 2002

[72] H Fukushima E Okazaki S Noda and Y Fukuda ldquoChangesin physical properties water holding capacity and color of heat-induced surimi gel prepared by emulsification with fish oilrdquoNippon Shokuhin Kagaku Kogaku Kaishi vol 54 no 1 pp 39ndash44 2007

[73] B N Pietrowski R Tahergorabi and J Jaczynski ldquoDynamicrheology and thermal transitions of surimi seafood enhancedwith 120596-3-rich oilsrdquo Food Hydrocolloids vol 27 no 2 pp 384ndash389 2012

[74] A K Balange S Benjakul and S Maqsood ldquoGel strengtheningeffect of wood extract on surimi produced frommackerel storedin icerdquo Journal of Food Science vol 74 no 8 pp C619ndashC6272009

[75] N Buamard and S Benjakul ldquoImprovement of gel properties ofsardine (Sardinella albella) surimi using coconut husk extractsrdquoFood Hydrocolloids vol 51 pp 146ndash155 2015

[76] A K Balange and S Benjakul ldquoEffect of oxidised phenolic com-pounds on the gel property of mackerel (Rastrelliger kanagurta)surimirdquo LWT- Food Science and Technology vol 42 no 6 pp1059ndash1064 2009

[77] A Balange and S Benjakul ldquoEnhancement of gel strength ofbigeye snapper (Priacanthus tayenus) surimi using oxidisedphenolic compoundsrdquo Food Chemistry vol 113 no 1 pp 61ndash702009

[78] Y A Arfat and S Benjakul ldquoEffect of zinc sulphate on gellingproperties of phosphorylated protein isolate from yellow stripetrevallyrdquo Food Chemistry vol 141 no 3 pp 2848ndash2857 2013

[79] M-S Bae and S-C Lee ldquoQuality characteristics of fried fishpaste containing anchovy powderrdquo Journal of the Korean Societyof Food Science and Nutrition vol 36 no 9 pp 1188ndash1192 2007

[80] M-S Bae J-U Ha and S-C Lee ldquoQuality properties of highcalcium fish paste containing anchovyrdquo Korean Journal of Foodand Cookery Science vol 23 pp 561ndash566 2007

[81] H-S Cho and K-H Kim ldquoQuality characteristics of fish pastecontaining skate (Raja kenojei) powderrdquo Journal of the EastAsian Society of Dietary Life vol 21 pp 808ndash813 2011

[82] Y H Park E Y Bum E R Jeon and LH Jung ldquoEffect of addedskate (Raja kenojei) on the quality characteristics of steamedfishmeat pasterdquo Food Science and Biotechnology vol 23 no 5 pp1453ndash1458 2014

[83] S-M Park B-B Lee Y-M Hwang and S-C Lee ldquoQualityproperties of fish paste containing Styela clavardquo Journal of theKorean Society of Food Science and Nutrition vol 35 pp 908ndash911 2006

[84] S-Y Choi E-Y Choi K-E Lee A-S Song S-H Park and S-C Lee ldquoPreparation and quality analysis of fish paste containingStyela clava tunicrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 41 no 11 pp 1591ndash1595 2012

[85] S-M Park H-K Seo and S-C Lee ldquoPreparation and qualityproperties of fish paste containing Styela plicatardquo Journal of theKorean Society of Food and Nutrition vol 35 pp 1256ndash12592006

[86] J-S Seo and H-S Cho ldquoQuality characteristics of fish pastewith shrimp powderrdquo Korean Journal of Food Preservation vol19 pp 519ndash524 2012

[87] H-S Cho and K-H Kim ldquoQuality properties of fish pastecontaining green laver powderrdquo Journal of the Korean Societyof Food Culture vol 29 pp 421ndash427 2014

[88] I-D Park ldquoQuality characteristics of fish paste containingLagocephalus lunaris powderrdquo Journal of the Korean Society ofFood Culture vol 28 pp 657ndash663 2013

[89] I Park ldquoQuality properties of fish paste containingCapsosiphonfulvescens powderrdquo Journal of The Korean Society of FoodCulture vol 31 no 4 pp 357ndash363 2016

[90] B-M Kim J-H Jung M-J Jung D-S Kim J-Y Jun and I-H Jeong ldquoThe quality characteristics and processing of fishpaste containing red snow crabChionoecetes japonicus leg-meatpowderrdquo Korean Journal of Fisheries and Aquatic Sciences vol49 pp 1ndash6 2016

[91] Y-J Shin and G-S Park ldquoQuality characteristics of fish-pastecontaining mulberry leaf powderrdquo Journal of the East AsianSociety of Dietary Life vol 15 pp 738ndash745 2005

[92] Y-J Shin ldquoQuality characteristics of fish paste containing lotus(Nelumbo nucifera) leaf powderrdquo Korean Journal of Food andCookery Science vol 23 pp 947ndash953 2007

[93] A D Thorat V R Joshi A U Pagarkar and A K BalangeldquoMicrowave pasteursation of fish paste product-Kamabokowith Beetroot and Spinachrdquo Ecology Environment and Conser-vation vol 13 no 1 pp 113ndash118 2007

[94] M-O Yang and E-J Cho ldquoQuality properties of surimi withadded citrus fruitsrdquo Journal of East Asian Society of Dietary Lifevol 17 pp 58ndash63 2007

[95] F Alakhrash U Anyanwu and R Tahergorabi ldquoPhysicochemi-cal properties of Alaska pollock (Theragra chalcograma) surimigels with oat branrdquo LWT- Food Science and Technology vol 66pp 41ndash47 2016

28 Journal of Food Quality

[96] J-S Kim and G-I Byun ldquoMaking fish paste with yam (Dios-corea japonica Thumb) powder and its characteristicsrdquo KoreanJournal of Culinary Research vol 15 pp 57ndash69 2009

[97] Y-J Shin J A Lee and G-S Park ldquoa Quality characteristics offish pastes containing Lycii fructus powderrdquo Journal of the EastAsian Society of Dietary Life vol 18 pp 22ndash28 2008

[98] D-W Shim J Jiang J-H Kim et al ldquoEffects of size adjustedwith red ginseng powders on quality of fish pastesrdquo Journal ofthe Korean Society of Food Science and Nutrition vol 41 no 10pp 1448ndash1453 2012

[99] Y-J Shin J A Lee and G-S Park ldquoQuality characteristics offish paste containing Angelicae gigantis Radix powderrdquo KoreanJournal of Food and Cookery Science vol 24 pp 699ndash705 2008

[100] S Choi ldquoQuality characteristics of fish paste containing Cur-cuma longa L powderrdquo The Korean Journal of Food and Nutri-tion vol 25 no 4 pp 833ndash841 2012

[101] J-A Jang H-A Kim and S-K Choi ldquoQuality characteristicsof fish cake made with silver pomfret (Pampus argenteus) withadded wasabi powderrdquo Journal of the East Asian Society ofDietary Life vol 20 pp 103ndash112 2010

[102] Y-J Shin K-S Kim and G-S Park ldquoTexture and sensorycharacteristics of fish paste containing white Poria cocos wolfpowderrdquo Korean J Food Cookery Sci vol 25 pp 119ndash125 2009

[103] J-U Ha S-G Koo H-Y Lee Y-M Hwang and S-C LeeldquoPhysical properties of fish paste containing Agaricus bisporusrdquoKorean Journal of Food Science and Technology vol 33 pp 451ndash454 2001

[104] S-G Koo Y-K Ryu Y-M Hwang J-U Ha and S-C LeeldquoQuality properties of fish-paste containing enoki mushroom(Flammuilna velutipes)rdquo Journal of the Korean Society of FoodScience and Nutrition vol 30 pp 288ndash291 2001

[105] M-H Son S-Y Kim J-U Ha and S-C Lee ldquoTexture prop-erties of surimi gel containing shiitake mushroom (Lentinusedodes)rdquo Journal of the Korean Society of Food Science andNutrition vol 32 pp 859-853 2003

[106] S-Y Kim M-H Son J-U Ha and S-C Lee ldquoPreparationand characterization of fried surimi gel containing king oystermushroom (Pleurotus eryngii)rdquo Journal of the Korean Society ofFood Science and Nutrition vol 32 pp 855ndash858 2003

[107] S I Chung S Y Kim Y J Nam andM Y Kang ldquoDevelopmentof surimi gel from king oyster mushroom and cuttlefish meatpasterdquo Food Science and Biotechnology vol 19 no 1 pp 51ndash562010

[108] S K Jin J H Park and S J Hur ldquoEffect of substituting surimiwith spent laying hen meat on the physicochemical character-istics of fried fish pasterdquo Food and Bioprocess Technology vol 7no 3 pp 901ndash908 2014

[109] A Debusca R Tahergorabi S K Beamer K E Matak and JJaczynski ldquoPhysicochemical properties of surimi gels fortifiedwith dietary fiberrdquo Food Chemistry vol 148 pp 70ndash76 2014

[110] H-S Yook J-W Lee H-J Lee B-S Cha S-Y Lee and M-W Byun ldquoQuality properties of fish paste prepared with refineddietary fiber from ascidian (Halocynthia roretzi) tunicrdquo Journalof the Korean Society of Food Science and Nutrition vol 29 pp642ndash646 2000

[111] A Debusca R Tahergorabi S K Beamer S Partington andJ Jaczynski ldquoInteractions of dietary fibre and omega-3-rich oilwith protein in surimi gels developed with salt substituterdquo FoodChemistry vol 141 no 1 pp 201ndash208 2013

[112] C Sell S Beamer J Jaczynski and K E Matak ldquoSensorycharacteristics and storage quality indicators of surimi franks

nutritionally enhanced with omega-3 rich flaxseed oil andsalmon oilrdquo International Journal of Food Science amp Technologyvol 50 no 1 pp 210ndash217 2015

[113] T Chang C Wang X Wang L Shi H Yang and M CuildquoEffects of soybean oil moisture and setting on the textural andcolor properties of surimi gelsrdquo Journal of Food Quality vol 38no 1 pp 53ndash59 2015

[114] J-S Kim M-L Cho and M-S Heu ldquoQuality improvement ofheat-induced surimi gel using calcium powder of cuttle Sepiaesculenta bone treated with acetic acidrdquo Journal of the KoreanFisheries Society vol 36 pp 198ndash203 2003

[115] G-W Kim G-H Kim J-S Kim et al ldquoQuality characteristicsof fried fish paste of Alaska pollack meat paste added withpropolisrdquo Journal of the Korean Society of Food Science andNutrition vol 37 no 4 pp 485ndash489 2008

[116] G-W Kim G-H Kim J-S Kim et al ldquoQuality of fried fishpaste prepared with sand-lance (Hypoptychus dybowskii) meatand propolis additiverdquo Journal of the Korean Fisheries Societyvol 41 pp 170ndash175 2008

[117] B Park H Cho and S Park ldquoStudy on quality characteristicsof fish paste containing cheonggukjang powderrdquo Journal of TheKorean Society of Food Culture vol 30 no 2 pp 213ndash219 2015

[118] SMiyao T Shindoh KMiyamori and T Arita ldquoEffects of highpressurization on the growth of bacteria derived from surimi(fish paste)rdquo Nippon Shokuhin Kogyo Gakkaishi vol 40 pp478ndash484 1993

[119] A Malicki Z Sysak S Bruzewicz J Zrodłowska-Danek andM Szpak ldquoApplication of high hydrostatic pressure to extendthe shelf-life of traditionally produced fish pasterdquo MedycynaWeterynaryjna vol 66 pp 695ndash698 2010

[120] J-H Kim J-Y Jeon S-R Ryu et al ldquoMicrobial quality andphysiochemical changes of grilled fish paste in a group-mealservice affected by gamma-irradiationrdquo Korean Journal of FoodPreservation vol 11 pp 522ndash529 2004

[121] H-O Cho J-H Kwon M-W Byun and M-K Lee ldquoPreserva-tion of fried fish-paste by Irradiationrdquo Korean Journal of FoodScience and Technology vol 17 pp 474ndash481 1985

[122] H-Y Shin Y-J Lee I-Y Park J-Y Kim S-J Oh and K BSong ldquoEffect of chlorine dioxide treatment onmicrobial growthand qualities of fish paste during storagerdquo Journal of the KoreanSociety for Applied Biological Chemistry vol 50 pp 42ndash47 2007

[123] S S YoonH Kim YM Lee E J Jeong andY J Cha ldquoShelf-lifeextension effects of fish paste product by adding pepper extractrdquoin Proceedings of the Korean Nutrition Society Conference p 216Seoul Korea 2001

[124] E-S Ahn M-S Kim and D-H Shin ldquoScreening of natu-ral antimicrobial edible plant extract for dooboo fish pastemakkoli spoilage microorganismrdquo Korean Journal of FoodScience and Technology vol 26 pp 733ndash739 1994

[125] Y-M Kim B-H Lee S-H Lee I-S Shin and T-S LeeldquoThe preservative effect of egg white lysozyme added surimiproductsrdquo Bulletin of the Korean Fisheries Society vol 21 pp269ndash275 1988

[126] S-H Cho I-S Joo I-W Seo and Z-W Kim ldquoPreservativeeffect of grapefruit seed extract on fish meat productrdquo Journalof Food Hygiene and Safety vol 6 pp 67ndash72 1991

[127] E-T Jeong M-Y Park E-W Lee U-T Park and D-S ChangldquoAntimicrobial characteristics against spoilage microorganismsand food preservative effect of cinnamon (Cinnamomum cassiaBlume) bark extractrdquo Korean Journal of Life Science vol 8 pp648ndash653 1998

Journal of Food Quality 29

[128] D-S Chang H-R Cho H-S Lee M-Y Park and S-M LimldquoDevelopment of alginic acid hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 823ndash826 1998

[129] H-R Cho D-S Chang W-D Lee E-T Jeong and E-WLee ldquoUtilization of chitosan hydrolysate as a natural foodpreservative for fish-paste productsrdquo Korean Journal of FoodScience and Technology vol 30 pp 817ndash822 1998

[130] K Yamazaki T Tashiro S Shirahama J-Y Jun and Y KawaildquoGrowth inhibition of spore-forming bacteria in fish-pasteproducts by Nisinrdquo Nippon Shokuhin Kagaku Kogaku Kaishivol 61 no 2 pp 70ndash76 2014

[131] K Hashimoto M L Bari Y Inatsu S Kawamoto and J ShimaldquoBiopreservation of kamaboko (steamed surimi) using pisci-colin KH1 produced by Carnobacteriummaltalomaticum KH1rdquoJapanese Journal of FoodMicrobiology vol 28 pp 193ndash200 2011

[132] S H Lee M S Lee S K Park D H Bae S D Ha and K BSong ldquoPhysical properties of protein films containing green teaextract and its antioxidant effect on fish paste productsrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1063ndash1067 2004

[133] G-O Lim Y-H Hong and K B Song ldquoIncorporating grape-fruit seed extract into Gelidium corneum-whey protein isolateblend packaging film increases the shelf life of fish paste -Research noterdquo Journal of Food Science and Nutrition vol 13no 4 pp 370ndash374 2008

[134] T C Lanier J Yongsawatdigul and P Carvajal-RondanellildquoSurimi gelation chemistryrdquo in Surimi and Surimi Seafood J WPark Ed pp 101ndash139Marcel Dekker NewYork NYUSA 2013

[135] M Kinoshita H Toyohara and Y Shimizu ldquoPurification andproperties of a novel latent proteinase showing myosin heavychain-degrading activity from threadfin-bream musclerdquo TheJournal of Biochemistry vol 107 no 4 pp 587ndash591 1990

[136] D H Wasson J K Babbitt and J S French ldquoCharacterizationof a heat stable protease from arrowtooth flounder Atheresthesstomiasrdquo Journal of Aquatic Food Product Technology vol 1 no3-4 pp 167ndash182 1993

[137] T A Seymour M T Morrissey M Y Peters and H An ldquoPuri-fication and characterization of pacific whiting proteasesrdquoJournal of Agricultural and Food Chemistry vol 42 no 11 pp2421ndash2427 1994

[138] H An V Weerasinghe T A Seymour and M T MorrisseyldquoCathepsin degradation of Pacific whiting surimi proteinrdquoJournal of Food Science vol 59 pp 1013ndash1017 1994

[139] AFDF Ground fish quality chart Alaska fisheries departmentfoundation Anchorage Alaska 1992

[140] G Sylvia S Larkin and M T Morrissey ldquoQuality and resourcemanagement bioeconomic analysis of the Pacific whitingindustryrdquo in Recent Advances inMarine Science and TechnologyO Bellwood H Choat and N Saxena Eds James CookUniversity Townsville QS Australia 1994

[141] S H Choi and S M Kim ldquoDevelopment of giant squid(Ommastrephes bartrami) surimi-based products with gel tex-ture enhancers and the effects of setting on gel qualityrdquo Journalof the Korean Society of Food Science and Nutrition vol 41 no7 pp 975ndash981 2012

[142] J A Ramırez R M Uresti G Velazquez and M VazquezldquoFood hydrocolloids as additives to improve the mechanicaland functional properties of fish products A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1842ndash1852 2011

[143] S-K Kim H-G Byun P-J Park and F Shahidi ldquoAngiotensinI converting enzyme inhibitory peptides purified from bovine

skin gelatin hydrolysaterdquo Journal of Agricultural and FoodChemistry vol 49 no 6 pp 2992ndash2997 2001

[144] I Kimura M Sugimoto K Toyoda N Seki K-I Arai andT Fujita ldquoA study on the cross-links reaction of myosin inkamaboko rsquosuwarirsquo gelsrdquo Nippon Suisan Gakkaisi vol 57 pp1386ndash1396 1991

[145] H An M Y Peters and T A Seymour ldquoRoles of endogenousenzymes in surimi gelationrdquo Trends in Food Science amp Technol-ogy vol 7 no 10 pp 321ndash327 1996

[146] R Nopianti N Huda andN Ismail ldquoA review on the loss of thefunctional properties of proteins during frozen storage and theimprovement of gel-forming properties of Surimirdquo AmericanJournal of Food Technology vol 6 no 1 pp 19ndash30 2011

[147] A M Martın-Sanchez C Navarro J A Perez-Alvarez and VKuri ldquoAlternatives for efficient and sustainable production ofsurimi A reviewrdquo Comprehensive Reviews in Food Science andFood Safety vol 8 no 4 pp 359ndash374 2009

[148] Korea Agro-Fisheries and Food Trade Corporation Processedfood segmented market survey-fish cake market Korea Agro-Fisheries and Food Trade Corporation Seoul Korea 2014

[149] D Kraft and A DerMarderosian The A-Z guide to food asmedicine CRC Press Boca Raton Fla USA 2016

[150] C V Morr and E A Foegeding ldquoComposition and function-ality of commercial whey and milk protein concentrates andisolates a status reportrdquo Food Technology vol 44 pp 100ndash1121990

[151] A Saiga T Okumura T Makihara et al ldquoAngiotensin I-converting enzyme inhibitory peptides in a hydrolyzed chickenbreast muscle extractrdquo Journal of Agricultural and Food Chem-istry vol 51 no 6 pp 1741ndash1745 2003

[152] B Li F Chen X Wang B Ji and Y Wu ldquoIsolation and iden-tification of antioxidative peptides from porcine collagenhydrolysate by consecutive chromatography and electrosprayionization-mass spectrometryrdquo Food Chemistry vol 102 no 4pp 1135ndash1143 2007

[153] A Trampuz R M Prabhu T F Smith and L M BaddourldquoAvian Influenza A New Pandemic Threatrdquo Mayo ClinicProceedings vol 79 no 4 pp 523ndash530 2004

[154] M C Gomez-Guillen B Gimenez M E Lopez-Caballeroand M P Montero ldquoFunctional and bioactive properties ofcollagen and gelatin from alternative sources A reviewrdquo FoodHydrocolloids vol 25 no 8 pp 1813ndash1827 2011

[155] D Li X Fu and S M Kim ldquoProduction of chum salmoncystatin from the recombinant Saccharomyces cerevisiae opti-mized using response surface methodologyrdquo Biotechnology andBioprocess Engineering vol 15 no 2 pp 314ndash323 2010

[156] H Akazawa Y Miyauchi K Sakurada H Wasson and K DReppond ldquoEvaluation of protease inhibitors in Pacific whitingsurimirdquo Journal of Aquatic Food Product Technology vol 2 no3 pp 79ndash95 1994

[157] A Hunt K J K Getty and J W Park ldquoRoles of starch in surimiseafood A reviewrdquo Food Reviews International vol 25 no 4 pp299ndash312 2009

[158] T Suzuki Fish and Krill Protein Processing Technology AppliedScience Publishers London UK 1981

[159] C M Lee ldquoSurimi process technologyrdquo Food Technology vol38 pp 69ndash80 1984

[160] M C Wu D D Hamann and T C Lanier ldquoRheological andcalorimetric investigations of starch-fish protein systems duringthermal processingrdquo Journal of Texture Studies vol 16 pp 53ndash74 1985

30 Journal of Food Quality

[161] M C Wu T C Lanier and D D Hamann ldquoRigidity and vis-cosity changes of croaker actomyosin during thermal gelationrdquoJournal of Food Science vol 50 no 1 pp 14ndash19 1985

[162] S-K Kim S-T Yang and E-H Lee ldquoThe starch content of fish-paste products onmarketrdquo Journal of the Korean Society of FoodScience and Nutrition vol 7 pp 41-42 1978

[163] G AMacDonald T C Lanier and P A Caruajal ldquoStabilizationof protein in surimirdquo in Surimi and Surimi Seafood J W ParkEd pp 91ndash125 Marcel Dekker Inc New York NY USA 2000

[164] J A Ramırez I A Santos O G Morales M T Morrisseyand M Vazquez ldquoApplication of microbial transglutaminaseto improve mechanical properties of surimi from silver carputilizacionde transglutaminasa microbiana paramellora-las-propiedades mecanicas de surimide carpaplateada utiliza-cionde transglutaminasamicrobiana paramejorarlaspropieda-des mecanicas de surimide carpaplateadardquo Ciencia y TecnologıaAlimentaria vol 3 no 1 pp 21ndash28 2000

[165] M C Gomez-Guillen A J Borderıas and P MonteroldquoSalt nonmuscle proteins and hydrocolloids affecting rigiditychanges during gelation of giant squid (Dosidicus gigas)rdquoJournal of Agricultural and Food Chemistry vol 45 no 3 pp616ndash621 1997

[166] J W Park ldquoIngredient technology and formulation develop-mentrdquo in Surimi and Surimi Seafood J W Park Ed pp 91ndash125Marcel Dekker Inc New York NY USA 2000

[167] F Garcıa-Ochoa V E Santos J A Casas and E Gomez ldquoXan-than gum production recovery and propertiesrdquo BiotechnologyAdvances vol 18 no 7 pp 549ndash579 2000

[168] A I Rodrıguez-Hernandez and A Tecante ldquoDynamic vis-coelastic behavior of gellan- 120580 -carrageenan and gellan-xanthangelsrdquo Food Hydrocolloids vol 13 no 1 pp 59ndash64 1999

[169] J A Casas and F Garcıa-Ochoa ldquoSophorolipid production byCandida bombicola Medium composition and culture meth-odsrdquo Journal of Bioscience and Bioengineering vol 88 no 5 pp488ndash494 1999

[170] H J Lim ldquoA study on the calcium and sodium intakes andurinary calcium excretion of preschool children in BusanrdquoKorean Journal of Nutrition vol 34 pp 786ndash796 2001

[171] WHO ldquoDiet nutrition and the prevention of chronic diseasesReport of a joint WHOFAO expert consultationrdquo Tech RepWHO World Health Organization Geneva Switzerland 2003

[172] L K Dahl ldquoPossible role of salt intake in the development ofessential hypertensionrdquo International Journal of Epidemiologyvol 34 no 5 pp 967ndash972 2005

[173] H-K Jeong D-S Kim S-J Chun K-S Jo and Y-H ParkldquoEffect of food humectant on lowering water activity of casingKamaboko 3rdquo Bulletin of the Korean Fisheries Society vol 16 pp88ndash96 1983

[174] J Han E Kim M Cheong S Chee and K Chee ldquoBioavailabil-ity and digestibility of organic calcium sources by bone healthindexrdquo Journal of Nutrition and Health vol 43 no 1 pp 12ndash252010

[175] M K Lee ldquoA study of the bio-functional evaluation of Rajaskates caught in Huksando areardquo Journal of the Kwangju HealthCollege vol 21 pp 253ndash265 1996

[176] S H Cho Extraction and characterization of gelatin andantimicrobial peptide from skate (Raja kenojei) skins ChonnamNational University Gwangju Korea 2003

[177] J H Choi ldquoIsolation and purification of in chondroitin sulfatefrom skate cartilagerdquo Tech Rep Pukyong National UniversityBusan Korea 2004

[178] Y G Jo ldquoThe sterol composition of Styela clavardquo Journal of theKorean Fisheries Society vol 11 pp 97ndash101 1978

[179] S H Ahn ldquoExtraction of glycosaminoglycans from Styela clavatunicrdquo Biotechnology and Bioprocess Engineering vol 18 pp180ndash185 2003

[180] J J Kim S J Kim S H Kim H R Park and S C LeeldquoAntioxidant and anticancer activities of extracts from Styelaclava according to the processing methods and solventsrdquoJournal of the Korean Society of Food Science and Nutrition vol35 pp 278ndash283 2006

[181] T Aoki K Takata and N Kunisaki ldquoComparison of nutrientcomponents of six species of wild and cultured fishesrdquo Bulletinof the Japanese Society for the Science of Fish vol 57 pp 1927ndash1934 1991

[182] Committee Donguibogam Translated Donguibogam Bubin-munwha Press Seoul Korea 1999

[183] Y-K Park H-J Kim and M-H Kim ldquoQuality characteristicsof fried fish paste added with ethanol extract of onionrdquo Journalof the Korean Society of Food Science and Nutrition vol 33 pp1049ndash1055 2004

[184] G L Dong J J Hyun and E-R Woo ldquoAntimicrobial prop-erty of (+)-lyoniresinol-3120572-O-120573-D- glucopyranoside isolatedfrom the root bark of Lycium chinense Miller against humanpathogenic microorganismsrdquo Archives of Pharmacal Researchvol 28 no 9 pp 1031ndash1036 2005

[185] C C Wang S C Chang B S Inbaraj and B H ChenldquoIsolation of carotenoids flavonoids and polysaccharides fromLycium barbarum L and evaluation of antioxidant activityrdquoFood Chemistry vol 120 no 1 pp 184ndash192 2010

[186] Z Zhang X Liu T Wu et al ldquoSelective suppression of cervicalcancer Hela cells by 2-O-120573-d- glucopyranosyl-l-ascorbic acidisolated from the fruit of Lycium barbarum Lrdquo Cell Biology andToxicology vol 27 no 2 pp 107ndash121 2011

[187] J S Kil M G Kim H M Choi et al ldquoInhibitory effects ofAngelicae GigantisRadix on osteoclast formationrdquo PhytotherapyResearch vol 22 no 4 pp 472ndash476 2008

[188] ANiranjan andD Prakash ldquoChemical constituents and biolog-ical activities of turmeric (Curcuma longa L) - a reviewrdquo Journalof Food Science and Technology vol 45 pp 109ndash116 2008

[189] K S Kim M G Choung and S H Park ldquoQuantitativedetermination and stability of curcuminoid pigments fromturmeric (Curcuma longaL) rootrdquo Korean Journal of CropScience vol 50 pp 211ndash215 2005

[190] I S Shin and J M Lee ldquoStudy on antimicrobial and antimuta-genic activity of horseradish (Wasabia japonica) root extractsrdquoJournal of the Korean Fisheries Society vol 31 pp 835ndash841 1998

[191] Y J ChoA study on the antioxidative and antimicrobial activitiesof wasabi (Wasabia koreana Cruciferae) extracts [PhD thesis]Sungshin Womens University Seoul Korea 2008

[192] A-S Kang T-S Kang H-R Shon et al ldquoStudies on improve-ment of artificial cultivation and antioxidative activity of Poriacocosrdquo The Korean Journal of Mycology vol 27 pp 378ndash3801999

[193] J-H Lee Y J Lee J-K Shin et al ldquoEffects of triterpenoidsfrom Poria cocos Wolf on the serotonin type 3A receptor-mediated ion current in Xenopus oocytesrdquo European Journal ofPharmacology vol 615 no 1ndash3 pp 27ndash32 2009

[194] K R Im M J Kim T K Jung and K S Yoon ldquoAnalysisof isoflavonoid contents in Astragalus membranaceus Bungecultivated in different areas and at various agesrdquo The KoreanSociety for Biotechnology and Bioengineering vol 25 pp 271ndash276 2010

Journal of Food Quality 31

[195] Y E Lee and S H Hong Oriental Medicine Food MaterialsKyomunsa Seoul Korea 2003

[196] D H Kim ldquoQuality characteristics of fish paste prepared withAstragalus membranaceus powderrdquo Food Engineering Progressvol 15 pp 362ndash369 2011

[197] S-E Kim B S Hwang J-G Song S W Lee I-K Lee andB-S Yun ldquoNew bioactive compounds from Korean nativemushroomsrdquoMycobiology vol 41 no 4 pp 171ndash176 2013

[198] National Institute of Agricultural Science The Mushrooms inKorea Dongbang Media Co Ltd Seoul Korea 2004

[199] Y-J Gao M Zhang and W-P Chen ldquoStudy on processing offish paste with waste of grass carprdquo Journal of Food Science andBiotechnology vol 31 pp 1031ndash1038 2012

[200] S Tolasa C M Lee and S Cakli ldquoPhysical and oxidativestabilization of omega-3 fatty acids in surimi gelsrdquo Journal ofFood Science vol 75 no 3 pp C305ndashC310 2010

[201] B N Pietrowski R Tahergorabi K E Matak J C Tou andJ Jaczynski ldquoChemical properties of surimi seafood nutrifiedwith 120596-3 rich oilsrdquo Food Chemistry vol 129 no 3 pp 912ndash9192011

[202] S H Kim J L Yang and Y S Song ldquoPhysiological function ofcheonggukjangrdquo Food Industry and Nutrition vol 4 pp 40ndash461999

[203] R Walker ldquoToxicology of sorbic acid and sorbatesrdquo Food Addi-tives amp Contaminants Part A vol 7 no 5 pp 671ndash676 1990

[204] B R Thakur and T R Patel ldquoSorbates in fish and fish productsmdasha reviewrdquo Food Reviews International vol 10 no 1 pp 93ndash1071994

[205] C-Y Wang H-W Huang C-P Hsu and B B Yang ldquoRecentadvances in food processing using high hydrostatic pressuretechnologyrdquo Critical Reviews in Food Science and Nutrition vol56 no 4 pp 527ndash540 2016

[206] J H Kwon M W Byun and J S Kim ldquoMicrobiological andorganoleptic qualities of boiled-dried anchovies during post-irradiation periodrdquo Journal of the Korean Society of Food Scienceand Nutrition vol 25 pp 283ndash287 1996

[207] J Noh and J H Kwon ldquoThe quality and thermoluminescenceproperties of dried pollack during storage following irradia-tionrdquo Korean Journal of Food Science and Technology vol 36pp 711ndash716 2004

[208] I Tukenmez M S Ersen A T Bakioglu A Bicer and VPamuk ldquoDose dependent oxidation kinetics of lipids in fish dur-ing irradiation processingrdquo Radiation Physics and Chemistryvol 50 no 4 pp 407ndash414 1997

[209] T Sakai and T Yamaguchi ldquoEffects of yuzu peel addition onthe lipid oxidation in kamaboko Effects of yuzu peel additionon the lipid oxidation in kamabokordquo Bulletin of the Faculty ofAgriculture Miyazaki University vol 57 pp 101-102 2011

[210] E-H Lee K-S Oh J-G Koo H-S Park S-Y Cho and Y-J Cha ldquoStudies on processing and keeping quality of retortpouched foods (3) Preparation and keeping quality of retortpouched fried mackerel meat pasterdquo Bulletin of the KoreanFisheries Society vol 17 pp 373ndash382 1984

[211] J-H Ha E-H Lee J-S Kim S-G Ji and J-G Koo ldquoA study onthe thermal treatment conditions of retort pouched fried fish-paste 1 Influence of thermal treatment conditions on qualityrdquoBulletin of the Korean Fisheries Society vol 20 pp 573ndash581 1987

[212] P Guenneugues and J Ianelli ldquoSurimi resources and marketrdquoin Surimi and surimi seafood J W Park Ed pp 25ndash53 MarcelDekker Inc New York NY USA 2013

Research ArticleDevelopment of a Chemically Defined Medium forBetter Yield and Purification of Enterocin Y31 fromEnterococcus faecium Y31

Wenli Liu12 Lanwei Zhang23 and Huaxi Yi3

1College of Chemistry and Environmental Engineering Shenzhen University Shenzhen Guangdong 518060 China2School of Food Science amp Technology Harbin Institute of Technology 73 HuangHe Avenue Harbin Heilongjiang 150090 China3College of Food Science and Engineering Ocean University of China Yushan Road 5 Qingdao Shandong 266100 China

Correspondence should be addressed to Lanwei Zhang zhanglwhiteducn and Huaxi Yi yihxouceducn

Received 31 March 2017 Revised 17 July 2017 Accepted 2 August 2017 Published 6 September 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Wenli Liu et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The macro- and micronutrients in traditional medium such as MRS used for cultivating lactic acid bacteria especially forbacteriocin production have not been defined preventing the quantitative monitoring of metabolic flux during bacteriocinbiosynthesis To enhance Enterocin Y31 production and simplify steps of separation and purification we developed a simplifiedchemically definedmedium (SDM) for the growth of Enterococcus faeciumY31 and production of its bacteriocin Enterocin Y31Wefound that the bacterial growthwas unrelated toEnterocinY31 production inMRS therefore both the growth rate and theEnterocinY31 production were set as the index for investigation Single omission experiments revealed that 5 gL NaCl five vitamins twonucleic acid basesMgSO

4sdot7H2OMnSO

4sdot4H2OKH

2PO4 K2HPO4 CH3COONa fourteen amino acids and glucosewere essential

for the strainrsquos growth and Enterocin Y31 production Thus a novel simplified and defined medium (SDM) was formulated with30 components in total Consequently Enterocin Y31 production yield was higher in SDM as compared to either MRS or CDMSDM improved the Enterocin Y31 production and simplified the steps of purification (only two steps) which has broad potentialapplications

1 Introduction

Bacteriocins are ribosomally synthesised antimicrobial pro-teins or protein complexes that inhibit other bacteria andthey either have a narrow antimicrobial spectrum (againstthe same species) or broad antimicrobial spectrum (againstacross genera) [1 2] Bacteriocin produced by lactic acidbacteria (LAB) is generally regarded as safe (GRAS) andQualified Presumption of Safety (QPS) status [3 4] andit is a desirable trait as a food additive for extending theshelf-life of the fermented food and controlling the safetyof foods [5 6] Based on their molecular structure bac-teriocins can be divided into four groups class I bacte-riocins contain posttranslational modifications (lantibioticsand molecular weight le 5 kDa) class II bacteriocins areunmodified and include small heat-stable nonlanthionine-containing peptides [7] The third class includes large

heat-labile bacteriocins Finally the fourth class comprisescomplex bacteriocins containing a protein moiety with oneor more other lipids or carbohydrates [8] Most bacteriocinsproduced by the Enterococcus faecium group of LAB are classII bacteriocins One subgroup class IIa contains bacteriocinswith certain sequence motifs in their N-terminal halves andis active against the food pathogen Listeria monocytogenes[9] Class IIa bacteriocins have become a focus of researchowing to their low molecular weight good dispersity andhigh thermostability This is also a case of Enterocin Y31produced by E faecium Y31 in the current work [10]

Enterocin Y31 is a class IIa bacteriocin produced byE faecium Y31 [11] Previous research results showed thatEnterocin Y31 had broad spectrum inhibition activity againstBacillus subtilis ATCC 6633 Escherichia coli ATCC 25922Listeria monocytogenes ATCC 19111 Bacillus cereus CICC20463 Staphylococcus aureus and Salmonella enterica serovar

HindawiJournal of Food QualityVolume 2017 Article ID 9017452 8 pageshttpsdoiorg10115520179017452

2 Journal of Food Quality

TyphimuriumATCC 14028The isoelectric point of EnterocinY31 was 825 it was stable in both acidity and alkalescenceconditions hence Enterocin Y31 has a broad applicationprospect (not published) However two main drawbacks ofEnterocin Y31 with regard to application in foods are asfollows (1) bacteriocins are secreted in very small quan-tities in the production media and (2) the media used togrow the bacteriocin-producing strains are very complex[12] as the LAB are fastidious organisms requiring aminoacids B vitamins and various minerals for their growthThese components are normally provided by sources such assoybean meal yeast extract and meat extract All of thesesources contain proteins and peptides as sources of aminoacids which are often very closely related to the bacteriocinproduced Therefore purification of bacteriocin from sucha complex medium requires a series of steps At each stepthere is some loss and sometimes after the final purificationthe antimicrobial activity may be completely lost Complexmedia do not allow the examination of all individual mediumfactors [13 14] affecting bacteriocin production

Ricciardi reported a modified chemically defined med-ium to promote the growth of Lactobacillus casei and Lacto-bacillus plantarum groups [15] In the present study weimproved the chemically defined medium to improve theyield of Enterocin Y31 produced by E faecium Y31 Thereare four objectives of this study (1) to develop a newand improved production method for Enterocin Y31 (pro-duced by E faecium Y31) (2) to determine the macro- andmicronutrients necessary for cultivating E faecium Y31 andimproving Enterocin Y31 production (3) to develop a noveland simple separation and purificationmethod for EnterocinY31 (avoiding a series of chromatography steps and the lossof Enterocin Y31 activity) and (4) to compare Enterocin Y31production in a defined medium with that in a complexmediumThis is feasible using a completely defined mediumand a minimal medium for bacteriocin production can thusbe established

2 Materials and Methods

21 Strains and Growth Conditions The bacteriocin-pro-ducer strain E faecium Y31 isolated from Chinese traditionalfermented foods (fermented vegetable juice from Lanzhou)was previously found to produce class IIa bacteriocin [10]which wasmaintained as stock cultures inMRSmediumwith18 glycerol at minus80∘C

Escherichia coli ATCC 25922 was selected as a sensitivestrain for antimicrobial activity assays because the bacte-riocin produced by E faecium Y31 has the highest activityagainst E coli ATCC 25922 in gram-negative bacteria

22 Medium The growth of E faecium Y31 and productionof Enterocin Y31 in a defined medium in a fermenter werecompared with those in MRS (reference medium) used forthe optimisation of the growth of E faecium Y31 and theproduction of Enterocin Y31 This medium CDM consistedof 44 components described by Khan et al [12] (listed inTable 1) All chemicals used for the preparation of the definedmedium were of analytical grade and obtained from either

Sigma-Aldrich (St Louis MO USA) or BDH ChemicalsLtd (Poole UK) For all the experiments aqueous stocksolutions of the individual components were prepared inthe appropriate concentrations and sterilized by autoclav-ing with the exception of the heat-sensitive componentsThe heat-sensitive amino acids (asparagine glutamine andtryptophan) all of the B vitamins and FeSO

4were filter-

sterilized (pore size 022120583m membrane Millipore CorpBillerica MA USA) All the stock solutions were then storedat 4∘C except FeSO

4which was freshly prepared before each

experiment because it is prone to oxidation during storage Inaddition to the defined medium MRS medium was used asa reference for comparison with the defined medium beforeeach experiment

23 Determination of the Antimicrobial Activity of EnterocinY31 The antimicrobial activity of bacteriocin was monitoredusing the agar well diffusion assay (AWDA) as describedpreviously [16] with some modifications E faecium Y31 wascultured for two or three generations and then the cell-free supernatants (CFSs) of E faecium Y31 were preparedby centrifuging for 30min at 10000timesg Aliquots (80 120583L) ofthe cell-free supernatants (CFSs) of E faecium Y31 wereadded to the wells (6mm diameter) on double-layer agarplates previously inoculated with 02mL overnight cultureof the indicator strain E coli ATCC 25922 Plates were keptstatic at room temperature for 3 h to allow diffusion of theCFSs evenly in the agar and then the plates were incubatedfor 24 h at 37∘C The bacteriocin titre was determined byeliminating the effect of the organic acid eliminating theeffect of H

2O2 and protease verificationThe diameter of the

zone of inhibition (not including the wells) was measuredusing a Vernier caliper An arbitrary unit (AUmL) wasdefined as the reciprocal of the highest dilution that producedan inhibition zone Specific activity was expressed as that unitper milligram of protein

24 Protein Concentration Determination Protein concen-tration was determined by the BCA (bicinchoninic acid)microassay method (Pierce Rockford IL USA) [17]

25 Monitoring of the Growth of E faecium Y31 The ODvalue of the fermentation liquid of E faecium Y31 wasmonitored with UV spectrophotometry at 600 nm each hourSterile culture medium was used as blanks to subtract thebackground value Samples having an OD600 nm value ofmore than 07 were diluted with the sterile culture mediumand the corrected OD value was obtained by multiplying thedilution factor ODmax (600 nm) represents the maximumOD value of the growth of E faecium Y31 ODmax (600 nm)was calculated before any centrifugation

26 Determination of the Relative Growth Rate The relativegrowth rate was calculated according to Monod [18] Thefollowing equation was used to calculate the growth rate

120583 = [(lnOD2minus lnOD

1) divide (1199052minus 1199051)] divide 120583CDM (1)

where 120583 is the relative growth rate (hminus1) ln is the symbol fornatural logarithm and OD

1and OD

2are the corrected OD

Journal of Food Quality 3

Table 1 Composition of CDM and SDMmedium

Constituent ContentCDM SDM

Amino acids (g Lminus1)L-Asparagine 100 100L-Aspartic acid 100 mdashL-Glutamic acid 100 100L -Glutamine 100 mdashL-Cys 100 100L-Alanine 100 mdashL-Arginine 100 100Glycine 100 100L-Histidine 100 100L-Isoleucine 100 100L-Leucine 100 100L-Lysine 100 100L-Methionine 100 100L-Phenylalanine 100 100L-Proline 100 mdashL-Serine 100 100L-Threonine 100 100L-Tryptophan 100 100L-Tyrosine 100 mdashL-Valine 100 mdash

Nucleic acid bases (g Lminus1)AdemomeSO

4002 002

Guanine 002 mdashInosine 002 mdashXanthine 002 mdashUracil 002 002Thymine 002 mdashOrotic acid 002 mdash

B vitamins (mgsdotLminus1)Biotin 2000 2000Para-aminobenzoic acid 1000 mdashNicotinic acid 200 200Ca-pantothenic acid 2000 2000Riboflavin 200 200Folic acid 200 200Cyanocobalamin 200 mdashThiamine 1000 mdashPyridoxal 2000 mdash

Minerals (gsdotLminus1)Manganese sulfate 005 005Magnesium sulfate 01 010Ferrous sulfate7H

2O 002 mdash

CaCl2

mdash mdashSodium citrate 500 500Potassium dihydrogen phosphate 200 200Dipotassium hydrogen phosphate 700 700

Table 1 Continued

Constituent ContentCDM SDM

Carbon source (gsdotLminus1)Glucose 1500 1500

Others (gsdotLminus1)Tween 80 100 100Glycerol mdash mdashNaCl mdash 500

27 Effects of NaCl CaCl2 and Glycerol on the Growth of Efaecium Y31 and Enterocin Y31 Production To determine theeffects of these components 5 gL 10 gL 15 gL and 20 gLNaCl 10 gL CaCl

2 and 50 gL glycerol were individually

added to 1000mLCDM andCDMmediumwith no addtionswas used as a control wherein the inoculum size was 2fermentation temperature was 37∘C and inoculum time was24 h The culturing liquid was then centrifuged for 20minat 10000timesg and then the CFSs were used to determineEnterocin Y31 activity and ODmax (24 h)

28 Effects of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth ofE faecium Y31 and Enterocin Y31 Production According tothe Leave One Out (LOO) technique each amino acid Bvitamin mineral and nucleic acid base was sequentially andindividually omitted from 1000mLCDMmedium andCDMwithout additions was used as a control The inoculum sizewas 2 fermentation temperature was 37∘C and inoculationtime was 24 h The culture liquid was then centrifugedfor 20min at 10000timesg and then the CFSs were used todetermine Enterocin Y31 activity and ODmax (24 h)

The following terms were used to describe the rela-tionship between each medium component and growth asdetermined by the single omission technique A constituentwas considered essential if its omission resulted in less thanhalf the maximum strain growth rate and production ofbacteriocin of the positive control stimulatory when itsabsence resulted in the fact that the growth rate and thebacteriocin production was between 50 and 80 of thatobserved in complete CDM and nonessential if the growthrate and Enterocin Y31 production was 80 (or more) of thatobtained in the complete CDM

29 Purification of Enterocin Y31 E faecium Y31 was allowedto grow in the SDM (Table 1) for 24 h The cells were thenremoved by centrifugation (11800timesg 25min) The CFSswere then filtered through a 022 120583m filter (low-protein-binding HVLP filter Millipore Corp) to remove any remain-ing cells These filtered CFSs were referred to as crude bacte-riocin The crude bacteriocin was subjected to ultrafiltrationof 1 kDa and 30 kDa The retentate from the 1 kDa step wasthen subjected to Tricine-SDS-PAGE

210 Statistical Analyses All experiments were preformedseparately three times and mean plusmn standard deviation (SD)values were calculated from triplicate determinations All

4 Journal of Food Quality

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 320002

0604

081012141618202224

ODpHInhibition zone diameter (mm)

Time (h)

OD

35404550556065707580

pH

0

2

4

6

8

10

12

14

Inhi

bitio

n zo

ne (

mm

)

Figure 1 Relationship between the growth of the bacteriocinogenicstrain and Enterocin Y31 production

data were subjected to one-way analysis of variance (one-way ANOVA) Comparison of means was performed withDuncanrsquos multiple range tests Statistical significance was setat 119875 lt 005

3 Results and Discussion

31 Relationship between the Growth of the Strain andEnterocin Y31 Activity The growth of E faecium Y31 wasunrelated to EnterocinY31 activity inMRSmedium as shownin Figure 1 The result was consistent with the result ofBacterocin J23 produced by Lactobacillus paracasei J23 asdescribed by Huaxi Yi in our research group (not published)whichwas inconsistentwith the result of Salivaricin producedby L salivarius CRL 1328 [19] thus the growth rate of EfaeciumY31 and Enterocin Y31 activity were used as detectionindexes for developing a novel chemical defined mediumEnterocin Y31 activity could be detected at the exponentialphase of the producing strain (9 h) and reached its highestvalue of 1126 plusmn 036mm at stationary phase of producingstrain (24 h) ODmax remained stable at 16 h of fermentationof strain Y31 thus ODmax (16 h) was used as an index of thestrain growth status

32 Effect of NaCl Concentration on the Growth of E faeciumY31 and Enterocin Y31 Production Theeffect of NaCl at 5 gL10 gL 15 gL and 20 gL was determined in CDMwith CDMwith no additives as the control The results indicated thatthe growth of E faecium Y31 and production of EnterocinY31 were not significant difference when adding 5 gL or10 gL NaCl and 0 gL and 15 gL NaCl had no effect onthe growth of strain Y31 and production of Enterocin Y31When the concentration of NaCl was 20 the growth of Efaecium Y31 and production of Enterocin Y31 reduced whichshowed the significant difference when compared to 0 gLand 15 gL NaCl We can conclude that 20 gL NaCl have anegative effect on the growth of strain Y31 and the productionof Enterocin Y31 When the adding concentration of NaClwas 5 gL the ODmax (16 h) of E faecium Y31 was highest

150

155

160

165

170

175

180

Enterocin Y31 production (AUmg protein)

CDM

(con

trol)

bc c

bc

ab

a

b b bab

a

GR

(16B

)

ODmax (16 B)

10A

L N

aCl

15A

L N

aCl

20A

L N

aCl

5A

L N

aCl 0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 2 Effect of NaCl concentration on the growth of Enterococ-cus faecium Y31 and Enterocin Y31 production Means not sharing acommon superscript letter are significantly different fromeach other(119875 lt 005)

172 plusmn 001 and the antibacterial activity also reached themaximum value 128364 plusmn 4140AUmg protein Based thesignificant difference analysis we could conclude that 5 gLNaCl stimulated the growth of strain Y31 (119875 lt 005) andhad no effect on the production of Enterocin Y31 (Figure 2)Similar results have been reported in a study of nutritionalrequirements of L salivarius CRL 1328 producing Salivaricin[19] Considering that the condition for the growth of Efaecium Y31 was crucial 5 gL NaCl was added to the novelchemically defined medium SDM (the medium ingredientsof SDM were listed in Table 1)

33 Effect of CaCl2 and Glycerol on the Growth of E faeciumY31 and Enterocin Y31 Production The results shown inTable 2 indicated that adding 10 gL CaCl

2to CDM had no

effect on the growth of E faecium Y31 but had a negativeeffect on the production of Enterocin Y31 (119875 lt 005) whereasadding 50 gL glycerol had a slight negative effect on thegrowth of E faecium Y31 (119875 lt 005) and a negative influenceon Enterocin Y31 production (119875 lt 005)

34 Effect of Individually Omitting Each Amino Acid BVitamin Mineral and Nucleic Acid Base on the Growth of Efaecium Y31 and Enterocin Y31 Production According to theLeaveOneOut (LOO) technique each amino acid B vitaminmineral and nucleic acid base was sequentially omitted ina series of prepared formulations along with CDM as acontrol The results shown in Table 3 indicated that L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser and L-Cys areessential amino acids which had an effect on the growth ofE faecium Y31 and Enterocin Y31 production and the stim-ulatory amino acids mainly included L-Asn L-Glu L-Iso L-Lys and L-Try Omitting the stimulatory amino acids resultedin the slow growth of E faecium Y31 and low production

Journal of Food Quality 5

Table 2 Effects of CaCl2and glycerol on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Added components ODmax (600 nm) after 16 h Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003b 124224 plusmn 4141c

10 gL CaCl2

170 plusmn 002b 28986 plusmn 4141a

50 gL glycerol 153 plusmn 003a 56591 plusmn 4181b

Note CDM is explained in Table 1 and means in the same row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

Table 3 Effect of omitting a single amino acid on the growth of Enterococcus faecium Y31 and Enterocin Y31 production

Omitted amino acid ODmax (16 h) Relative growth rate Enterocin Y31 production (AUmg protein)None (CDM) 169 plusmn 003h 100 124224 plusmn 4141cd

L-Ala 150 plusmn 005g 90 122843 plusmn 6325cd

L-Arg 076 plusmn 002c ng mdasha

L-Asp 143 plusmn 004g 93 117322 plusmn 6325cd

L-Asn 091 plusmn 003d 60 122843 plusmn 8225cd

L-Cys 100 plusmn 004de 44 mdasha

L-Glu 152 plusmn 004g 72 110420 plusmn 2391c

L-Gln 171 plusmn 004h 84 124224 plusmn 5686d

L-Gly 061 plusmn 003ab ng mdasha

L-His 066 plusmn 003bc ng mdasha

L-Iso 106 plusmn 004ef 79 66252 plusmn 8251b

L-Leu 071 plusmn 003bc ng mdasha

L-Lys 116 plusmn 004f 80 62111 plusmn 4140b

L-Met 053 plusmn 002a ng mdasha

L-Phe 077 plusmn 002c ng mdasha

L-Pro 181 plusmn 003h 71 110420 plusmn 6545cd

L-Ser 049 plusmn 003a ng mdasha

L-Thr 068 plusmn 002bc ng mdasha

L-Try 112 plusmn 003ef 80 57322 plusmn 2391b

L-Tyr 170 plusmn 007h 100 120082 plusmn 3487cd

L-Val 196 plusmn 008i 98 122843 plusmn 6582cd

Note ldquongrdquo represents that the strain did not grow and ldquomdashrdquo represents that there was no inhibition activity CDM is explained in Table 1 and means in thesame row not sharing a common superscript letter are significantly different from each other (119875 lt 005)

of Enterocin Y31 Therefore the essential amino acids andstimulatory amino acids were included in the SDM (listedin Table 1) A previous study reported the similar results asZhang et al found that six amino acids (arginine histidineisoleucine leucine methionine and valine) were necessaryfor the lactococci enterococci and streptococci [20]

Pyridoxal and pantothenic acid are essential B vitaminswhich had an effect on the growth of E faeciumY31 and Ente-rocin Y31 production and the stimulatory B vitamins mainlyincluded niacin and riboflavin Wherein the stimulatory Bvitamins could not result in the growth arrest of E faeciumY31 and the biosynthesis arrest of Enterocin Y31 they couldcause low growth rate and low biosynthesis volume There-fore the essential and stimulatory B vitamins were neededin the SDM Omitting folic acid would cause a reduction of80 in the ODmax (16 h) of E faecium Y31 therefore folicacid is also needed for the growth of E faecium Y31 and theproduction of Enterocin Y31 (Figure 3) It has been reported

that nutritional requirements of L delbrueckii ssp lactis CRL581 growthwere nicotinic acid and pyridoxal and pantothenicacid whereas the growth of L delbrueckii ssp lactis CRL654 requires niacin and pantothenic acid and riboflavinand cyanocobalamin were found to be stimulatory for bothstrains [21] Research results about S thermophilus strains(ST1 ST7 ST8 ST11 ST18 and ST21) indicated that riboflavinwas essential for the growth of all strains whereas Ca-pantothenic acid and nicotinic acid were also required [22]

In the present study MgSO4sdot7H2O was an essential min-

eral andMnSO4sdot4H2OKH

2PO4 K

2HPO4 andCH

3COONa

were stimulatory minerals which had an effect on the growthof E faecium Y31 and Enterocin Y31 production (Figure 4)The necessity of magnesium and phosphate has previouslybeen reported by other researchers for various LAB species[20 23 24]

Adenine and uracil are stimulatory nucleic acids whichhad an effect on the growth of E faecium Y31 and Enterocin

6 Journal of Food Quality

Non

e (CD

M)

Pyrid

oxal

Thia

min

e

Nia

cin

D-B

iotin

Ribo

flavi

n

Cyan

ocob

alam

in

Folic

acid

p-A

min

oben

zoic

acid

Pant

othe

nic a

cid

02040608101214161820

Omitted vitamins

f

b

f

c

f

d

e ef

a

d

b

d

b

ccd

cdcd

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

(AU

mg

prot

ein)

Figure 3 Effect of individually omitting each B vitamin on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Y31 production (Figure 5) No nucleic acid was essential forthe growth of E faecium Y31 and Enterocin Y31 production

35 Comparison of Enterocin Y31 Production onMRSMediumand SDM A novel chemical defined medium (SDM) wasdeveloped (Table 1 and Figures 3 4 and 5) and SDMcontainedNaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-Thr L-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

and uracil Strain Y31 grew better on SDM than on MRSmedium (Figure 6) As shown in Figure 7 Enterocin Y31production on SDM was 16 times than that on MRS

36 Purification and Characterization of Enterocin Y31 Afterthe removal of cells from the defined medium the cell-free supernatant was subjected to ultrafiltration through a30 kDa ultrafiltration membrane The active permeate liquorwas then subjected to a second ultrafiltration step using a1 kDa NMWL The antimicrobial activity was again foundin the retentate (10240AUL) Enterocin Y31 was purified byTricine-SDS-PAGE and its molecular weight was 674 kDa(showed in Figure 8)

4 Conclusion

When culturing E faecium Y31 using novel chemical definedmedium (SDM) Enterocin Y31 production increased 16times than that on MRS The ingredients were composedof NaCl L-Arg L-Gly L-His L-Leu L-Met L-Phe L-ThrL-Ser L-Cys L-Asn L-Glu L-Iso L-Lys L-Try pyridoxalpantothenic acid niacin riboflavin folic acid MgSO

4sdot7H2O

Non

e (CD

M)

Am

mon

ium

citr

ate d

ibas

ic

MnS

O4 middot 4

H2O

MgS

O4 middot 7

H2O

KH2P

O4

K2H

PO4

Sodi

um ac

etat

e

0204060810121416182022

Omitted minerals

d d

b

a

b

c ce e

b

a

c

d d

Enterocin Y31 production (AUmg protein)$

GR

(16B

)$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

Ente

roci

n Y3

1 pr

oduc

tion

Figure 4 Effect of individually omitting each a mineral on thegrowth of Enterococcus faecium Y31 and Enterocin Y31 productionMeans not sharing a common superscript letter are significantlydifferent from each other (119875 lt 005)

Non

e (CD

M)

Aden

ine

Gua

nine

Inos

ine

Xant

hine

Oro

tic ac

id

Ura

cil

Thym

ine

14

15

16

17

18

19

20

Omitted nucleic acid bases

d

a

c

d d d

b

d

d

abbc

d d d

a

cd

Enterocin Y31 production (AUmg protein)

GR

(16B

)

$GR (16 B)

(AU

mg

prot

ein)

0

200

400

600

800

1000

1200

1400

1600

Ente

roci

n Y3

1 pr

oduc

tion

Figure 5 Effect of individually omitting each a nucleic acid baseon the growth of Enterococcus faecium Y31 and Enterocin Y31production Means not sharing a common superscript letter aresignificantly different from each other (119875 lt 005)

MnSO4sdot4H2O KH

2PO4 K2HPO4 CH3COONa adenine

uracil and glucose which were the macro- and micronu-trients needed by biosynthesis of Enterocin Y31 SDM washelpful to the growth of E faecium Y31 and EnterocinY31 production improvement In addition SDM avoided aseries of chromatography steps and the loss of Enterocin Y31

Journal of Food Quality 7

0 5 10 15 20 25 30 3500020406081012141618202224

Time (h)

SDMMRS

GR

(16B

)

Figure 6 Growth of Enterococcus faecium Y31 on MRS and SDM

0 5 10 15 20 25 30 3502468

10121416182022

Time (h)

Inhi

bitio

n zo

ne d

iam

eter

(mm

)

SDMMRS

Figure 7 Enterocin Y31 productions on MRS and SDM

Enterocin Y31

M 140 +$

30+$

20 +$

10 +$

46 +$

17 +$

Figure 8 Tricine-SDS-PAGE of Enterocin Y31 M protein marker1 Enterocin Y31

activity only two steps of ultrafiltration and Tricine-SDS-PAGE were needed to separate and purify Enterocin Y31Therefore chemically defined medium has better potentialfor improving the bacteriocin production and reducing thesteps of separation and purification Chemically definedmedia is useful for purification of not only large bacteriocinssuch as Enterocin Y31 but also small peptide bacteriocinsThe alternative use of a chemically defined medium meetsthe nutritional requirements of strains producing bacteri-ocins and therefore is an excellent alternative to reduce theload of contaminating peptides from the medium therebydecreasing the purification steps To our knowledge no suchstudies have been conducted to improve class IIa bacteriocinEnterocin Y31 production and purify Enterocin Y31

Ethical Approval

This study complies with the research ethics guidelines and itdoes not contain any studies with human or animal subjects

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this article

Acknowledgments

This work was financially supported by the 60th Finan-cial Grant from China Postdoctoral Science Foundation(Grant no 2016M602534) the Youth Innovation TalentsProject of General Higher School in Guangdong Province(2016KQNCX144) and theNationalNatural Science Founda-tion of China (Grants nos 31571850 31771988 and 31701621)

References

[1] R C R Martinez M Wachsman N I Torres J G LeBlancS D Todorov and B D G D M Franco ldquoBiochemical anti-microbial and molecular characterization of a noncytotoxicbacteriocin produced by Lactobacillus plantarum ST71KSrdquo FoodMicrobiology vol 34 no 2 pp 376ndash381 2013

[2] I M Aasen T Moslashretroslash T Katla L Axelsson and I StorroslashldquoInfluence of complex nutrients temperature and pH on bacte-riocin production by Lactobacillus sakei CCUG 42687rdquo AppliedMicrobiology andBiotechnology vol 53 no 2 pp 159ndash166 2000

[3] P Alvarez-Sieiro M Montalban-Lopez D Mu and O PKuipers ldquoBacteriocins of lactic acid bacteria extending thefamilyrdquo Applied microbiology and biotechnology vol 100 no 7pp 2939ndash2951 2016

[4] F A C Martinez E M Balciunas A Converti P D Cotterand R P De Souza Oliveira ldquoBacteriocin production by Bifido-bacterium spp A reviewrdquo Biotechnology Advances vol 31 no 4pp 482ndash488 2013

[5] E F OrsquoShea P D Cotter R P Ross and C Hill ldquoStrategiesto improve the bacteriocin protection provided by lactic acidbacteriardquo Current Opinion in Biotechnology vol 24 no 2 pp130ndash134 2013

[6] A-M Zouhir E Kheadr I Tahiri J Ben Hamida and IFliss ldquoCombination with plant extracts improves the inhibitoryaction of divergicin m35 against Listeria monocytogenesrdquo Jour-nal of Food Quality vol 31 no 1 pp 13ndash33 2008

8 Journal of Food Quality

[7] J Pei Y Yuan and T Yue ldquoPrimary characterization of bacteri-ocin paracin C - A novel bacteriocin produced by Lactobacillusparacaseirdquo Food Control vol 34 no 1 pp 168ndash176 2013

[8] D Drider and S Rebuffat ldquoClassification of Bacteriocins fromGram-Positive Bacteriardquo in Prokaryotic Antimicrobial Peptidespp 29ndash53 Springer New York NY USA 2011

[9] T Aymerich H Holo L S Havarstein M Hugas M Garrigaand I F Nes ldquoBiochemical and genetic characterization of ente-rocin A from Enterococcus faecium a new antilisterial bac-teriocin in the pediocin family of bacteriocinsrdquo Applied andEnvironmental Microbiology vol 62 no 5 pp 1676ndash1682 1996

[10] W Liu L Zhang H Yi et al ldquoQualitative detection of class IIabacteriocinogenic lactic acid bacteria from traditional Chinesefermented food using a YGNGV-motif-based assayrdquo Journal ofMicrobiological Methods vol 100 no 1 pp 121ndash127 2014

[11] W Liu L Zhang J Shi et al ldquoAssessment of the safety and appli-cations of bacteriocinogenic Enterococcus faecium Y31 as anadjunct culture in North-eastern Chinese traditional fermen-tation paocairdquo Food Control vol 50 pp 637ndash644 2015

[12] H Khan S H Flint and P-L Yu ldquoDevelopment of a chemicallydefined medium for the production of enterolysin A fromEnterococcus faecalis B9510rdquo Journal of Applied Microbiologyvol 114 no 4 pp 1092ndash1102 2013

[13] M Silva d M Andrade d S A Bauermeister et al ldquoA SimpleDefined Medium for the Production of True Diketopiperazinesin Xylella Fastidiosa and Their Identification by Ultra-FastLiquidChromatography-Electrospray Ionization IonTrapMassSpectrometryrdquoMolecules vol 22 no 6 p 985 2017

[14] E Texeira J Checa A Rıal et al ldquoA New Chemically DefinedMedium for Cultivation of Streptococcus Pneumoniae SerotyperdquoJournal of Biotech Research vol 6 p 54 2015

[15] A Ricciardi R G Ianniello E Parente and T Zotta ldquoModifiedchemically definedmedium for enhanced respiratory growth ofLactobacillus casei and Lactobacillus plantarum groupsrdquo Journalof Applied Microbiology vol 119 no 3 pp 776ndash785 2015

[16] U Schillinger and K Lucke F ldquoAntibacterial activity of Lacto-bacillus sake isolated from meatrdquo Applied and EnvironmentalMicrobiology vol 55 no 8 pp 1901ndash1906 1989

[17] P K Smith R I Krohn G Hermanson et al ldquoMeasurement ofprotein using bicinchoninic acidrdquo Analytical biochemistry vol150 no 1 pp 76ndash85 1985

[18] J Monod ldquoThe Growth of Bacterial Culturesrdquo Annual Reviewsin Microbiology vol 3 no 1 pp 371ndash394 1949

[19] E V Pingitore EMHebert F Sesma andM E Nader-MacıasldquoInfluence of vitamins and osmolites on growth and bacteriocinproduction by Lactobacillus salivarius CRL 1328 in a chemicallydefinedmediumrdquoCanadian Journal of Microbiology vol 55 no3 pp 304ndash310 2009

[20] G Zhang D AMills and D E Block ldquoDevelopment of chemi-cally defined media supporting high-cell-density growth ofLactococci Enterococci and Streptococcirdquo Applied and Environ-mental Microbiology vol 75 no 4 pp 1080ndash1087 2009

[21] E M Hebert R R Raya and G S De Giori ldquoNutritionalrequirements of Lactobacillus delbrueckii subsp lactis in achemically defined mediumrdquo Current Microbiology vol 49 no5 pp 341ndash345 2004

[22] C Letort and V Juillard ldquoDevelopment of a minimal chemi-cally-defined medium for the exponential growth of Streptococ-cus thermophilusrdquo Journal of AppliedMicrobiology vol 91 no 6pp 1023ndash1029 2001

[23] N Terrade and R Mira de Orduna ldquoDetermination of theessential nutrient requirements of wine-related bacteria fromthe genera Oenococcus and Lactobacillusrdquo International Journalof Food Microbiology vol 133 no 1-2 pp 8ndash13 2009

[24] F M Saguir and M C M De Nadra ldquoImprovement of a chem-ically definedmedium for the sustained growth of Lactobacillusplantarum nutritional requirementsrdquo Current Microbiologyvol 54 no 6 pp 414ndash418 2007

Research ArticleLipid Oxidation Color Changes and MicrobiologicalQuality of Frozen Beef Burgers Incorporated with ShiraziThyme Cinnamon and Rosemary Extracts

Hadi Hashemi Gahruie Seyed Mohammad HashemHosseiniMohammad Hossein Taghavifard Mohammad Hadi EskandariMohammad-Taghi Golmakani and Ehsan Shad

Department of Food Science and Technology School of Agriculture Shiraz University Shiraz Iran

Correspondence should be addressed to Mohammad Hadi Eskandari eskandarshirazuacir

Received 3 January 2017 Revised 17 March 2017 Accepted 11 April 2017 Published 21 May 2017

Academic Editor Moreno Bondi

Copyright copy 2017 Hadi Hashemi Gahruie et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In this study the oxidative stability of beef burgers incorporated with Shirazi thyme cinnamon and rosemary extracts wascompared with that of BHT-incorporated and antioxidant-free samples The chemical composition TBARS metmyoglobin pHcolor and microbial and sensory characteristics were evaluated during storage at minus18∘C for 2 months The results indicated thatShirazi thyme and cinnamon extracts did not change the colorimetric properties significantly (119875 lt 005) Incorporating naturalantioxidants led to a significant (119875 lt 005) reduction in TBARS (3658ndash4634) and metmyoglobin (1625ndash1847) as compared tocontrol Except for the control sample total microbial counts of burgers were lower than the maximum allowed limit Burgersformulated with Shirazi thyme revealed the lowest amount of total count Regarding the sensory characteristics the overallacceptability of different samples decreased in the order of cinnamon gt BHT gt Shirazi thyme gt rosemary gt control Finally theresults showed that these plant extracts can be utilized as an alternative to synthetic antioxidants in formulation of burgers

1 Introduction

Meat and meat products are among the most importantprotein sources in the daily diet of people living in developedcountries Beef burger is almost the most popular meatproduct consumed by millions of people from all over theworld The common processes (such as mincing cookingand salt addition) applied in the production of burgersenhance the formation of reactive oxygen species thereforethe resultant product is highly vulnerable to oxidation [1]Lipid and protein oxidations have been reported as theprincipal reason for the decreased quality of burgers duringstorage resulting in decreasing the shelf life [2ndash4]

Application of antioxidants is the best strategy to pre-vent oxidation reactions [5] Synthetic antioxidants such asBHT TBHQ and BHA have various adverse human healtheffects including allergy headache asthma and dermatitis

Therefore the application of natural antioxidants (such asherbal essential oils and extracts) is of interest and canbe observed in a growing number of research works [6ndash8](Aliakbarlu et al 2016)Moreover consumers are increasinglydemanding for green-labeled food products such as thosecontaining natural antioxidant Natural compounds can beobtained from natural sources such as plants fruits vegeta-bles oil seeds spices team honey bee pollen and cereals[9] A lot of extracts have been approved as GRAS (GenerallyRecognized as Safe) that is the addition of these chemicals orsubstances into food is considered safe by experts and theirapplication is exempted from the usual Federal Food Drugand Cosmetic Act (FFDCA) [10]

The potential of natural antioxidants in preventing thelipid oxidation in different food products has been evaluatedby many researchers around the world [11] It has beenreported that the extracts of kinnow rind pomegranate rind

HindawiJournal of Food QualityVolume 2017 Article ID 6350156 9 pageshttpsdoiorg10115520176350156

2 Journal of Food Quality

Hamburger ingredients Extracts (20 g herb + 500 ml water)

Preparation of base batter

Formula 1without additives

(control)

Formula 2with BHT(100 ppm)

Formula 3with Shirazi thyme

(22 mlkg)

Formula 4with rosemary

(28 mlkg)

Formula 5with cinnamon

(73 mlkg)

Analysis (0 15 30 45 and 60 days)

Chemical analysis

Chemical compotation(i) Moisture

(ii) Protein(iii) Fat(iv) Carbohydrate(v) Ash

Deterioration criteria(i) TBARS

(ii) pH(iii) Metmyoglobin

Microbiological analysis(i) Total aerobic bacterial count

Sensory analysis(i) Appearance

(ii) Texture(iii) Taste(iv) Odor(v) Overall acceptance

Color analysis(i) Llowast

(ii) alowast

(iii) blowast

(iv) ΔE

Production and storage at minus18∘C

Figure 1 Schematic diagram of experimental design

and seed powders were significantly able to decrease the lipidoxidation in goat meat patties [12] The effects of natural(sage and rosemary) and synthetic (BHT) antioxidants onprotein oxidation discoloration and texture of refrigeratedpatties produced from pig liver have been studied by Estevezet al [13] Authors reported that the antioxidant propertiesof natural and synthetic antioxidants were similar In treatedsamples the increase in the carbonyl content as a result ofoxidation was significantly (P lt 005) lower than controlsamples Moreover antioxidants could successfully protectheme molecules from degradation Among different naturalantioxidants it has been reported that the extracts of Shirazithyme cinnamon and rosemary reveal substantial antioxi-dant capacity [14]

The main objective of the current study was to comparethe effects of Shirazi thyme cinnamon and rosemary extracts(denoted as natural antioxidants) with those of BHT on pro-tein and lipid oxidations and physicochemicalmicrobial andsensory characteristics of frozen beef burgers during storageThe results of this study may have potential implications

in substituting the synthetic antioxidants with nature-madeones

2 Materials and Methods

A schematic representation of beef burger production isshown in Figure 1

21 Materials Beef flanks (18 fat) from freshly slaughteredanimals (24 hours post slaughter)were purchased froma localmarket (Shiraz Iran) and transported to the laboratory ininsulated polystyrene ice-boxes The meat was ground (MeatGrinder Philips HR2743 AmsterdamNetherlands) througha perforated plate with a hole diameter of 5mm Thiobar-bituric acid (Sigma-Aldrich St Louis MO USA) 1133-tetraethoxypropane (Sigma-Aldrich St Louis MO USA)and diphenyl-2-picrylhydrazyl (DPPH∙) (Sigma-Aldrich StLouisMOUSA) soy protein isolate (SPI 90 protein SonicCo India) onions salt spices and ruskwere also used in thisstudy

Journal of Food Quality 3

22 Plant Extracts Shirazi thyme (Zatariamultiflora) cinna-mon (Cinnamomum zeylanicum) and rosemary (Rosmarinusofficinalis) were purchased from a local grocery The genusand species were certified by experts from the Herbariumof Biology Department (Shiraz University Shiraz Iran)Dried plants were powdered with a mill and then kept inpolyethylene bags at room temperature before extraction

221 Extract Preparation Plant powder (20 g) was thor-oughly mixed with boiling distilled water (500mL) for5min followed by filtration through Whatman grade No 1filter papers and concentration in rotary evaporator (BuchiRotavapor R Switzerland) at 50∘C [15]

222 DPPH Radical Scavenging Activity Antioxidant activ-ity of natural extracts and BHT was calculated using DPPHfree radicalmethod described by Cam et al [16]The amountsof extracts required to replace BHT were calculated basedon the IC50 of BHTThe required amounts of natural extractsshould have equal antioxidant activity to BHT

23 Beef Burger

231 Burger Preparation and Storage The formulation ofbeef burger used in this study was composed of beef (70)onions (134) rusk (4) water (8) SPI (3) salt (1)black (03) and red (02) peppers Ground meat saltwater and minced onion were mixed together After thatSPI was added and then mixed for 15min to obtain ahomogenousmixture Rusk and spices were added in the nextstep Finally natural extracts andor BHT were incorporatedinto the homogenate and thenmixing process was continuedThe concentration of BHT was 100 ppm A burger maker(9 cm internal diameter) was used to shape the mixture intopatties of approximately 90 g and 5mm thickness Burgers(15 patties per treatment) were then packed in light-resistantpolyethylene containers and frozen at minus18∘C Analyses wereperformed during 15-day intervals for two months Beforeanalysis the samples were thawed at +4∘C and then hand-mixed for 30 s

232 Chemical Analysis Moisture protein fat and ashcontents of burgers were determined according to the AOACmethods [17] Carbohydrate content was estimated by sub-tracting the total amounts of moisture protein fat and ashfrom 100

233 pH Measurement Meat sample (10 g) was homog-enized with 50mL deionized water for 1min pH wasmeasured at room temperature using a digital pH meter(Suntex TS-1 Taiwan) equipped with a probe-type combinedelectrode (Ingold) through direct immersion of electrode intothe mixture [17]

234 Instrumental Color Evaluation Color attributes of beefburgers were measured by 119871lowast119886lowast119887lowast method described byYam and Papadakis [18] The values of 119871lowast (brightness) 119886lowast(redness-greenness) and 119887lowast (yellowness-blueness) weremea-sured on the whole outer surfaces of beef burger A wooden

box (50 times 50 times 60 cm3) equipped with a natural daylightsource (6500K) and a digital camera (CanonPowershotA540of six megapixels resolution) in a vertical position and adistance of 25 cm from the samples was used for takingphotos Adobe PhotoshopCS6 was applied to determine theaverage surface color

235 Determination of Lipid Oxidation Lipid oxidationwas monitored by measuring thiobarbituric acid reactivesubstances (TBARS) Meat sample (4 g) was homogenizedwith 20mL trichloroacetic acid solution (20 wv) and thencentrifuged at 3000119892 for 10min The supernatant (2mL) wasmixed with 2mL thiobarbituric acid solution (01 wv indouble distillated water) followed by heating in a water bathat 100∘C for 30min and then cooling to room temperatureTherefore TBARS were extracted in chilled atmosphere Theabsorbance of each extract was measured at 520 nm in aspectrophotometer (spec 1650PC Shimadzu Japan) 1133-tetraethoxypropane was used to develop the standard curvefor TBARS assay TBARS values were reported as mg ofmalonaldehyde per kg of beef burger [7]

236 Metmyoglobin Measurement A modified method ofAn et al [19] was used to measure the metmyoglobincontent in raw beef burgers The sample (4 g) was mixedin a homogenizer with 20mL of phosphate buffer (004MpH 68) and then stored at 1∘C for 1 h The mixture wasthen centrifuged at 3500119892 and 4∘C for 30min Finally thesupernatant was filtered through Whatman grade No 1filter paper The absorbance of the solution was measuredat 525 572 and 700 nm Metmyoglobin () was calculatedaccording to the following equation

Metmyoglobin () = [1395 minus [(119860572 minus 119860700)(119860525 minus 119860700)]]times 100

(1)

Total Aerobic Bacterial Count Total aerobic bacteria werequantified every 15 days using the method described byAliakbarlu et al (2016) Beef burgers (10 g) were asepti-cally transferred into individual stomaching bags containing90mL of sterile saline (09) and homogenized for 2minSerial 10-fold dilutions were prepared in saline and 100 120583Lfrom appropriate dilutions was spread on the surface of platecount agar for total aerobic count (TMC) and then incubatedat 35∘C for 24 h

237 Sensory Evaluation Sensory analyses have been per-formed by 20 trained panelists from the Department of FoodScience and Technology (Shiraz University) Panelists wereboth male and female in the age range of 23ndash28 years oldPanelists were selected based on their previous experiences inconsuming traditional beef burgers Moreover they receivea preparatory session before the sensory test to train themhow to describe all evaluated factors completely Burgers werefried at 150∘C in a forced draft oven to a core temperatureof 72∘C and kept warm in the oven for 3ndash8min until thesensory testing [20] Rectangular pieces of approximately

4 Journal of Food Quality

2 cm were cut from the center of each burger and then servedat room temperature Each panelist randomly evaluated threepieces of all formulations and asked to give a numericalvalue between 1 and 9 for the following attributes taste 1(imperceptible) to 9 (extremely intense) texture attributesand juiciness 1 (extremely dry) to 9 (extremely moist)appearance 1 (extremely soft) to 9 (extremely tough) andodor 1 (imperceptible) to 9 (extremely intense) Tap waterwas provided for panelists to rinse their mouth betweendifferent samples At the end of evaluation each panelist wasasked to give an overall score from 1 (dislike very much) to9 (like very much) for the overall acceptability of differentformulations

24 Statistical Analysis A completely randomized blockdesign with five treatments (including antioxidant-free (con-trol) treatment and those incorporated with BHT cinnamonrosemary and Shirazi thyme extracts) was used in this studyExperiments were performed during a 60-day storage periodat 15-day intervals (0 15 30 45 and 60) Independent blocks(developed from three different batches) were replicatedthree times at each sampling point A two-way analysisof variance (ANOVA) and Duncanrsquos multiple range tests(SAS 80 software SAS Institute Inc Cary NC USA) wereperformed to analyze the effect of treatments storage periodand their interaction on the physicochemical microbial andsensory characteristics of beef burgers at a confidence levelof 005 In the analysis models the treatments storage timesand their interaction were assigned as fixed effects and thereplications as random effects

The given scores of different sensory attributes werecompared between the treatments using general linear model(GLM) Duncanrsquos multiple range tests were used for compar-ison of means at a confidence level of 005 Treatments andassessors were considered as main effects and the replicationsas random effects Data was reported as mean plusmn standarderror (SE)

3 Results and Discussion

31 Antioxidant Activity of Extracts The IC50 values (definedas the concentration of an antioxidant required to reduce theinitial DPPH concentration by 50 using DPPH free radicalmethod described by Cam et al [16]) of natural extracts(including Shirazi thyme cinnamon and rosemary) andsynthetic BHT were 0022 0373 0062 and 0107mgmLrespectively Therefore the amounts of Shirazi thyme cinna-mon and rosemary concentrated extracts required to replace100 ppm BHT in formulation were 22 73 and 28mL per kgof beef burger respectively Cinnamon is a source of bioactivecompounds such as cinnamaldehyde eugenol and coumarin[21] The effect of cinnamon extract as direct scavengersof free radicals has been studied by Roussel et al [22]Carnosic acid and carnosol are the main bioactive com-pounds present in the rosemary extract [23] According toSharififar et al [24] the major chemical compounds presentin Shirazi thyme were carvacrol (3365) thymol (3759) p-cymene (772) 120574-terpinene (388) and 120573-caryophyllene(206)

40

45

50

55

60

65

70

75

80

Met

myo

glob

in (

)

15 30 45 600Storage period (days)

ControlBHTCinnamon extract

Rosemary extractShirazi thyme extract

Figure 2 Effect of incorporating Shirazi thyme cinnamon androsemary extracts on the metmyoglobin () developed in raw beefburgers during frozen storage at minus18∘C

32 Physicochemical Properties of Beef Burger The resultsindicated that the samples contained 5913 moisture 19protein 12 fat 772 carbohydrate and 2 ash

33 Color Stability When assessing meat a consumer paysa great attention to its color which as a visual impressionis induced mainly by the presence of pigments but it alsodepends on tissue composition and meat structure Hencethe color of fresh meat is an important quality parameterthat determines a consumerrsquos response and decision to buyor not to buy that product at retail Changes in 119871lowast 119886lowast and119887lowast values of beef burgers during frozen storage are shown inTable 1 No significant difference (119875 gt 005) was observedbetween the samples incorporated with natural antioxidantsand those incorporated with BHT at production time (day 0)resulting in low Δ119864 values at early stages of storage All of theformulations showed significant decrease in 119886lowast during frozenstorage Formulation incorporated with rosemary extractshowed lower amounts of 119886lowast at the end of storage timeThe significant decrease in 119886lowast values indicated the red colorreduction of products during storage this is despite the factthat BHT- and extract-incorporated treatment significantlyreduced the Met-mb development ratio in comparison tocontrol one (Figure 2) During the first 30 days of storage119871lowast values increased significantly (119875 lt 005) then remainedconstant During frozen storage changes in the amountsof 119871lowast in cinnamon- (642) or Shirazi thyme-incorporatedsamples (597) were less than those in other formulationsSamples incorporated with rosemary extract showed the leastredness (433)

A significant decrease in 119886lowast values of raw pork pat-ties containing grape seed extract and bearberry has beenreported over a 12-day storage by Carpenter et al [25]however 119887lowast values (particularly of control samples) increasedsignificantly (119875 lt 005) Similarly Nunez de Gonzalez et al[26] reported that 119886lowast value of beefs stored under refrigeration

Journal of Food Quality 5

Table 1 Effect of addition of Shirazi thyme cinnamon and rosemary extracts and BHT on 119871lowast 119886lowast 119887lowastand Δ119864 values of raw beef burgersduring frozen storage at minus18∘CParameter Sample Storage period (days)

0 15 30 45 60

119871lowastControl 6033 plusmn 088 glowastlowast 5800 plusmn 058 hi 7133 plusmn 034 abc 7167 plusmn 034 ab 7267 plusmn 067 aBHT 5867 plusmn 088 ghi 5733 plusmn 034 i 6833 plusmn 034 de 6933 plusmn 034 cd 7067 plusmn 067 abc

Cinnamon extract 6033 plusmn 067 g 5433 plusmn 034 j 5967 plusmn 067 gh 6533 plusmn 067 f 6800 plusmn 058 deRosemary extract 5733 plusmn 034 i 5433 plusmn 082 i 6967 plusmn 088 bcd 7133 plusmn 088 abc 7167 plusmn 034 ab

Shirazi thyme extract 5733 plusmn 146 i 5667 plusmn 067 i 5700 plusmn 058 i 6700 plusmn 058 ef 6833 plusmn 067 de

119886lowastControl 1133 plusmn 034 a 833 plusmn 034 de 833 plusmn 034 de 767 plusmn 034 ef 667 plusmn 034 fghBHT 1100 plusmn 058 ab 667 plusmn 034 fgh 767 plusmn 067 ef 700 plusmn 058 fg 667 plusmn 034 fgh

Cinnamon extract 933 plusmn 034 cd 733 plusmn 034 efg 667 plusmn 034 fgh 567 plusmn 034 hij 533 plusmn 034 ijkRosemary extract 1167 plusmn 034 a 533 plusmn 034 ijk 533 plusmn 034 ijk 467 plusmn 034 jk 433 plusmn 034 k

Shirazi thyme extract 1000 plusmn 058 667 plusmn 034 fgh 633 plusmn 034 ghi 567 plusmn 034 hij 533 plusmn 034 ijk

119887lowastControl 2333 plusmn 034 kl 2500 plusmn 058 ij 3233 plusmn 034 bc 3267 plusmn 067 b 3400 plusmn 058 aBHT 2233 plusmn 034 lmn 2333 plusmn 034 kl 3100 plusmn 058 cd 3133 plusmn 067 bcd 3167 plusmn 067 bcd

Cinnamon extract 2167 plusmn 034 mno 2267 plusmn 034 lm 2533 plusmn 034 ij 2600 plusmn 058 i 2767 plusmn 034 hRosemary extract 2033 plusmn 0340 2100 plusmn 058 no 2900 plusmn 058 fgh 3067 plusmn 034 de 3133 plusmn 067 bcd

Shirazi thyme extract 2300 plusmn 000 klm 2433 plusmn 034 jk 2833 plusmn 034 gh 2933 plusmn 034 efg 3033 plusmn 034 def

Δ119864lowastlowastlowastControl 000 plusmn 000 f 1700 plusmn 025 aBHT 272 plusmn 069 e 1409 plusmn 018 bc

Cinnamon extract 282 plusmn 072 e 1078 plusmn 095 dRosemary extract 442 plusmn 104 e 1559 plusmn 102 ab

Shirazi thyme extract 354 plusmn 030 e 1229 plusmn 080 cdlowastlowastData represent averages of three independent repeats plusmn standard errorslowastlowastMeans with different letters are significantly different (119875 le 005)lowastlowastlowastFor each storage time the color difference (Δ119864) was calculated by comparing the color attributes of different formulations with those of control sample

for 10 weeks decreased significantly (119875 lt 005) The resultsof the current study showed that high antioxidant activity ofnatural extracts can be potentially used to develop naturalcolor stabilizers particularly for controlling 119871lowast and 119887lowast valuesin frozen beef burger

As mentioned already samples incorporated with BHTand natural extracts did not show any significant differencein Δ119864 value at the beginning of the storage time However atthe end of storage the lowest and highest changes in Δ119864wereobserved in cinnamon-incorporated and control samplesRedmeat color is an important property of visual appearanceand could influence meat purchasing decisions more thanany other quality parametersThe color of meat products andmeat is influenced by metmyoglobin percentage in muscleInitially the myoglobin was changed into oxymyoglobin(light pink color) which could result in brighter redmeat andthen oxymyoglobin was oxidized into metmyoglobin duringstorage [7]

34 Metmyoglobin Content Assay The amount of metmyo-globin has been positively linked to the extent of proteinoxidation in meat products The heme complex of heme(in) proteins consists of iron in the ferrous state (Fe+2)which turns into the ferric state (Fe+3) via a process calledautoxidation [27] The effects of natural extracts on thechanges of metmyoglobin content are shown in Figure 2Themaximum amount of metmyoglobin (7426) was measuredin antioxidant-free samples The presence of antioxidantsresulted in a significant decrease (1625ndash1847) in the

amounts of metmyoglobin developed during storage whichwas attributed to the strong antioxidant activity An etal [19] evaluated the percent metmyoglobin of the porkjerky samples incorporated with different kimchi powderconcentrations It has been reported that the metmyoglobincontents () of the samples prepared with various kimchipowder levels (ranged from 81 to 83) were significantly(119875 lt 005) lower than that of control sample (85) [19]There was no significant difference between the amounts ofmetmyoglobin under the influence of natural extracts or BHTindicating that these natural extracts can be utilized as asubstitute for BHT to prevent discoloration

The myoglobin reactions with peroxides result in theformation of lipid oxidation promoting compounds [28]The lowest amount of metmyoglobin was measured in thesamples formulated with cinnamon extract indicating thatit was more effective than the other antioxidants (eithernatural or synthetic) in preventing metmyoglobin formationA reverse relationship between the metmyoglobin level and119886lowast value was observed in this study A decrease in 119886lowast valuescorresponding to the decreased redness of lamb meat as aresult of myoglobin oxidation (metmyoglobin formation) hasbeen reported previously [29 30]

Metmyoglobin content increased during storage Thelowest increasing rate was observed in the samples incor-porated with rosemary extract The highest amount of met-myoglobin was observed in the control sample at the endof storage Changes in the metmyoglobin content of controlsample became significant after 15 days

6 Journal of Food Quality

Table 2 Thiobarbituric acid reactive substances (TBARS) values (mg malonaldehyde per kg) of beef burger during frozen storage at minus18∘CSample Storage period (days)

0 15 30 45 60Control 012 plusmn 001lowast 015 plusmn 002 020 plusmn 002 023 plusmn 001 041 plusmn 004BHT 010 plusmn 001 013 plusmn 001 015 plusmn 002 018 plusmn 001 023 plusmn 002Cinnamon extract 011 plusmn 001 013 plusmn 001 016 plusmn 001 017 plusmn 002 024 plusmn 002Rosemary extract 011 plusmn 001 013 plusmn 002 017 plusmn 002 019 plusmn 002 022 plusmn 002Shirazi thyme extract 012 plusmn 001 014 plusmn 002 017 plusmn 002 018 plusmn 001 026 plusmn 002lowastData represent averages of three independent repeats plusmn standard errors

35 Oxidative Stability Initiation is the step in which afatty acid radical is produced Two notable initiators inoxidative stability are OH∙ and HOO∙ which combines witha hydrogen atom to make water and a fatty acid radical Thefatty acid radical is not a very stable molecule so it reactsreadily with molecular oxygen thereby creating a peroxyl-fatty acid radical This radical is also an unstable species thatreacts with another free fatty acid producing a different fattyacid radical and a lipid peroxide or a cyclic peroxide if ithad reacted with itself This cycle continues as the new fattyacid radical reacts in the same wayThe radical reaction stopswhen two radicals react and produce a nonradical speciesThe lipid oxidation leads to produce of some componentscausing off-flavors and reduced nutritional quality such asmalondialdehyde and 4-hydroxynonenal

Thiobarbituric acid test can be used to determine thesecondary products of lipid oxidation in different foods suchas meat and its products [31] Thiobarbituric acid reactivesubstances (TBARS) values of different formulations (as afunction of storage time) are shown in Table 2 Exceptfor control sample the variations in TBARS values of theother formulations revealed a similar pattern Due to theabsence of antioxidant in formulation the observed changesin TBARS values of control were significantly (119875 lt 005)higher than others (8636 higher than rosemary) Natu-ral extracts were as effective as BHT for preventing lipidoxidation in beef burgers This observation indicated thatnatural herbal extracts are suitable replacers for syntheticantioxidant It has been reported that rosemary oleoresin(7704) and a mixture of BHT and BHA (7869) wasequally efficient in inhibiting the lipid oxidation of breakfastsausage containing 25 turkey meat [32] These findings arealso in good agreement with those of Mielnik et al [33] whoreported lower TBARS values after cooking of mechanicallydeboned turkey meat already stored in dark cold and treatedwith rosemary (8834) and grape seed extracts (8383)Sanchez-Escalante et al [34] reported that incorporatingrosemary essential oil into beef patties led to a significant(119875 lt 005) decrease (6400) in TBARS values during coldstorage The essential oil of rosemary was also effective inpreventing (7243) the rancidity of heat-treated turkeymeatproducts [35] It has also been reported that rosemary extractaddition into deboned poultry meat can protect (9820) theproduct from cooking-induced oxidation [36]

Regardless of sample type examined TBARS valuesincreased significantly during the frozen storage and reached

43

45

47

49

51

53

55

57

59

Tota

l aer

obic

bac

teria

l cou

nt (l

og cf

ug)

15 30 45 600Storage period (Days)

52

53

54

55

56

57

58

59

6

61

pH

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

ControlBHTRosemary extractCinnamon extractShirazi thyme extract

Figure 3 Total aerobic bacterial count (log cfug) (solid symbols)and pH value (open symbols) of different beef burger formulationsas a function of storage time

to a maximum amount of 041mg malonaldehyde per kg inantioxidant-free (control) sample after 60 days At TBARSvalues of 20 off-flavors are definitely detectable and themeatis considered to be unacceptable [37]

36 Changes in pH Values Changes in pH values of beefburgers during frozen storage are shown in Figure 3 Allformulations revealed relatively similar pH values just afterproduction ranging from 588 to 593 coinciding with theISIRI 2008 Mohamed and Mansour [38] similarly reportedthat no significant differences (119875 gt 005) were observed in thepH values of beef patties after incorporating natural herbalextracts

A downward pattern of different rates was observed in thepH values of all formulations during frozen storage As nomicrobial growth was expected during storage the decreasein the pH values could be attributed to the microbial growthduring thawing (by consuming sugar and producing organicacids) Control sample had the lowest pH (551) at the end ofstorage Emiroglu et al [39] reported that the pH values of

Journal of Food Quality 7

all fresh ground beef patty samples treated with thyme andoregano generally decreased after sixth day of storage (119875 gt005)

Also the result showed that to decrease pH amount oflipid oxidation and metmyoglobin significantly increasedLapidot et al (2005) evaluated lipid peroxidation of grilledred turkey muscle (Donor Kabab) as affected by pH In thisstudy they show indeed that lipid peroxidation and myo-globin of a real fast food (turkey Doner Kebab shawarma) issignificantly more rapidly oxidized at pH 30 than at pH 50

37 Microbial Growth As shown in Figure 3 total aerobicbacterial counts of antioxidants-incorporated formulationswere not significantly (119875 lt 005) different The highestamount of total count was observed in control sample(Figure 3) Shirazi thyme-incorporated beef burgers had thelowest microbial count which could be attributed to thehigh antimicrobial properties resulting from thymol and car-vacrol The antibacterial mechanism of thymol and carvacrolis the disruption of the cytoplasmic membrane which raisesits permeability and depolarizes its potential Total countof frozen raw beef burger should be lower than 6 log cfug[40] Except for the control sample the microbial counts ofbeef burgers were lower than the maximum allowed countA relatively good correlation was observed between the pHvalues and total aerobic counts For example control samplehad the lowest pH and the highestmicrobial count Rosemaryextract (1000 ppm) inhibitory effect on the microbial growthof surface-applied beef steaks has been reported by Djenaneet al [41] However Sanchez-Escalante et al [34] reportedthat rosemary did not affect the microbial counts of beefpatties during storage (3 logCFUg)

An increase in the microbial counts was observed duringstorage but not beyond the standard range As a rule ofthumb in good manufacturing and hygienic practices duringpreparation of beef burger and its related products rapidand proper storage is important for decreasing the microbialgrowth and enhancing the shelf life

Vieira et al [42] studied the effect of frozen storage condi-tions (temperature and length of storage) on microbiologicaland sensory quality of rustic crossbred beef at different statesof ageing The result showed that psychrotrophic bacteriaincreased (138 logCFUg) significantly during 90-day storage38 Sensory Properties Color flavor and texture are themostimportant sensory attributes which influence the acceptabil-ity of meat products by consumers [43] Sensory evaluationresults of cooked beef burgers are shown in Figure 4 Gener-ally incorporating Shirazi thyme cinnamon and rosemaryextracts into beef burger formulations had no significantinfluence on the sensory properties Although samples for-mulated with Shirazi thyme and cinnamon extracts with6944 and 7167 acceptability obtained the highest tastescores by panelists (119875 lt 005) The antioxidant prop-erties of natural extracts were the main reason for theincreased sensory scores of natural extract-incorporatedformulations through preventing the formation of oxidation-mediated off-flavors and off-odors (short-chain aldehydes

4

45

5

55

6

65

7Appearance

Taste

OdorTexture

Overall

ControlBHTRosemary extract

Shirazi thyme extractCinnamon extract

Figure 4 Sensory evaluation of different beef burger formulationsa 9-point descriptive scale (1 = extremely poor and 9 = highlyacceptable) was used during evaluation

and ketones) during storage Moreover the presence ofpleasant volatile constituents in natural extracts (particu-larly in cinnamon and Shirazi thyme) led to an increasedsensory score in comparison to the BHT-incorporatedformulation

A significant increase in the flavor scores of beef pattiesincorporated with antioxidant mechanically deboned poul-try meat during frozen storage was similarly reported byMohamed and Mansour [38]

4 Conclusion

This work aimed to study the possible replacement ofsynthetic antioxidant BHT with natural extracts (includingShirazi thyme cinnamon and rosemary extracts) in beefburger formulation Different samples were prepared thendifferent characteristics such as protein and lipid oxidationand physicochemical microbial and sensory properties wereevaluated during frozen storage Herbal extracts could inhibitthe lipid oxidation in formulated burgers Moreover it wasdemonstrated that natural herbal extracts were generallybetter than BHT in preventing the lipid and protein oxi-dations as well as improving the sensory attributes of beefburgersTherefore it can be concluded that natural extracts ofShirazi thyme (0022mgmL) cinnamon (0373mgmL) androsemary (0062mgmL) can be used as natural substitutesfor BHT (0107mgmL)This substitutionmay have potentialimplication for developing green-labeled meat product Infuture studies it would be informative to study the effect ofmixed extracts and their possible synergistic or antagonisticeffects in extending the shelf life of meat products

8 Journal of Food Quality

Additional Points

Practical Applications Beef burger containing natural antiox-idant is one of themost important functional food for humanconsumption attributable to its nutritional properties andhealth effects However the nutraceutical properties of thisfood have improved due to alternative BHT with extractsThe present investigation demonstrated the effects of addingvarious natural antioxidants to the beef burger so as tomonitor the changes that occur to the physicochemicalantimicrobial and sensorial properties of the beef burger

Conflicts of Interest

The authors declare that they have no conflicts of interest

Acknowledgments

This research project was financially supported by ScientificAffairs Shiraz University and Department of Food Scienceand Technology Shiraz University Shiraz Iran

References

[1] D Ladikos and V Lougovois ldquoLipid oxidation in muscle foodsa reviewrdquo Food Chemistry vol 35 no 4 pp 295ndash314 1990

[2] C JMussinan andM JMorello ldquoFlavor analysis developmentsin isolation and characterizationrdquo American Chemical Societypp 343ndash358 1998

[3] E B Ozvural QHuang andM L Chikindas ldquoThe comparisonof quality and microbiological characteristic of hamburgerpatties enriched with green tea extract using three techniquesDirect addition edible coating and encapsulationrdquo LWTmdashFoodScience and Technology vol 68 pp 385ndash390 2016

[4] G Comi E Tirloni D Andyanto M Manzano and LIacumin ldquoUse of bio-protective cultures to improve the shelf-life and the sensorial characteristics of commercial hamburg-ersrdquo LWTmdashFood Science and Technology vol 62 no 2 pp 1198ndash1202 2015

[5] F Shahidi ldquoAntioxidants in food and food antioxidantsrdquoFoodNahrung vol 44 pp 158ndash163 2000

[6] S Arabshahi-D D Vishalakshi Devi and A Urooj ldquoEvaluationof antioxidant activity of some plant extracts and their heat pHand storage stabilityrdquo Food Chemistry vol 100 no 3 pp 1100ndash1105 2007

[7] X Zhang L Deyong Q Meng C He and L Ren ldquoEffectof mulberry leaf extracts on color lipid oxidation antioxidantenzyme activities and oxidative breakdown products of rawground beef during refrigerated storagerdquo Journal of Food Qual-ity 2016

[8] H H Hashemi Gahruie M H Eskandari G Mesbahi andM A Hanifpour ldquoScientific and technical aspects of yogurtfortification a reviewrdquo Food Science and Human Wellness vol4 no 1 pp 1ndash8 2015

[9] K Yamazaki S Kawamorita H Ohmiya and M SawamuraldquoDirected ortho borylation of phenol derivatives catalyzed by asilica-supported iridium complexrdquo Organic Letters vol 12 no18 pp 3978ndash3981 2010

[10] A Roberts and L A Haighton ldquoA hard look at FDArsquos review ofGRAS noticesrdquo Regulatory Toxicology and Pharmacology vol79 pp S124-S128 2016

[11] H H Hashemi Gahruie E Ziaee M H Eskandari andS M Hosseini ldquoCharacterization of basil seed gum-basededible films incorporated with Zataria multiflora essential oilnanoemulsionrdquo Carbohydrate Polymers vol 166 pp 93ndash1032017

[12] S K Devatkal K Narsaiah and A Borah ldquoAnti-oxidant effectof extracts of kinnow rind pomegranate rind and seed powdersin cooked goatmeat pattiesrdquoMeat Science vol 85 no 1 pp 155ndash159 2010

[13] M Estevez R Ramırez S Ventanas and R Cava ldquoSage androsemary essential oils versus BHT for the inhibition of lipidoxidative reactions in liver paterdquo LWTmdashFood Science andTechnology vol 40 no 1 pp 58ndash65 2007

[14] E Abdollahzadeh M Rezaei and H Hosseini ldquoAntibacterialactivity of plant essential oils and extracts the role of thymeessential oil nisin and their combination to control listeriamonocytogenes inoculated in minced fish meatrdquo Food Controlvol 35 no 1 pp 177ndash183 2014

[15] A Alaklabi I A Arif A Ahamed R Surendra Kumar andA Idhayadhulla ldquoEvaluation of antioxidant and anticanceractivities of chemical constituents of the saururus chinensis rootextractsrdquo Saudi Journal of Biological Sciences 2017

[16] M Cam Y Hısıl and G Durmaz ldquoClassification of eightpomegranate juices based on antioxidant capacity measured byfourmethodsrdquo FoodChemistry vol 112 no 3 pp 721ndash726 2009

[17] AOAC Association of Official Agricultural Chemists ldquoOfficialmethods of analysis of AOAC Internationalrdquo in AgricultureChemicals Contaminants Drugs vol 1 AOAC InternationalArlington VA USA 16th edition 1995

[18] K L Yam and S E Papadakis ldquoA simple digital imagingmethodfor measuring and analyzing color of food surfacesrdquo Journal ofFood Engineering vol 61 no 1 pp 137ndash142 2004

[19] K-I An J-H Choi Y-S Choi et al ldquoEffects of kimchi powderon quality characteristics of semi-dried pork jerkyrdquo KoreanJournal for Food Science of Animal Resources vol 30 no 2 pp198ndash205 2010

[20] B Kodal Coskun E Calikoglu Z Karagoz Emiroglu and KCandogan ldquoAntioxidant active packaging with soy edible filmsand oregano or thyme essential oils for oxidative stability ofground beef pattiesrdquo Journal of Food Quality vol 37 no 3 pp203ndash212 2014

[21] B Shan Y Z Cai M Sun and H Corke ldquoAntioxidant capacityof 26 spice extracts and characterization of their phenolicconstituentsrdquo Journal of Agricultural and Food Chemistry vol53 no 20 pp 7749ndash7759 2005

[22] A-M Roussel I Hininger R Benaraba T N Ziegenfuss andR A Anderson ldquoAntioxidant effects of a cinnamon extract inpeople with impaired fasting glucose that are overweight orobeserdquo Journal of the American College of Nutrition vol 28 no1 pp 16ndash21 2009

[23] S Moreno T Scheyer C S Romano and A A VojnovldquoAntioxidant and antimicrobial activities of rosemary extractslinked to their polyphenol compositionrdquo Free Radical Researchvol 40 no 2 pp 223ndash231 2006

[24] F Sharififar M H Moshafi S H Mansouri M Khodashenasand M Khoshnoodi ldquoIn vitro evaluation of antibacterial andantioxidant activities of the essential oil and methanol extractof endemic Zataria multiflora Boissrdquo Food Control vol 18 no7 pp 800ndash805 2007

[25] R Carpenter M N OrsquoGrady Y C OrsquoCallaghan N M OrsquoBrienand J P Kerry ldquoEvaluation of the antioxidant potential of grape

Journal of Food Quality 9

seed and bearberry extracts in raw and cooked porkrdquo MeatScience vol 76 no 4 pp 604ndash610 2007

[26] M T Nunez de Gonzalez B S Hafley R M Boleman R KMiller K S Rhee and J T Keeton ldquoAntioxidant propertiesof plum concentrates and powder in precooked roast beef toreduce lipid oxidationrdquo Meat Science vol 80 no 4 pp 997ndash1004 2008

[27] M P Richards and M A Dettmann ldquoComparative analysisof different hemoglobins autoxidation reaction with peroxideand lipid oxidationrdquo Journal of Agricultural and FoodChemistryvol 51 no 13 pp 3886ndash3891 2003

[28] J Everse and N Hsia ldquoThe toxicities of native and modifiedhemoglobinsrdquo Free Radical Biology and Medicine vol 22 no6 pp 1075ndash1099 1997

[29] C Kennedy D J Buckley and J P Kerry ldquoInfluence of differentgas compositions on the short-term storage stability of mother-packaged retail-ready lamb packsrdquo Meat Science vol 69 no 1pp 27ndash33 2005

[30] J P Kerry M G OrsquoSullivan D J Buckley P B Lynch andP A Morrissey ldquoThe effects of dietary 120572-tocopheryl acetatesupplementation and modified atmosphere packaging (MAP)on the quality of lamb pattiesrdquo Meat Science vol 56 no 1 pp61ndash66 2000

[31] J Fernandez J A Perez-Alvarez and J A Fernandez-LopezldquoThiobarbituric acid test for monitoring lipid oxidation inmeatrdquo Food Chemistry vol 59 no 3 pp 345ndash353 1997

[32] S Barbut D B Josephson and A J Maurer ldquoAntioxidantproperties of rosemary oleoresin in Turkey sausagerdquo Journal ofFood Science vol 50 no 5 pp 1356ndash1359 1985

[33] M B Mielnik K Aaby and G Skrede ldquoCommercial antioxi-dants control lipid oxidation in mechanically deboned turkeymeatrdquoMeat Science vol 65 no 3 pp 1147ndash1155 2003

[34] A Sanchez-Escalante D Djenane G Torrescano J A Beltranand P Roncales ldquoThe effects of ascorbic acid taurine carnosineand rosemary powder on colour and lipid stability of beef pattiespackaged in modified atmosphererdquoMeat Science vol 58 no 4pp 421ndash429 2001

[35] M B Mielnik S Sem B Egelandsdal and G Skrede ldquoBy-products from herbs essential oil production as ingredient inmarinade for Turkey thighsrdquo LWTmdashFood Science and Technol-ogy vol 41 no 1 pp 93ndash100 2008

[36] J H Macneil P S Dimick and M G Mast ldquoUse of chemicalcompounds and a rosemary spice extract in quality mainte-nance of deboned poultry meatrdquo Journal of Food Science vol38 no 6 pp 1080-1081 1973

[37] E TEC ldquoMeat technology update 1-6 2009rdquo[38] H M H Mohamed and H A Mansour ldquoIncorporating

essential oils of marjoram and rosemary in the formulation ofbeef patties manufactured with mechanically deboned poultrymeat to improve the lipid stability and sensory attributesrdquoLWTmdashFood Science and Technology vol 45 no 1 pp 79ndash872012

[39] Z K Emiroglu G P Yemis B K Coskun and K CandoganldquoAntimicrobial activity of soy edible films incorporated withthyme and oregano essential oils on fresh ground beef pattiesrdquoMeat Science vol 86 no 2 pp 283ndash288 2010

[40] ISIR Raw frozen hamburgermdashSpecifications vol 2304 Instituteof standards and industrial research of Iran Karaj Iran 3rdedition 2008

[41] DDjenane A Sanchez-Escalante J A Beltran andP RoncalesldquoAbility of 120572-tocopherol taurine and rosemary in combination

with vitamin C to increase the oxidative stability of beef steakspackaged in modified atmosphererdquo Food Chemistry vol 76 no4 pp 407ndash415 2002

[42] C Vieira M T Diaz B Martınez and M D Garcıa-CachanldquoEffect of frozen storage conditions (temperature and lengthof storage) on microbiological and sensory quality of rusticcrossbred beef at different states of ageingrdquo Meat Science vol83 no 3 pp 398ndash404 2009

[43] J Aliakbarlu and S Khalili Sadaghiani ldquoEffect of avishaneshirazi (zataria multiflora) and clove (syzygium aromaticum)essential oils on microbiological chemical and sensory proper-ties of ground sheep meat during refrigerated storagerdquo Journalof Food Quality vol 38 no 4 pp 240ndash247 2015

Research ArticleOptimization of Ultrasound Extraction of Cactus Pear(Opuntia ficus indica) Seed Oil Based on AntioxidantActivity and Evaluation of Its Antimicrobial Activity

Mariacutea de los Angeles Ortega-Ortega Nelly del Socorro Cruz-CansinoErnesto Alaniacutes-Garciacutea Luis Delgado-Olivares Joseacute Alberto Ariza-OrtegaEsther Ramiacuterez-Moreno and Joseacute de Jesuacutes Manriacutequez-Torres

Centro de Investigacion Interdisciplinario Area Academica de Nutricion Instituto de Ciencias de la Salud Universidad Autonoma delEstado de Hidalgo Circuito Actopan-Tilcuautla SN Ex Hacienda La Concepcion 42160 San Agustın Tlaxiaca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 20 February 2017 Accepted 9 April 2017 Published 27 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Marıa de los Angeles Ortega-Ortega et alThis is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

The purpose of the present study was to determine the optimal ultrasound conditions (amplitude level and time) for the extractionof cactus pear seed oil with the highest antioxidant activity using a closed system Seed oil was analyzed for yield antioxidant activityby ABTS and DPPH and antimicrobial activity Conventional extraction methods were assessed for comparison Amplitude levelsignificantly affected antioxidant activity in linear terms (p lt 00001 DPPH and p lt 0001 ABTS resp) so at lower amplitudes thehigher antioxidant activity was achieved The optimum ultrasound extraction conditions were of 78 amplitude for 10min andyielded antioxidant activity values of 6625mg AAE100 g and 289120583mol TE100 g for ABTS and DPPH respectively Comparedwith conventional extraction methods ultrasound exhibited lower oil yield and antioxidant activity but had the potential toachieve comparable results if multiple ultrasound extractions are performed in the time needed by conventional methods Seed oilsshowed similar antimicrobial activity despite the extraction method and were more effective against Escherichia coli The resultsdemonstrated that ultrasound can be an alternative extraction method of seed oils from fruits such as cactus pear

1 Introduction

Cactus pear fruit (Opuntia ficus indica) is common in aridand semiarid regions around the world [1] This fruit that ismainly consumed fresh in Mexico [2] is composed by pulppeel and seeds [3] According to several studies cactus pearfruit has bioactive compounds [4 5] with high antioxidantand antimicrobial activity [6 7] Some of these compoundsare found in the seeds [8] which comprise 3 to 15 of thecactus pear pulp [9] and are usually considered waste afterpulp processing [7] Seeds also have a high content of oil(988 gkg) [10] characterized by high levels of linoleic andoleic acids [7] and other components as phenols [11] all whichmay contribute to humanhealth [12] Currently seed oils havebeen used as natural agents for food preservation [13] andmany have exhibited antimicrobial and antioxidant activity

some of these oils are from pumpkin [14] apple [15] blackcumin [16] and basil [17] among other seeds Cactus pearseeds fromOpuntia dillenii also have a high antioxidant activ-ity derived from bioactive compounds such as polyphenolsand polyunsaturated fatty acids [18] Some polyunsaturatedfatty acids have also been identified in seeds from Opuntiaficus indica [19 20] implying that these seeds may also havehigh antioxidant activity

Seed oil is usually extracted by means of conventionalmethods such as Soxhlet and maceration using heat agita-tion or long extraction times [21] Microwave supercriticalfluids and ultrasonic assisted extraction are unconventionalmethods that exert a physical effect on the sample [22]Ultrasound has been used to extract antioxidants frommanyfood materials including seeds Ultrasound and ultrasound-assisted extractions use sound waves to produce cavitation

HindawiJournal of Food QualityVolume 2017 Article ID 9315360 9 pageshttpsdoiorg10115520179315360

2 Journal of Food Quality

microbubbles that collapse violently in the sample and facili-tate the release and extraction of several compounds [23ndash25]Some researchers had evaluated ultrasound-assisted extrac-tion in an open system using a sonicator probe directly onthe liquid sample to obtain seed oil fromflaxseed [26] Koreanpine [27] and pomegranate [28] The purpose of the presentstudy was to optimize the extraction conditions of cactuspear seed oil using ultrasound in a closed system based onantioxidant activity and using response surfacemethodologyYield extraction and antioxidant and antimicrobial activitywere compared with conventional methods

2 Materials and Methods

21 Sample Green cactus pear (Opuntia ficus indica) Reynavariety was provided by the Mexican Association CoMeN-Tuna (Consejo Mexicano del Nopal y la Tuna AC ofActopanHidalgoMexico) in spring of 2012Thegreen cactuspear seeds were obtained after several washes with water thatremoved the pulp and residues The seeds were leaved todry at ambient temperature until they reached a moisture of643 After the seeds were crushed using an industrial mill(Cyclotec 1093 Tecator Hoganas AB Sweden) the powderwas passed through a mesh sieve to obtain a particle size ofapproximate 05mm and then stored in sealed plastic bags atroom temperature and dark conditions

22 Ultrasound Extraction Ultrasound (VCX-1500 Sonic ampMaterials Inc Newtown CTUSA) at 1500Wwith a constantfrequency of 20 kHz and a probe of 25mm was used forthe extraction of green cactus pear seeds oil Extractionfrom milled and sieved seeds (20 g) was carried out at anamplitude and time ranges of 80 to 90 and 5 to 15minrespectively and a fixed outlet temperature of 25∘C A sampleof 400mL was introduced in a jacketed vessel with waterat 4∘C circulating through the secondary layer [29] Afterextraction the aqueous and solid phases were separatedby filtration using a vacuum pump (DOA-P704-AA GASTManufacturing Inc BentonHarbor MI USA) Both phasesaqueous and solid (this last was dried) (Weston 74-1001-wWeston Products LLC Strongsville OH USA) were mixedwith hexane for 30min and then separated from the solventby filtration The aqueous phase was centrifuged (Allegra25R Beckman Couler CA USA) at 10000 rpm for 30minat 4∘C and was stored in plastic containers and kept frozenuntil analysis The solid phase was stored in hermeticallysealed bags in the dark The solvent obtained from the twophaseswas evaporated (BUCHILabortechnikAG Flawil SGSwitzerland) at 40∘C to obtain the oil

23 Soxhlet Extraction Soxhlet extraction was performedaccording to the AOAC [30] Milled and sieved seeds (5 g)hexane (120mL) and a universal fat extraction system (BuchiLabortechnik AG Flawil SG Switzerland) were used

24 Maceration Extraction Milled and sieved seeds (10 g)were introduced in a previously defatted cotton bag andthen immersed in 200mL of hexane in a closed glass at atemperature of asymp25∘C After the sample was stored in a dark

place for 24 hrs the oil was obtained after solvent evaporationusing a rotary evaporator (BUCHI Labortechnik AG FlawilSG Switzerland) at 40∘C

25 Yield Oil yield was determined according to Chouguiet al [31] using the following equation

Oil () = (1198721 minus11987201198722 ) times 100 (1)

where1198720 is the weight of the empty Eppendorf tube (g)1198721is the weight of the Eppendorf tube after evaporation (g) and1198722 is the weight of the milled seeds (g)

The oil was stored in 2mL amber Eppendorf tubes atminus32∘C until analysis

26 Determination of Antioxidant Activity

261 ABTS Assay Antiradical capacity by ABTS was mea-sured according to Kuskoski et al [32] The radical cation221015840azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) diam-monium salt (ABTS∙+) was produced by reacting 7mMABTSstock solution with 245mM potassium persulfate in thedark at room temperature for 16 hrs before being used TheABTS∙+ solution was diluted with deionized water to anabsorbance of 070 plusmn 010 at 754 nm An aliquot of 20120583L ofsample was added to 980120583L of the diluted ABTS∙+ solutionand absorbance readings were taken after 7min incubationat room temperature The absorbance of the mixture wasmeasured at 754 nm in themicroplate reader (PowerWaveXSUV-Biotek software KC Junior VT USA) and antioxidantcapacity was expressed as mg ascorbic acid equivalent per100 g of oil (mg AAE100 g)

262 DPPH Assay Antiradical activity was measured using11-diphenyl-2-picrylhydrazyl (DPPH∙) radical as describedby Morales and Jimenez-Perez [33] A methanol-acetatesolution (74mg100mL) of the stable DPPH∙ radical wasprepared A sample aliquot of 100120583Lwas placed into vials and500 120583L of DPPH∙ solution was added before the mixture wasleft to sit at room temperature for 1 hr Finally absorbancewasmeasured at 520 nm in the microplate reader (Power WaveXS UV-Biotek software KC JuniorWinooski VT USA) andantioxidant activity was expressed as 120583mol of Trolox equiva-lents per 100 g of oil (120583mol TE100 g)

27 Experimental Design

271 Optimization The optimization of the ultrasoundextraction conditions was performed using the responsesurface methodology (RSM) with a central composite rotat-able design for two independent extraction variables at fivelevelsThe independent extraction variables (amplitude level80ndash90 time 5ndash15min) were determined based on prelimi-nary experiments where higher antioxidant activity by ABTSand DPPH was observed Design consisted in thirteen com-binations with five central points replicates (Table 1) Exper-imental data were subjected to multiple nonlinear regression

Journal of Food Quality 3

Table 1 Experimental design matrix

Numbera Pattern Amplitude level () Time (min)119883119894 119883119895

(1) 00 85 10(2) +minus 90 5(3) ++ 90 15(4) 00 85 10(5) A0 92 10(6) minusminus 80 5(7) 00 85 10(8) a0 78 10(9) 0A 85 17(10) minus+ 80 15(11) 00 85 10(12) 00 85 10(13) 0a 85 3aNonrandomized

analysis (JMP 702 SAS Institute Inc Cary NC USA) fittedto a second-order polynomial model

119884 = 1205730 +2

sum119894=1

120573119894119883119894 +2

sum119894=1

1205731198941198941198832119894 +sum119894

sum119895=119894+1

120573119894119895119883119894119883119895 (2)

where 119884 is the predicted response 1205730 is the constant coeffi-cient120573119894 is the lineal coefficient120573119894119894 is the quadratic coefficientand120573119894119895 is the interaction coefficients In thismodel119883119894 and119883119895are the independent extraction variables amplitude level ()and time (min) respectively

The adequacy of themathematicalmodel was determinedusing the coefficient 1198772The significance of the model regres-sion coefficients was evaluated using an analysis of varianceThree-dimensional curves from the response surface plotswere obtained to interpret the effects of the interactionbetween independent variables on the response variablesContour plots were generated to represent the extrapolationand interpret the optimization of the extraction variablesusing the Sigma Plot 123 graphing software (SYTAT softwareInc Richmond CA USA)

272 Treatment Comparison Comparison between extrac-tion methods (ultrasound-optimized Soxhlet and macera-tion) was carried out by a one-way analysis of variance(ANOVA) All determinations were performed in triplicateand significant differences between means were determinedby Duncan test (p le 005) using the SPSS program (150 SPSSInc Chicago IL USA)

28 Scanning Electron Microscopy Scanning electron micro-scopy (SEM) was used to examine the morphological alter-ations caused to the cactus pear seeds before and after theultrasound extraction Samples deposited on the siliconwaferwere coated with a thin layer of gold (Denton VacuumDesk V Moorestown NJ USA) applying 20 millitorr and

20mA during 4min Samples were observed in a scanningelectronic microcopy (JEOL JSM-6300 Peabody MA USA)at 1000 and 500 amplifications and micrographs were takento establish the structural comparison between both samples

29 Antimicrobial Activity The green cactus pear seed oilwas tested against one Gram-positive bacteria Staphylococ-cus aureus (ATCC 1654) and two Gram-negative bacteriaEscherichia coli (ATCC 25922) and Pseudomonas aeruginosa(ATCC 27853) All microorganisms were obtained from theMexicanMicrobial Culture Collection of CINVESTAV of theNational Polytechnic Institute (Mexico) For each microor-ganism bacterial suspensions were made in a soybean-casein digest medium to a concentration of approximately108 CFUmL

To evaluate the antimicrobial activity and the mini-mum inhibitory concentration (MIC) the disk diffusionmethod was used Each bacterial suspension (100 120583L fromthe 108 CFUmL) was spread on prepared agar plates (sterileStandardMethodsAgar for bacteria) Filter sterile paper discs(6mm in diameter) were impregnated with 6667 50 3333and 1667 120583L of the undiluted oil and were placed on theinoculated plates The negative control was hexane whileampicillin (10 120583g) and streptomycin (10 120583g) were used aspositive controls The plates where incubated at 37∘C (ArsaAR-130 Felisa Jalisco Mexico) for 24 hrs The diameters ofthe inhibition zones were measured in millimeters and theresults of MIC were expressed as 120583g120583L

3 Results and Discussion

31 Extraction Yield Table 2 shows the oil yields achievedby the ultrasound treatments The extraction yield variedfrom 375 to 6 and the maximum yield was obtained at thehighest amplitude level of 92 Oil yield strongly dependedon amplitude level probably because at high amplitudes thecavitation effect increases [21] and induces physical changeson the structure of the seed such as disruption of the cell wallsreduction of the particle size and increase of exposure areaThese conditions may facilitate the penetration of the solventand thus the extraction of oil [26 28 34] The maximumyield was achieved after 10min of treatment and longertimes (15min) at high amplitudes (90) did not increase oilextraction (Table 2) Albeit time is an important variable afteryield reaches a peak a longer treatment does not maximizeextraction the same was described by Zhang et al [27] forKorean pine seed who demonstrated that oil yield increasedwith time but when it reached amaximum yield equilibratedand then decreased gradually This may be attributed to aninitial complete fracture of the cell walls during the firstminutes of the cavitation effect [26 28 34]

32 Antioxidant Activity of Green Cactus Pear Seed OilExtracted by Ultrasound Due to the complexity of theoxidation processes it is advisable to performmore than onemethod to obtain the antioxidant profile of a sample [35]In order to determine the antioxidant activity of the green

4 Journal of Food Quality

Table 2 Extraction yield and antioxidant activity of green cactus pear seed oil extracted by ultrasound under different conditions

Extraction conditions Antioxidant activity

Amplitude level () Time (min) Oil yield () ABTS DPPHmg AAE100 g 120583mol TE100 g

85 10 575 plusmn 003 6615 plusmn 407 24610 plusmn 09290 5 415 plusmn 001 5598 plusmn 313 14176 plusmn 39090 15 485 plusmn 002 5993 plusmn 445 16702 plusmn 11485 10 525 plusmn 001 6812 plusmn 659 23601 plusmn 32292 10 600 plusmn 006 5584 plusmn 236 10163 plusmn 46880 5 525 plusmn 001 6607 plusmn 217 26707 plusmn 73785 10 375 plusmn 000 6837 plusmn 392 24505 plusmn 23778 10 540 plusmn 010 6599 plusmn 501 28926 plusmn 02685 17 560 plusmn 006 6578 plusmn 037 26009 plusmn 13380 15 540 plusmn 000 6691 plusmn 320 28496 plusmn 09385 10 575 plusmn 000 6773 plusmn 040 27755 plusmn 17185 10 530 plusmn 010 6744 plusmn 389 24508 plusmn 29285 3 550 plusmn 010 6763 plusmn 000 25005 plusmn 199plusmn standard deviation

Table 3 Antioxidant activity regression coefficients of the ultra-sound extraction conditions

Coefficient ABTS DPPH1205730 67562964a 24996199a

120573119894 minus3927762b minus6357459a120573119895 02724311 71702572120573119894119895 077572 18421052120573119894119894 minus3719624b minus2977102b120573119895119895 minus0826106 004258041198772adj 093 096120573119894 amplitude level 120573119895 time significance levels a119901 lt 00001 b119901 lt 0001

cactus pear seed oil two parameters were evaluated antiox-idant and scavenging capacity by ABTS and DPPH respec-tively The results and experimental design are described inTable 2 Antioxidant activity ranged from 5584 to 6837mgAAE100 g for ABTS and 10163 to 28926120583mol TE100 g forDPPH A 1198772 value closest to one or at least of 080 indicates agood fit of themodel [36]The1198772 values for ABTS andDPPHwere 093 and 096 respectively (Table 3) indicating thatthe averages obtained adjusted to the mathematical responsesurface model

33 Effect of Ultrasound Extraction Conditions on the Antiox-idant Activity of Cactus Pear Seed Oil In this study asecond-order polynomial model for predicting the antiox-idant activity of green cactus pear seed oil was obtainedby multiple linear regression analysis of the experimentaldata Table 3 shows the regression coefficients and significantprobabilities of the linear quadratic and interaction effects ofthe ultrasound conditions on the seed oil antioxidant activityBoth ABTS and DPPH values were significantly affected byamplitude level in linear term (120573119894) at 119901 lt 00001 DPPH and119901 lt 0001 ABTS respectively as well as in its quadratic term

(120573119894119894) at 119901 lt 0001 DPPH and ABTS The three-dimensionalsurface plots constructed to observe the effect of ultrasoundprocessing (Figure 1) demonstrated that antioxidant activitywas higher when the applied amplitude decreased

34 Optimization of the Ultrasound Extraction Conditions ofCactus Pear Seed Oil Optimal extraction conditions wereselected from the overlapped contour plots inwhich the effectof amplitude level and time on the antioxidant activity ofgreen cactus pear seed oil was considered

Figure 2 shows the optimal zone where the highestantioxidant activity by ABTS and DPPH was achieved Theconditions corresponded to amplitude of 78 applied for10min In this zone the values for antioxidant activity wereof 6625mg AAE100 g and 289 120583mol TE100 g for ABTS andDPPH respectively

35 Comparison between Methods

Extraction Yield and Antioxidant Activity Figure 3 comparesthe oil yields obtained by the three extraction methodsThe results revealed that the yield obtained using the opti-mized ultrasound extraction was significantly lower than theobtained with the Soxhlet and maceration procedures Thehigher oil yield obtained by Soxhlet could be attributed to theconstant and extended contact (4 to 6 hrs) of the sample withthe solvent at high temperatures in addition to the repeatedwashing cycles [37] The ultrasound yield was closer to thatof maceration method but this last one required longer time(24 hrs) as compared to 10min ultrasound treatment

The results of antioxidant activity by ABTS andDPPH areshown in Figure 4 Both parameters were significantly higherin the oil extracted by Soxhlet (5433 plusmn 084mg AAE100 gand 26660 plusmn 197 120583mol TE100 g resp) compared to theother extraction methods The ultrasound and macerationextractions exhibited similar antioxidant activity by ABTSwhile DPPH was significantly higher for the ultrasound seed

Journal of Food Quality 5

45

50

55

60

65

70

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(mg

AA

E100

g)A

ntio

xida

nt ac

tivity

(a)

50

100

150

200

250

300

350

7880

8284

8688

9092

46810121416

Amplitud

e lev

el (

)

Time (min)

(120583m

ol T

E100

g)A

ntio

xida

nt ac

tivity

(b)

Figure 1 Effect of the ultrasound extraction on the antioxidant activity of green cactus pear seed oil (a) ABTS (b) DPPH

121

109

133145

157

169181

157

169

193

169

181

205

193

205

217

217

205

229

217

229

241

229

241

253

241

253

253

265

265

265

265

277

277

277

265

289

DPPH

5650

5650

557555005425

572558005875

5950

6025

6100

6175

6250

5950

6025

63256400

6175

6250

6250

6325

6475

6325

64006475

6400

6550

6475

6550

6550

6625

6625

6625

6700

6700

6700

6775

6775

6775

6700

6700

6625

6550

6475

6625

ABTS

Optimun condition

4

6

8

10

12

14

16

Tim

e (m

in)

80 82 84 86 88 90 9278Amplitude level ()

Figure 2 Optimal ultrasound extraction conditions of green cactuspear seed oil based on the highest antioxidant activity

oil Albeit the oil extracted by the Soxhlet method presentedhigher yield and antioxidant activity the ultrasound-assistedextraction may be enhanced if multiple extractions arecarried out in a time comparable to the required by theSoxhlet procedure (4ndash6 hrs)

36 Antimicrobial Activity Escherichia coli and Staphylo-coccus aureus are distributed in nature (water soil andvegetation) and are also part of the human intestinal

c

a

b

Ultrasound Soxhlet Maceration0

1

2

3

4

5

6

7

8Yi

eld

()

Figure 3 Cactus pear seed oil yield achieved by different extractionmethods abcDifferent letters mean significant differences betweenmethods (p lt 005)

b a b

b

a

c

Ultrasound Soxhlet Maceration0

255075

100125150175200225250275300

DPPH (120583mol TE100 g)ABTS (mg AAE100 g)

Figure 4 Antioxidant activity by ABTS and DPPH of cactus pearseed oil extracted by different methods abcDifferent letters meansignificant differences between methods (p lt 005)

6 Journal of Food Quality

Table 4 Antimicrobial activity of cactus pear seed oil extracted by different methods

Diameter of inhibition zone (mm)Oillowast (+) control (minus) control

Staphylococcus aureus (Gram-positive)Ultrasound 917 plusmn 029a 1889 plusmn 154 NDSoxhlet 950 plusmn 087a 1878 plusmn 164 NDMaceration 978 plusmn 069a 1811 plusmn 117 NDEscherichia coli (Gram-negative)Ultrasound 778 plusmn 019a 1556 plusmn 212 NDSoxhlet 756 plusmn 019a 1533 plusmn 265 NDMaceration 756 plusmn 038a 1400 plusmn 233 NDPseudomonas aeruginosa (Gram-negative)Ultrasound ND 1256 plusmn 038 NDSoxhlet ND 1222 plusmn 038 NDMaceration ND 1278 plusmn 038 NDlowastSeed oil 6667120583L (+) control ampicillin (disc 10 120583g Staphylococcus aureus and Escherichia coli) and streptomycin (disc 10 120583g Pseudomonas aeruginosa) (minus)control hexane ND not detected plusmn standard deviation a Same superscripts indicates that there is no significant difference (p gt 005)

microbiota [38] Pseudomonas aeruginosa besides beingpresent in the intestinalmicrobiota [39] is a bacteria found inthe soil fertilizers and water used for food production [40]and thus it can contaminate fresh or processed food whichis an indicator of inadequate sanitation or improper han-dling during food production [41] Table 4 summarizes theantimicrobial activity of green cactus pear seed oil Extractionmethod did not have a significant effect on the antimicrobialactivity against Staphylococcus aureus and Escherichia colibut the effect was lower than the positive controls Theseresults may be explained by the similar seed oil concentrationand combined action of compounds on the structure ofmicrobial cells [42 43] despite the extraction method Seedoil did not exhibit antimicrobial activity against Pseudomonasaeruginosa probably due to the oil chemical composition thetype of microorganism and the own characteristics of thebacteria [42ndash44]The antimicrobial activity of oils is generallymore effective against Gram-positive bacteria in comparisonto Gram-negative bacteria which are more resistant mainlybecause their outer membrane is less permeable [42 4345 46] The results suggest that Pseudomonas aeruginosawas more resistant than Escherichia coli probably due tothe lipopolysaccharides present in the outer membrane thatrestrict the diffusion of compounds making it less permeable[45]The resistance can also be caused by systems of exclusionpumps that eject antimicrobial compounds from the inside ofthe bacteria before they can cause damage [39 44]

37 Effect of Ultrasound on the Physical Structure Scanningelectron micrographs of the green cactus pear seeds powderbefore and after the ultrasound treatment at magnificationsfactors of 1000x and 500x are shown in Figure 5 Beforethe ultrasound treatment and despite the previous millingprocess in the control sample it was possible to identify intactstructures of the seeds cell as well as some starch granules

(Figure 5(a)) After the ultrasound treatment the cell struc-tural damage and the variations in the shape and size of theparticles were observed (Figure 5(b)) For instance starchgranules were not observed because sonication fragmentedthese particles while cavitation phenomenon disrupted thecell structures of the seeds [47 48]

4 Conclusions

This study demonstrated that response surface methodologyand a second-order polynomial model were effective tools todetermine the optimumprocessing conditions of ultrasound-assisted extraction based on the maximum values of antiox-idant activity The results demonstrated that cactus pearseed oil has good antioxidant and antimicrobial propertiesUltrasound-assisted extraction was comparable to macera-tion but a single ultrasound process yielded less oil andlower antioxidant activity than solvent extraction (Soxhlet)Ultrasound can be considered an alternative technology forthe extraction of seed oil but further research is required todetermine the uses of the seed oil and the technology withinthe food industry and the potential of several ultrasoundcycles at the optimized conditions

Conflicts of Interest

The authors declare that there are no conflicts of interest

Acknowledgments

This work was financially supported by Programa Integral deFortalecimiento Institucional (PIFI 2014-2015) The authorsacknowledge Mexican Association CoMeNTuna (HidalgoMexico) for providing the plant materials Marıa de losAngeles Ortega-Ortega participated in this research and she

Journal of Food Quality 7

(i) (ii)

A A

(a)

(i) (ii)

(b)

Figure 5 Scanning electron micrographs of green cactus pear seed powder before (a) and after (b) ultrasound treatment (i) 1000x (ii) 500xA The black circle shows a starch granule

received her Bachelorrsquos degree in nutrition in the Universi-dad Autonoma del Estado de Hidalgo Mexico (Act no 12872016)

References

[1] L Lozano ldquoEcofisiologıa de la tuna (Opuntia ficusmdashindica (L)Mill)rdquo Horticultura Argentina vol 30 no 72 pp 37ndash52 2011

[2] LMedina-Torres J A Gallegos-Infante R F Gonzalez-Laredoand N E Rocha-Guzman ldquoDrying kinetics of nopal (Opuntiaficusmdashindica) using three different methods and their effect ontheir mechanical propertiesrdquo LWTmdashFood Science and Technol-ogy vol 41 no 7 pp 1183ndash1188 2008

[3] J A Reyes-Aguero J R Aguirre-Rivera and H M HernandezldquoSystematic notes and a detailed description of Opuntia ficusindica (L)Mill (Cactaceae)rdquoAgrociencia vol 39 no 4 pp 395ndash408 2005

[4] H I Jun M N Cha E I Yang D G Choi and Y S KimldquoPhysicochemical properties and antioxidant activity of Koreancactus (Opuntia humifusa) cladodesrdquoHorticulture Environmentand Biotechnology vol 54 no 3 pp 288ndash295 2013

[5] A Rabhi H Falleh F Limam R Ksouri C Abdelly and ARaies ldquoUpshot of the ripening time on biological activitiesphenol content and fatty acid composition of Tunisian Opuntiaficus-indica fruitrdquo African Journal of Biotechnology vol 12 no40 pp 5875ndash5885 2013

[6] M Kaur A Kaur and R Sharma ldquoPharmacological actions ofOpuntia ficus indica a reviewrdquo Journal of Applied Pharmaceuti-cal Science vol 2 no 7 pp 15ndash18 2012

[7] M R Bhatt and P S Nagar ldquoEvaluation of physicochemicalproperty and fatty acid composition ofOpuntia elatior seed oilrdquoJournal of the Professional Association for Cactus Developmentvol 15 pp 13ndash19 2013

[8] M Ennouri H Fetoui E Bourret N Zeghal F Guermazi andH Attia ldquoEvaluation of some biological parameters of Opuntiaficus indica 2 Influence of seed supplemented diet on ratsrdquo Bio-resource Technology vol 97 no 16 pp 2136ndash2140 2006

[9] SAGARPA Secretarıa de Agricultura Ganaderıa DesarrolloRural Pesca y Alimentacion Pliegos de condiciones para eluso de la marca oficial Mexico calidad suprema en tuna 2005httpwwwmexicocalidadsupremaorgassetsgaleriaPC 0462005 Tunapdf

[10] M F Ramadan and J-TMorsel ldquoOil cactus pear (Opuntia ficus-indica L)rdquo Food Chemistry vol 82 no 3 pp 339ndash345 2003

[11] K El-Mostafa Y Kharrassi A Badreddine et al ldquoNopal Cactus(Opuntia ficus-indica) as a source of bioactive compounds fornutrition health and diseaserdquo Molecules vol 19 no 9 pp14879ndash14901 2014

[12] Z Ghazi M Ramdai M L Fauconnier B El Mahi and RCheikh ldquoFatty acids sterols and Vitamin E composition of seedoil of Opuntia ficus indica and Opuntia dilenii from MoroccordquoJournal of Materials and Environmental Science vol 4 no 6 pp967ndash972 2013

[13] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extrac of Laururs nobillis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

8 Journal of Food Quality

[14] A Nawirska-Olszanska A Kita A Biesiada A Sokol-Łętowska and A Z Kucharska ldquoCharacteristics of antioxidantactivity and composition of pumpkin seed oils in 12 cultivarsrdquoFood Chemistry vol 139 no 1ndash4 pp 155ndash161 2013

[15] V Cervantes-Cardoza N E Rocha-Guzman J A Gallego-Infante M Rosales-Castro L Medina-Torres and R FGonzalez-Laredo ldquoActividad antioxidante de extractos desemilla de tres variedades de manzana (Malus domestica Borkh-Rosaceae-)rdquo Boletın Latinoamericano y del Caribe de PlantasMedicinales y Aromaticas vol 9 no 6 pp 446ndash456 2010

[16] M K M Nair P Vasudevan and K Venkitanarayanan ldquoAnti-bacterial effect of black seed oil onListeriamonocytogenesrdquoFoodControl vol 16 no 5 pp 395ndash398 2005

[17] A I Hussain F Anwar S T H Sherazi and R PrzybylskildquoChemical composition antioxidant and antimicrobial activi-ties of basil (Ocimum basilicum) essential oils depends on sea-sonal variationsrdquo Food Chemistry vol 108 no 3 pp 986ndash9952008

[18] W Liu Y J Fu Y G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[19] M T Labuschagne and A Hugo ldquoOil content and fatty acidcomposition of cactus pear seed compared with cotton andgrape seedrdquo Journal of Food Biochemistry vol 34 no 1 pp 93ndash100 2010

[20] S Zine S Gharby and M El Hadek ldquoPhysicochemical char-acterization of Opuntia ficus-indica seed oil from MoroccordquoBiosciences Biotechnology Research Asia vol 10 no 1 pp 99ndash105 2013

[21] R Azuola and P Vargas ldquoExtraccion de sustancias asistida porultrasonido (EUA)rdquoTecnologıa enMarcha vol 20 no 4 pp 30ndash40 2007

[22] M Gao and C Z Liu ldquoComparison of techniques for theextraction of flavonoids fromcultured cells of SaussureamedusaMaximrdquo World Journal of Microbiology and Biotechnology vol21 no 8-9 pp 1461ndash1463 2005

[23] B Karki B P Lamsal S Jung et al ldquoEnhancing protein andsugar release from defatted soy flakes using ultrasound tech-nologyrdquo Journal of Food Engineering vol 96 no 2 pp 270ndash2782010

[24] F Adam M Abert-Vian G Peltier and F Chemat ldquolsquoSolvent-freersquo ultrasound-assisted extraction of lipids from freshmicroal-gae cells a green clean and scalable processrdquo BioresourceTechnology vol 114 pp 457ndash465 2012

[25] T Allaf V Tomao K Ruiz and F Chemat ldquoInstant controlledpressure drop technology and ultrasound assisted extraction forsequential extraction of essential oil and antioxidantsrdquo Ultra-sonics Sonochemistry vol 20 no 1 pp 239ndash246 2013

[26] Z S Zhang L J Wang D Li S S Jiao X D Chen and ZH Mao ldquoUltrasound-assisted extraction of oil from flaxseedrdquoSeparation and Purification Technology vol 62 no 1 pp 192ndash198 2008

[27] T Zhang Z Wang and X Chen ldquoUltrasound-associatedextraction of seed oil of Korean pinerdquo Journal of Forest Researchvol 16 no 2 pp 140ndash142 2005

[28] A M Goula ldquoUltrasound-assisted extraction of pomegranateseed oilmdashkinetic modelingrdquo Journal of Food Engineering vol117 no 4 pp 492ndash498 2013

[29] Q Y Zafra-Rojas N S Cruz-Cansino A Quintero-Lira etal ldquoApplication of ultrasound in a closed system optimum

condition for antioxidants extraction of blackberry (Rubusfructicosus) residuesrdquoMolecules vol 21 no 7 p 950 2016

[30] AOAC Official Methods of Analysis AOAC InternationalGaithersburg Md USA 18th edition 2005

[31] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[32] EM Kuskoski A G Asuero AM Troncoso J Mancini-Filhoand R Fett ldquoAplicacion de diversos metodos quımicos paradeterminar actividad antioxidante en pulpa de frutosrdquo Cienciae Tecnologia de Alimentos vol 25 no 4 pp 726ndash732 2005

[33] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[34] Y Tian Z Xu B Zheng and Y Martin Lo ldquoOptimization ofultrasonic-assisted extraction of pomegranate (Punica grana-tum L) seed oilrdquo Ultrasonics Sonochemistry vol 20 no 1 pp202ndash208 2013

[35] M L Agudo ldquoTecnicas para la determinacion de compuestosantioxidantes en alimentosrdquo 2010 httpwwwanpebadajozesautodidactaautodidacta archivosnumero 9 archivosl amedinapdf

[36] S K Ho C P Tan Y Y Thoo F Abas and C W HoldquoUltrasound-assisted extraction of antioxidants inMisai Kucing(Orthosiphon stamineus)rdquo Molecules vol 19 no 8 pp 12640ndash12659 2014

[37] S R Kirk R Sawyer and H Egan ldquoMetodos quımicos gen-eralesrdquo inComposicion y Analisis de Alimentos pp 25ndash29 Com-panıa editorial continental Ciudad de Mexico Mexico 2002

[38] S Vazquez S OrsquoNeill and M Legnani ldquoImportancia de loscoliformes en los alimentosrdquo 2013 httpwwwmontevideogubuysitesdefaultfilesimportancia de los coliformes en losalimentospdf

[39] C A Gomez-Alvarez A L Leal-Castro M J Perez de Gonza-lez and M L Navarrete-Jimenez ldquoMecanismos de resistenciaen Pseudomonas aeruginosa entendiendo a un peligroso ene-migordquo Revista de la Facultad de Medicina de la UniversidadNacional de Colombia vol 53 no 1 pp 27ndash34 2005

[40] S D Kominos C E Copeland B Grosiak and B Postic ldquoIntro-duction of Pseudomonas aeruginosa in to a hospital via vegeta-blesrdquo Applied Microbiology vol 24 no 4 pp 567ndash570 1972

[41] NOM Norma Oficial Mexicana NOM-210-SSA1-2014 Pro-ductos y servicios Metodos de prueba microbiologicosDeterminacion de microorganismos indicadores Determina-cion de microorganismos patogenos 2014 httpdofgobmxnota detallephpcodigo=539868ampfecha=26062015

[42] F Reyes-Jurado E Palou and A Lopez-Malo ldquoMetodos deevaluacion de la actividad antimicrobiana y de determinacionde los componentes quımicas de los aceites esencialesrdquo TemasSelectos de Ingenierıa de Alimentos vol 8 pp 68ndash78 2014

[43] D Zekaria ldquoLos aceites esenciales una alternativa a los antimi-crobianosrdquo 2015 httpwwwwpsa-aecaesaeca imgs docswpsa1182855355apdf

[44] DM Livermore ldquoMultiplemechanisms of antimicrobial resist-ance in Pseudomonas aeruginosa our worst nightmarerdquo Clini-cal Infectious Diseases vol 34 no 5 pp 634ndash640 2002

[45] M Viuda-Martos M A Mohamady J Fernandez-Lopez et alldquoIn vitro antioxidant and antibacterial activities of essentials oilsobtained from Egyptian aromatic plantsrdquo Food Control vol 22no 11 pp 1715ndash1722 2011

Journal of Food Quality 9

[46] X Feas L M Estevinho C Salinero et al ldquoTriacylglyc-eride antioxidant and antimicrobial features of virgin camelliaoleiferaC reticulata andC sasanqua oilsrdquoMolecules vol 18 no4 pp 4573ndash4587 2013

[47] R G Earnshaw ldquoUltrasound a new opportunity for foodpreservationrdquo in Ultrasound in Food Processing M J W PoveyandT JMason Eds pp 183ndash192 Editorial BlackAcademic andProfessional New York NY USA 1998

[48] M Vinatoru ldquoAn overview of the ultrasonically assisted extrac-tion of bioactive principles from herbsrdquo Ultrasonics Sonochem-istry vol 8 no 3 pp 303ndash313 2001

Research ArticleAntioxidant and Antimicrobial Properties of CactusPear (Opuntia) Seed Oils

Esther Ramiacuterez-Moreno1 Raquel Carintildeo-Corteacutes2 Nelly del Socorro Cruz-Cansino1

Luis Delgado-Olivares1 Joseacute Alberto Ariza-Ortega1 Vanessa Yelina Montantildeez-Izquierdo3

Mariacutea Manuela Hernaacutendez-Herrero3 and Tomaacutes Filardo-Kerstupp4

1Academic Area of Nutrition Health Sciences Institute Autonomous University of Hidalgo State 42160 Pachuca HGO Mexico2Academic Area of Medicine Autonomous University of Hidalgo State Eliseo Ramırez Ulloa 400 42090 Pachuca HGO Mexico3Department of Food Hygiene Faculty of Veterinary Autonomous University of Barcelona 08193 Bellaterra Spain4Academic Area of Chemistry Basic Science and Engineering Institute Autonomous University of Hidalgo StateCarretera Pachuca-Tulancingo Km 45 Mineral de la Reforma 42183 Pachuca HGO Mexico

Correspondence should be addressed to Nelly del Socorro Cruz-Cansino ncruzuaehedumx

Received 23 January 2017 Accepted 5 April 2017 Published 26 April 2017

Academic Editor Andrea Laukova

Copyright copy 2017 Esther Ramırez-Moreno et alThis is an open access article distributed under the Creative CommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Seed oils from two Mexican varieties of cactus pear (green Opuntia albicarpa and red Opuntia ficus indica) were extracted withdifferent solvents (hexane ethanol and ethyl acetate) to evaluate their antioxidant activity The seed oil with higher antioxidantactivitywas selected to evaluate antimicrobial activityThe fatty acid profilewas analyzed by gas chromatography-mass spectrometry(GC-MS) Oil from green cactus pear seeds obtained with ethanol and ethyl acetate exhibited higher antioxidant activity (119901 lt 005)of 323 and 316 120583mol TE20mg (p lt 005) respectively compared to red cactus pear seed oil (asymp274 and 247 120583mol TE20mgwith ethyl acetate and ethanol resp) The oil obtained with ethanol and higher antioxidant activity was used to determine theantimicrobial activity Both cactus pear oils produced a microbial inhibition zone in most of the microorganisms evaluatedparticularly Saccharomyces cerevisiae which had similar diameter (38ndash40mm) The oil fatty acids profiles of both varieties weresimilar and exhibited a high content of linoleic acid while two fatty acids (linolenic and behenic) found in red cactus pear were notobserved in the green variety

1 Introduction

A relatively untapped source of lipid and protein rawmaterialis the by-product of fruit-processing plants Millions ofpounds of fruit seeds are discarded yearly causing disposalproblems while proper utilization of these waste productscould lead to an important new source of oil and meal [1]Seeds of fruits collect at least some cytoplasmic lipid bodies asmajor storage reserve for lipid accumulation [2] Fruit seedsoils are of great interest because they are edible oils with highdegree of unsaturation antioxidant radical scavenging prop-erties [3ndash8] and a broad spectrum of antimicrobial activity[9ndash15] Therefore the oil from plants can be potentially usedby the food industry for the manufacturing of ldquonaturalrdquo orldquogreenrdquo safe foods [16] and extend shelf-life [17 18]

The oil from cactus pear seed has been found to havean appreciable amount of oil with high levels of unsaturatedfatty acids [19] with antioxidant [20 21] and antimicrobialactivity [22] as well as cardioprotective antithrombotic anti-inflammatory antiarrhythmic hypolipidemic and antihy-perglycemic effect [23 24] These properties are of interestfor the pharmaceutical and food industry However theconcentration and effectiveness of these oils may vary amongcultivars or varieties crop environmental factors (eg lighttemperature and type of soil nutrients) or methods andsolvents used for their extraction Therefore the purpose ofthis research was to determine the antioxidant and antimi-crobial activity and fatty acid profile of the oil obtained fromtwo Mexican varieties of cactus pear (Opuntia albicarpa andOpuntia ficus indica) seeds extracted with different solvents

HindawiJournal of Food QualityVolume 2017 Article ID 3075907 8 pageshttpsdoiorg10115520173075907

2 Journal of Food Quality

2 Materials and Methods

21 Plant Material Two Mexican varieties of cactus pear(Opuntia albicarpa and Opuntia ficus indica) fruit green (cvReyna) and red (cv Rojo Pelon) respectively were providedby theMexican association CoMeNTuna (ConsejoMexicanodel Nopal y la Tuna AC Actopan Hidalgo Mexico) Fruitsfree of external injuries were selected washed and manuallypeeled Cactus pear seeds were obtained after juice wasextracted stirring the pulpwith an industrial blender (38BL52LBC10 Waring Comercial USA) and passing it through aconventional strainer The seeds retained were washed in thestrainer with water until pulp residues were removed

22 Powder Seed and Oil Extraction Green cactus pear seeds(GCPS) and red cactus pear seeds (RCPS)were sun-dried andthen grounded (Cyclotec 1093 Tecator Sweden) to a 1mmdiameter mesh and stored at minus32∘C until further analysisTheseed oil was extracted as follows 25 g of powdered seeds wasmixed with 500mL of solvents with varying polarities (hex-ane ethanol and ethyl acetate) and the obtained residue wasreextracted until extraction solvents become colourless Allthe extracts were filtered through filtration paper Whatmannumber 1 and the filtered extracts were collected for furtherdrying and removal of the remaining solvent at 50∘C using arotary evaporator (BUCHI R-200 Switzerland) All extractswere placed in plastic bottles and then stored at minus20∘C untilused The oils obtained were used to further analysis

23 Free Radical Scavenging Assay The free radical scaven-ging activity was measured using 11-diphenyl-2-picrylhy-drazyl (DPPH∙) radical as described byMorales and Jimenez-Perez [25] A volume of 500 120583L of ethanolic DPPH∙ solution(74mg100mL) was added to a sample aliquot of 100 120583Lplaced in vialsThemixturewas left to sit at room temperaturefor 1 h and then was vortexed and centrifuged at 3000 rpm for10 minutesThe absorbance of the supernatant was measuredat 520 nm in amicroplate reader (PowerWave XSUV-Bioteksoftware KC Junior USA) and 120583mol of Trolox equivalentsper 20 milligram (120583mol TE20mg) of sample was obtainedOil samples with best antioxidant capacity obtained from thedifferent solvents were used for the antimicrobial analysis

24 Antimicrobial Activity Eight standard freeze-dried cul-tures of bacteria Candida albicans (ATCC 10231) Escherichiacoli O58H21 (ATCC 10536) Escherichia coli O157H7(CCUG 44857) Staphylococcus aureus (ATCC 13565) Liste-ria monocytogenes (CCUG 15526) Pseudomonas aeruginosa(ATCC 15442) Saccharomyces cerevisiae (CECT 1942) andSalmonella Typhi (CCUG 29478) were obtained in ther-mosealed vials from the Spanish Type Culture Collection(Autonomous University of Barcelona Barcelona Spain)Freeze-dried cultures were rehydrated in tryptone soy brothat 37∘C for 18 h and then were used to inoculate tryptone soyagar and malt extract agar plates all microorganisms wereincubated at 37∘CexceptCandida albicans and Saccharomycescerevisiae which were incubated at 25∘C Individual colonies

were maintained on specific agar slants stored at 4∘C andsubcultured every 15 days

Disc Diffusion Assay Antimicrobial activity of oil extractedfromGCPS andRCPSwas carried out using the disc diffusionmethod [26] Petri plates were filled with sim20mL of steriletryptone soy agar for bacteria and malt extract agar for fungiThe test cultures were swabbed on the top of the solidifiedmedia and allowed to dry for 10 minutes Serial dilutions(10ndash50 120583gmL) of the seed oil from a stock solution (1mgmL)were prepared in 20 DMSO and 10 120583L loaded onto thesterile blank discs (BBL Sensi-Disc) of 6 millimetersof diameter On the media surface the loaded disks wereplaced and left for 30 minutes at room temperature toallow compound diffusion The seed oil was serially dilutedin MuellerndashHinton broth medium and duplicate tubes ofeach dilution (10ndash100 120583gmL) were inoculated with 5 times106 cells of the test bacteria strain and culturesThe antibioticagents Sensi-Disc streptomycin ampicillin and sulfamethox-azoletrimethoprim (BBL Sensi-Disc) were used as positivecontrols at the same concentration level After plates wereincubated at 37∘C for 24 h the diameters of the inhibitionzones were recorded in millimeters Three independentrepetitions were performed and tests were made in triplicate

25 GC-MS Analysis The GC-MS analysis was performedwith a GC-MS HP-5890 (Hewlett-Packard Company PaloAlto California USA) equipped with a Flame IonizationDetector (FID) and a ZB-WAX fused silica capillary column(60m times 025mm id times 025mm film thickness) packedwith 5 phenylmethylpolysiloxane (Phenomenex TorranceCA) To obtain the methyl esters the cactus pear seed oilswere saponified and derivatized using KOH 1N (IUPAC1969) Changes in the fatty acids of the oils samples werecompared against a standard mixture of 37 components offatty acids methyl esters (FAMEs) (Food Industry FAMEsMix Restek) comprised by methyl esters with chains C40C60 C80 C100 C110 C120 C130 C140 C141 C150C151 C160 C161 C170 C171 C180 C181n9c C181n9tC182n6c C182n6t C183n6 C183n3 C200 C201n9 C202C203n6 C203n3 C204n6 C205n3 C210 C220 C221n9C222 C226n3 C230 C240 and C241n9 The samplevolume injected was of 2 120583L (split ratio 20 2) at an injectorand detector temperatures of 225 and 225∘C respectively N2was used as carrier gas at a flow rate of 12mLsdotminminus1 Fattyacids were calculated as percentage of total FAMEs

26 Statistical Analysis All values were obtained by triplicateand expressed as means plusmn standard deviations (SD) Datawere analyzed using the SPSS V15 software (SPSS InstituteInc Cary NC) An ANOVA was carried out to determinedifferences between oils extracted as well as its antimicrobialactivity that were significant at the 5 level of probability anda Tukey test was used for comparison of data

3 Results and Discussion

31 Yield Comparison between Extraction Solvents Hexaneethanol and ethyl acetate were used to extract the oil from

Journal of Food Quality 3

1183

669

1013

511

106

381

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

2

4

6

8

10

12

14

Oil

yiel

d (

)

Figure 1 Oil yields () extracted from GCPS and RCPS withhexane ethanol and ethyl acetate

cactus pear seeds The extraction yields are compared inFigure 1 which shows that the higher amount of oil () wasobtained from the green cultivar and that yield depended onthe solvent used Oil extraction with hexane was higher forboth fruit varieties (1183 for GCPS and 689 for RCPS)followed by ethanol which reached the same yield as ethylacetate for GCPS (asymp10) Ethyl acetate was the least effectivesolvent for RCPS The extraction yields were similar to thosereported (asymp7 to 11) for several varieties of Opuntia ficusindica [27ndash29] This extraction yields will vary depending onseveral factors as fruit variety harvest period maturationgeographic region percentage of oil in the seed and chemicalcompounds found in the source and by the extractionmethod[30] Researchers have determined that solvent extractioncombinedwith othermethods could increase oil yield as highpressure or supercritical fluid combined with solvent reacheda yield of 933 from tobacco seeds (Nicotiana tabacum L)while sonication and Soxhlet reached a 775 and 1372respectively [31]

32 Free Radical Scavenging Activity Solvent extraction isusually used for isolation of antioxidants the extractiondepends on the solvent selected based on the different antiox-idant compounds with varying polarity [32 33] DPPH is astable free radical that accepts an electron or hydrogen radicalto become a stable diamagnetic molecule [34 35]The DPPHassay has also been used to predict the oxidative stability ofedible oils [36 37] The antioxidant activity determined byDPPH of the oil extracted from RCPS and GCPS is shownin Figure 2 Oil from the GCPS extracted with ethanol andethyl acetate exhibited the higher antioxidant activity (119901 lt005) of 323 and 316 120583mol TE20mg extract respectivelyfollowed by RCPS oil extracted with ethyl acetate (274120583molTE20mg extract) and ethanol (247 120583mol TE20mg extract)These results demonstrate that the extraction solvent hada significant effect on the free radical scavenging capacityof the oil where the hexane had the lower values In ourstudy the green variety exhibited a higher antioxidant activityregardless of solvent Different results may depend mainly

e

d

a

c

ab

Gre

enh

exan

e

Red

hexa

ne

Gre

ene

than

ol

Red

etha

nol

Gre

ene

thyl

acet

ate

Red

ethy

l ace

tate

0

50

100

150

200

250

300

350

휇m

ol T

E20

mg

extr

act

Figure 2 Antioxidant activity of GCPS and RCPS oils extractedwith different solvents andashdDifferent letters above bars indicate thatsamples are significantly different (119901 lt 005)

on the content and concentration of bioactive compounds inthe oil but other factors such as solvent polarity solubilityof the extracts in different testing systems stereoselectivityof the radicals [38] and strong synergism between fattyacids [6] may affect antioxidant activities Other studies havealso reported diverse antioxidant activity among oils fromdifferent Opuntia varieties [20 39 40]

33 Antibacterial and Antifungal Activity The most recom-mended way to prevent or inhibit microbial growth in foodsis the use of food preservatives Essential oils are secondarymetabolites of plants that have wide applications in thefood flavoring and preservative industry [41] Six differentbacterium and two fungi species were used to screen theantimicrobial potential of the oils extracted from the twovarieties of cactus pear seeds Oil extracted with ethanolexhibited the highest antioxidant activity and therefore itwas used to evaluate the antibacterial and antifungal activityFigure 3 shows the results from the microbial assay wheremost microorganisms showed an inhibition zone whenexposed to GCPS and RCPS oils except Salmonella Typhiand Escherichia coli O157H7 (image not shown) From thesetwo microorganisms the first showed an inhibition zonein the presence of antibiotic agents streptomycin (S) ampi-cillin (AMP) and sulfamethoxazoletrimethoprim (STX) indiameters of 146 113 and 273mm respectively (Table 1)while Escherichia coli O157H7 was only inhibited by SXT(253mm) which agrees with other reports of multiantibi-otic resistance of E coli O157H7 due to the presence ofthe gene cluster AMR-SSuT [42] and production of beta-lactamase [43] On the other hand Saccharomyces cerevisiaewas highly inhibited (38ndash40mm) by the extracted oils butgrew in presence of the antimicrobial agents (Figure 3)Similar results were observed for Candida albicans althoughinhibition zones were smaller and similar for both oilsThese observations demonstrate that certain compounds inthe cactus pear seed oil have antimicrobial activity Otherresearchers also reported similar observations for cactus

4 Journal of Food Quality

Table 1 Diameters of growth inhibition zones (mm) in the presence of oil extracted from cactus pear seeds and conventional antimicrobialsA

Microbial cultures Extract Antimicrobial agentGCPS RCPS S AMP SXT

Saccharomyces cerevisiae (CECT1942) 383 plusmn 42a 403 plusmn 45a ND ND NDEscherichia coli O58H21 (ATCC 10536) 119 plusmn 07d 114 plusmn 09d 195 plusmn 14b 178 plusmn 15c 299 plusmn 09a

Escherichia coli O157H7 (CCUG 44857) NDB ND ND ND 253 plusmn 10Staphylococcus aureus (ATCC 13565) 121 plusmn 10c 111 plusmn 11c 183 plusmn 09b 281 plusmn 15a 333 plusmn 19a

Listeria monocytogenes (CCUG15526) 133 plusmn 15c 114 plusmn 09d 213 plusmn 12a 173 plusmn 08c 376 plusmn 18a

Pseudomonas aeruginosa (ATCC15442) 164 plusmn 21c 151 plusmn 20c 201 plusmn 15b 241 plusmn 25a 366 plusmn 29a

Salmonella typhi (CCUG29478) ND ND 146 plusmn 04b 113 plusmn 18c 273 plusmn 08a

Candida albicans (ATCC 10231) 111 plusmn 10a 110 plusmn 18a ND ND NDAInhibition zone diameters for oil and reference antibiotics are means plusmn SE of three replicas GCPS green cactus pear seed oil extract RCPS red cactus pearseed oil extract S streptomycin (10120583gdisc) AMP ampicillin (10 120583gdisc) and SXT sulfamethoxazoletrimethoprim (10120583gdisc) BND not detected activityandashdDifferent letters in the same row indicate significant differences

RG

SXT

S

AMP

(a)

RG

SXT

S

AMP

(b)

R G

SXTS

AMP

(c)

RG

SXTS

AMP

(d)

RG

SXT

S

AMP

(e)

R G

SXT

S

AMP

(f)

Figure 3 Antimicrobial activity of oil extracted from green cactus pear (G) oil extracted from red cactus pear seeds (R) streptomycin(S) ampicillin (AMP) and sulfamethoxazoletrimethoprim (SXT) Candida albicans (ATCC 10231) (a) Escherichia coli O58H21 (ATCC10536) (b) Staphylococcus aureus (ATCC 13565) (c) Listeria monocytogenes (CCUG15526) (d) Pseudomonas aeruginosa (ATCC15442) (e)Saccharomyces cerevisiae (CECT1942) (f)

pear fruit cv Opuntia stricta [44] and for other plants asfennel (Foeniculum vulgare L) and chamomile (Matricariachamomilla L) [5] Differences in the levels of antimicrobialactivity may be partially attributed to variable chemicalcomposition of the oils [45] Mnayer et al [46] suggestedthat oil compounds can act on different bacterial structureswhile Gill et al [47] mentioned that whole oils have a greater

antibacterial activity than the major component mixed sothat minor components are critical for the activity and exerta synergistic effect [16 48 49]

In the present study the antimicrobial activity of cactuspear seed oil was more effective against fungi comparedto bacteria cultures These interesting results suggest thatthere is a link between the oil chemical contents and the

Journal of Food Quality 5

Table 2 Percentages of FAMEs in crude cactus pear seed oil extracts

FAMEs Green cactus pear seed oil extract Red cactus pear seed oil extractC140 0078 plusmn 000 0066 plusmn 001C160 12327 plusmn 009 12887 plusmn 002C161 0429 plusmn 002 0570 plusmn 001C162 0073 plusmn 000 0540 plusmn 000C170 0060 plusmn 001 0075 plusmn 000C180 3436 plusmn 001 3389 plusmn 007C181 16215 plusmn 003 17061 plusmn 001C182 67448 plusmn 008 65407 plusmn 001C183 Ni 0372 plusmn 001C220 Ni 0160 plusmn 001Means of 3 replicates plusmn SE Ni not identified

140

160

181

182

18017

016

116

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(a)14

0 161

162

170

180

181

182

183

220

160

2

00

01

02

(Vol

ts)

5 10 15 20 25 300(Minutes)

(b)

Figure 4 Chromatograms of FAMEs of cactus pear seed oil extract (a) Green cactus pear seed oil extract (b) red cactus pear seed oil extractIn both oils extracts were identified myristic (C140) palmitic (C160) palmitoleic (C161 cis-9) hexadecadienoic (C162 cis-9 12) margaric(C170) stearic (C180) oleic (C181 cis-9) linoleic (C182 cis-9 12) except linolenic (C183 cis-6 9 12) and behenic (C220) fatty acids thatwere identified only in red cactus pear seed

antimicrobial activity The membrane disruption could beone mechanism of action by inactivating microbial adhesionenzymes and proteins transport [15 46] RCPS and GCPSextracts inhibited most of the evaluated bacterial and fungispecies (Table 1) however antimicrobial activity was notdetected for Salmonella Typhi which is a gram-negative bac-terium In general gram-negative bacteria have an effectiveoutermembrane that restricts the penetration of amphipathiccompounds and has a mechanism to extrude toxins across[50]Thismay explain the apparent antimicrobial ineffective-ness of the oils against the permeability barrier in addition tothe presence of multidrug resistance encoding plasmids [51]

34 Fatty Acid Profile FAMEs chromatograms and percent-ages are shown in Figure 4 and Table 2 Cactus pear seed oilscontained saturated and unsaturated fatty acids the linoleicfatty acid being the predominant (674 and 654 in GCPSand RCPS oils resp) Minimal amounts of myristic (C140)palmitoleic (C161) hexadecadienoic (C162) and margaric(C170) fatty acids in both oils were also identified The fattyacids profiles of the two cactus pear varieties were similarhowever theGCPS had a slightly higher content of the linoleicacid (C182)while the fatty acids linolenic (C183) and behenic(C220) were in minimal amounts only in the RCPS

Different studies have established that factors as cultivartype temperature and harvest time have a strong influence inparameter as pH Brix vitamin C sugars and fat content [5253] Oumato et al [52] found differences in linoleic fatty acid(C182) content among cactus pear cultivars In other studythe oleic acid (C181) content was significantly influenced bythe cultivar and location interaction [53] providing uniquecharacteristics to the oil

In comparison with other plants oils the linoleic acid(C182) content of the cactus pear fruit was similar to thelevels reported for sunflower oil (62) [54] and higher thanwheat germ oil (5505) [55] and soybean oil (5270)[56] The contents of other FAMEs in cactus pear varietiessuch as palmitic (C160) oleic (C181) and stearic (C180)were similar to those reported for Castilla blackberry (Rubusglaucus Benth) with 1124 passion fruit (Passiflora edulis)with 1547 [57] and grape (Vitis vinifera) with 35 [58]

Other researchers have reported similar fatty acidsprofile to our findings for different plant materials andhave analyzed the antimicrobial effectiveness against dif-ferent microorganisms For instance fatty acids found inAllium cepa were found to effectively inhibit Staphylococcusaureus Bacillus subtilis Enterococcus faecalis Escherichia coliand Klebsiella pneumoniae [59] Oil extracted from SwieteniaMacrophylla king seed oil inhibited growth of S aureus

6 Journal of Food Quality

S Typhimurium and P aeruginosa [60] These studies de-monstrate that seed oil can inhibit fungi and bacteria buttheir efficacy would depend on their concentration levels andspecific pathogen [15]

4 Conclusions

Oil yield from the green cactus pearwas higher in comparisonto the red cultivar andwas also influenced by the solvent usedHexane exhibited high extraction yield while oils extractedwith ethanol had the better antioxidant activity The resultsdemonstrated that oil extracts from both varieties have anoticeable antimicrobial activity against gram-positive andgram-negative bacteria comparable to antimicrobial com-pounds such as ampicillin streptomycin and sulfamethoxa-zoletrimethoprimThis research provides further incentivesto develop additives for the food cosmetic and pharmaceu-tical sectors seeking natural compounds with antimicrobialactivity Further studies are needed to determine the specificcomponent responsible for the antimicrobial activity in cac-tus pear seeds oil and determine the optimum levels of oilextract and the antimicrobial effectiveness in the foodmatrix

Additional Points

Practical Application Our results suggest that the oilsextracted from cactus pear seeds have the potential to be usedas a natural antioxidant and antimicrobial agents by the foodcosmetic and pharmaceutical sectors

Conflicts of Interest

The authors have declared that no conflicts of interest exist

Acknowledgments

This study was possible thanks to the financial supportfrom the Programa Integral de Fortalecimiento Institucional(PIFI 2013ndash2015) Mexico This research project was partiallysupported by the Food Hygiene Department Faculty ofVeterinary from the Autonomous University of BarcelonaSpain The authors acknowledge the Mexican associationCoMeNTuna (Consejo Mexicano del Nopal y la TunaHidalgo Mexico) for providing the plant materials

References

[1] B S Kamel and Y Kakuda ldquoFatty acids in fruits and fruit prod-uctsrdquo in Acids in Foods and Their Health Implications pp 263ndash301 CRC Press 3rd edition 2007

[2] D J Murphy I Hernandez-Pinzon and K Patel ldquoRole oflipid bodies and lipid-body proteins in seeds and other tissuesrdquoJournal of Plant Physiology vol 158 no 4 pp 471ndash478 2001

[3] A Kedia B Prakash P KMishra andN K Dubey ldquoAntifungaland antiaflatoxigenic properties of Cuminum cyminum (L)seed essential oil and its efficacy as a preservative in storedcommoditiesrdquo International Journal of Food Microbiology vol168-169 pp 1ndash7 2014

[4] S Singh S S Das G Singh C SchuffM P de Lampasona andC A Catalan ldquoComposition in vitro antioxidant and antimi-crobial activities of essential oil and oleoresins obtained fromblack cumin seeds (Nigella sativa L)rdquo BioMed Research Inter-national vol 2014 Article ID 918209 10 pages 2014

[5] M H H Roby M A Sarhan K A-H Selim and K I KhalelldquoAntioxidant and antimicrobial activities of essential oil andextracts of fennel (Foeniculum vulgare L) and chamomile(Matricaria chamomilla L)rdquo Industrial Crops and Products vol44 pp 437ndash445 2013

[6] G Kavoosi A Tafsiry A A Ebdam and V Rowshan ldquoEvalua-tion of antioxidant and antimicrobial activities of essential oilsfrom carum copticum seed and ferula assafoetida latexrdquo Journalof Food Science vol 78 no 2 pp T356ndashT361 2013

[7] S Lalas O Gortzi V Athanasiadis J Tsaknis and I ChinouldquoDetermination of antimicrobial activity and resistance tooxidation of Moringa peregrina seed oilrdquoMolecules vol 17 no3 pp 2330ndash2334 2012

[8] B Ozcan M Esen M K Sangun A Coleri and M CaliskanldquoEffective antibacterial and antioxidant properties of methano-lic extract of Laurus nobilis seed oilrdquo Journal of EnvironmentalBiology vol 31 no 5 pp 637ndash641 2010

[9] R S Bhat and S Al-daihan ldquoAntimicrobial activity of Litchichinensis and Nephelium lappaceum aqueous seed extractsagainst some pathogenic bacterial strainsrdquo Journal of King SaudUniversitymdashScience vol 26 no 1 pp 79ndash82 2014

[10] J M Silvan E Mingo M Hidalgo S de Pascual-Teresa A VCarrascosa and A J Martinez-Rodriguez ldquoAntibacterial activ-ity of a grape seed extract and its fractions against Campylobac-ter spprdquo Food Control vol 29 no 1 pp 25ndash31 2013

[11] K Rakholiya M Kaneria D Desai and S Chanda ldquoAntimi-crobial activity of decoction extracts of residual parts (seedand peels) ofMangifera indica L var Kesar against pathogenicand food spoilage microorganismrdquo in Microbial pathogens andstrategies for combating them science technology and educationA Mendez-Vilas Ed vol 2 pp 850ndash856 2013

[12] N A Hasan M Z Nawahwi and H Ab Malek ldquoAntimicrobialactivity ofNigella sativa seed extractrdquo Sains Malaysiana vol 42no 2 pp 143ndash147 2013

[13] Z I Sajid F Anwar G Shabir G Rasul KM Alkharfy and A-H Gilani ldquoAntioxidant antimicrobial properties and phenolicsof different solvent extracts from bark leaves and seeds ofPongamia pinnata (L) pierrerdquoMolecules vol 17 no 4 pp 3917ndash3932 2012

[14] M Khoobchandani B K Ojeswi N Ganesh et al ldquoAntimicro-bial properties and analytical profile of traditional Eruca sativaseed oil comparisonwith various aerial and root plant extractsrdquoFood Chemistry vol 120 no 1 pp 217ndash224 2010

[15] V Kesari A Das and L Rangan ldquoPhysico-chemical charac-terization and antimicrobial activity from seed oil of Pongamiapinnata a potential biofuel croprdquo Biomass and Bioenergy vol34 no 1 pp 108ndash115 2010

[16] K Carovic-Stanko S Orlic O Politeo et al ldquoComposition andantibacterial activities of essential oils of seven Ocimum taxardquoFood Chemistry vol 119 no 1 pp 196ndash201 2010

[17] MM Tajkarimi S A Ibrahim andDO Cliver ldquoAntimicrobialherb and spice compounds in foodrdquo Food Control vol 21 no 9pp 1199ndash1218 2010

[18] F Solorzano-Santos andM GMiranda-Novales ldquoEssential oilsfrom aromatic herbs as antimicrobial agentsrdquo Current Opinionin Biotechnology vol 23 no 2 pp 136ndash141 2012

Journal of Food Quality 7

[19] N Chougui A Tamendjari W Hamidj et al ldquoOil compositionand characterisation of phenolic compounds of Opuntia ficus-indica seedsrdquo Food Chemistry vol 139 no 1ndash4 pp 796ndash8032013

[20] W Liu Y-J Fu Y-G Zu et al ldquoSupercritical carbon dioxideextraction of seed oil from Opuntia dillenii Haw and itsantioxidant activityrdquo Food Chemistry vol 114 no 1 pp 334ndash3392009

[21] B Matthaus and M M Ozcan ldquoHabitat effects on yield fattyacid composition and tocopherol contents of prickly pear(Opuntia ficus-indica L) seed oilsrdquo Scientia Horticulturae vol131 pp 95ndash98 2011

[22] P Zito M Sajeva M Bruno S Rosselli A Maggio and FSenatore ldquoEssential oils composition of two Sicilian cultivars ofOpuntia ficus-indica (L)Mill (Cactaceae) fruits (prickly pear)rdquoNatural Product Research vol 27 no 14 pp 1305ndash1314 2013

[23] KMobraten TMHaug C R Kleiveland and T Lea ldquoOmega-3 and omega-6 PUFAs induce the same GPR120-mediatedsignalling events but with different kinetics and intensity inCaco-2 cellsrdquo Lipids in Health and Disease vol 12 no 1 ArticleID 101 2013

[24] A BerraaouanA ZiyyatHMekhfi et al ldquoEvaluation of antidi-abetic properties of cactus pear seed oil in ratsrdquo PharmaceuticalBiology vol 52 no 10 pp 1286ndash1290 2014

[25] F J Morales and S Jimenez-Perez ldquoFree radical scavengingcapacity of Maillard reaction products as related to colour andfluorescencerdquo Food Chemistry vol 72 no 1 pp 119ndash125 2001

[26] P R Murray E J Baron M A Pfaller F C Tenover and R HYolkeManual of Clinical Microbiology 1995 Washington DCUSA

[27] M Ennouri H Fetoui E Bourret N Zeghal and H AttialdquoEvaluation of some biological parameters of Opuntia ficusindica 1 Influence of a seed oil supplemented diet on ratsrdquoBioresource Technology vol 97 no 12 pp 1382ndash1386 2006

[28] Y Habibi L Heux M Mahrouz and M R Vignon ldquoMorpho-logical and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruitsrdquo Carbohydrate Polymers vol 72 no 1pp 102ndash112 2008

[29] MMoudenM Boujnah S Salmaoui S Zantar and A DouiraldquoEffect of two extraction methods and harvest period andperformance there statement of fatty oils of figs pear seedrdquoInternational Journal of Pure amp Applied Bioscience vol 4 no1 pp 1ndash8 2016

[30] A El Finti M Belayadi R El Boullani F Msanda and A ElMousadik ldquoAssessment of some agro-technological parametersof cactus pear fruit (Opuntia ficus-indica Mill) in Moroccocultivarsrdquo Journal of Medicinal Plants Research no 7 pp 2574ndash2583 2013

[31] S Majdi M Barzegar A Jabbari and M Agha AlikhanildquoSupercritical fluid extraction of tobacco seed oil and itscomparison with solvent extraction methodsrdquo Journal of Agri-cultural Science and Technology vol 14 no 5 pp 1043ndash10512012

[32] E M Marinova and N V Yanishlieva ldquoAntioxidative activity ofextracts from selected species of the family Lamiaceae insunflower oilrdquo Food Chemistry vol 58 no 3 pp 245ndash248 1997

[33] Y-Y Soong and P J Barlow ldquoAntioxidant activity and phenoliccontent of selected fruit seedsrdquo Food Chemistry vol 88 no 3pp 411ndash417 2004

[34] J R Soares T C P Dinis A P Cunha and L M AlmeidaldquoAntioxidant activities of some extracts of Thymus zygisrdquo FreeRadical Research vol 26 no 5 pp 469ndash478 1997

[35] I GulcinMOktay E Kirecci and O I Kufrevioglu ldquoScreeningof antioxidant and antimicrobial activities of anise (Pimpinellaanisum L) seed extractsrdquo Food Chemistry vol 83 pp 371ndash3822003

[36] J Lee H Chung P-S Chang and J Lee ldquoDevelopment of amethod predicting the oxidative stability of edible oils using 22-diphenyl-1-picrylhydrazyl (DPPH)rdquo Food Chemistry vol 103no 2 pp 662ndash669 2007

[37] A Fazio P Plastina J Meijerink R F Witkamp and BGabriele ldquoComparative analyses of seeds of wild fruits ofRubus and Sambucus species from Southern Italy fatty acidcomposition of the oil total phenolic content antioxidant andanti-inflammatory properties of the methanolic extractsrdquo FoodChemistry vol 140 no 4 pp 817ndash824 2013

[38] R L Prior X Wu and K Schaich ldquoStandardized methods forthe determination of antioxidant capacity and phenolics infoods and dietary supplementsrdquo Journal of Agricultural andFood Chemistry vol 53 no 10 pp 4290ndash4302 2005

[39] A Cardador-Martınez C Jimenez-Martınez and G SandovalldquoRevalorization of cactus pear (Opuntia spp) wastes as a sourceof antioxidantsrdquo Ciencia e Tecnologia de Alimentos vol 31 no3 pp 782ndash788 2011

[40] Z Ghazi M Ramdani M Tahri et al ldquoChemical compositionand antioxidant activity of seeds oils and fruit juicerdquo Journalof Materials and Environmental Science vol 6 no 8 pp 2338ndash2345 2015

[41] V K Bajpai K-H Baek and S C Kang ldquoControl of Salmonellain foods by using essential oils a reviewrdquo Food ResearchInternational vol 45 no 2 pp 722ndash734 2012

[42] K Ziebell R P Johnson A M Kropinski et al ldquoGenecluster conferring streptomycin sulfonamide and tetracyclineresistance in Escherichia coli O157H7 phage types 23 45 and67rdquo Applied and Environmental Microbiology vol 77 no 5 pp1900ndash1903 2011

[43] O Chandra K J Putra and I Wayan ldquoAntibiotic resistanceprofiles of Escherichia coli O157H7 in cattle at Suth-KutaBadung Regency Bali Indonesiardquo Global Veterinaria vol 15no 5 pp 480ndash484 2015

[44] E Moosazadeh M R Akhgar and A Kariminik ldquoChemicalcomposition and antimicrobial activity of Opuntia stricta Fessential oilrdquo Journal of Biodiversity and Environmental Sciencesvol 4 pp 94ndash101 2014

[45] S Burt ldquoEssential oils their antibacterial properties and poten-tial applications in foods - a reviewrdquo International Journal ofFood Microbiology vol 94 no 3 pp 223ndash253 2004

[46] D Mnayer A-S Fabiano-Tixier E Petitcolas et al ldquoChemicalcomposition antibacterial and antioxidant activities of sixessentials oils from the Alliaceae familyrdquo Molecules vol 19 no12 pp 20034ndash20053 2014

[47] A O Gill P Delaquis P Russo and R A Holley ldquoEvaluationof antilisterial action of cilantro oil on vacuum packed hamrdquoInternational Journal of FoodMicrobiology vol 73 no 1 pp 83ndash92 2002

[48] M Turgis K D Vu C Dupont and M Lacroix ldquoCombinedantimicrobial effect of essential oils and bacteriocins againstfoodborne pathogens and food spoilage bacteriardquoFoodResearchInternational vol 48 no 2 pp 696ndash702 2012

[49] H Zengin and A H Baysal ldquoAntibacterial and antioxi-dant activity of essential oil terpenes against pathogenic andspoilage-forming bacteria and cell structure-activity relation-ships evaluated by SEM microscopyrdquo Molecules vol 19 no 11pp 17773ndash17798 2014

8 Journal of Food Quality

[50] G Tegos F R Stermitz O Lomovskaya and K Lewis ldquoMul-tidrug pump inhibitors uncover remarkable activity of plantantimicrobialsrdquo Antimicrobial Agents and Chemotherapy vol46 no 10 pp 3133ndash3141 2002

[51] M Baltazar A Ngandjio K E Holt et al ldquoMultidrug-resistantSalmonella enterica serotype typhi Gulf of Guinea RegionAfricardquo Emerging Infectious Diseases vol 21 no 4 pp 655ndash6592015

[52] J Oumato S ZriraM Boujnah andB Saidi ldquoEffect ofmaturitystage onmorphological and chemical characteristics ofOpuntiaficus indica from Moroccordquo International Journal of Innovationand Applied Studies vol 20 no 1 pp 400ndash410 2017

[53] M deWit A Hugo N Shongwe and R van derMerwe ldquoEffectof cultivar season and locality on lipid content and fatty acidcomposition of cactus pear seed oilrdquo South African Journal ofPlant and Soil no 33 pp 279ndash288 2016

[54] Australian Oilseeds Federation Incorporated 2015 Section 1ldquoQuality standards technical information amp typical analysisrdquono 14 pp 31ndash40 2016 (Accessed 1 November 2015)

[55] A Awad A Adel A A M Nady and AAE ldquoWheat germ anoverview on nutritional value antioxidant potential andantibacterial characteristicsrdquo Food and Nutrition Sciences vol6 no 2 pp 265ndash277 2015

[56] P Pumrojana S Terapuntuwat and P Pakdee ldquoInfluence offatty acid composition of soybean oil vs beef tallow on egg yolkfatty acid profiles of laying hensrdquo Pakistan Journal of Nutritionvol 14 no 7 pp 383ndash387 2015

[57] A F Ceron M O Osorio and B A Hurtado ldquoIdentificacionde acidos grasos contenidos en los aceites extraıdos a partir desemillas de tres diferentes especies de frutasrdquo Acta Agronomicavol 61 no 2 pp 126ndash132 2012

[58] J Orsavova L Misurcova J Vavra Ambrozova R Vicha andJ Mlcek ldquoFatty acids composition of vegetable oils and itscontribution to dietary energy intake and dependence of car-diovascular mortality on dietary intake of fatty acidsrdquo Interna-tional Journal of Molecular Sciences vol 16 no 6 pp 12871ndash12890 2015

[59] M Derbali A Elaissi I Cheraief and M Aouni ldquoFatty acidcomposition and antimicrobial activity against sensitive andmulti-drug resistant bacteria of Tunisian Allium cepa seedextractrdquo Research amp Reviews Journal of Hospital and ClinicalPharmacy vol 2 no 2 pp 30ndash34 2016

[60] M B Suliman A H Nour M M Yusoff P Kuppusamy A RYuvaraj and S A Mazza ldquoFatty acid composition and antibac-terial activity of Swietenia macrophylla king seed oilrdquo AfricanJournal of Plant Science vol 7 no 7 pp 300ndash303 2013

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