Decontamination technologies for meat products

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Meat Science 78 (2008) 114129

MEATSCIENCE

Decontamination technologies for meat products

T. Aymerich, P.A. Picouet *, J.M. Monfort

IRTA, Finca Camps i Armet, E-17121 Monells, Girona, Spain

Received 9 March 2007; received in revised form 4 July 2007; accepted 9 July 2007

Abstract

Consumers demand high quality, natural, nutritious, fresh appearance and convenient meat products with natural flavour and tasteand an extended shelf-life. To match all these demands without compromising safety, in the last decades alternative non-thermal pres-ervation technologies such as HHP, irradiation, light pulses, natural biopreservatives together with active packaging have been proposedand further investigated. They are efficient to inactivate the vegetative microorganisms, most commonly related to food-borne diseases,but not spores. The combination of several non-thermal and thermal preservation technologies under the so-called hurdle concept hasalso been investigated in order to increase their efficiency. Quick thermal technologies such as microwave and radiofrequency tunnels orsteam pasteurization bring new possibilities to the pasteurization of meat products especially in ready to eat meals. Their applicationafter final packaging will prevent further cross-contamination during post-processing handling. The benefits of these new technologiesand their limitations in an industrial application will be presented and discussed. 2007 Elsevier Ltd. All rights reserved.

Keywords: Non-thermal and thermal technologies; Meat; Irradiation; High hydrostatic pressure; Biopreservation and natural antimicrobials; Activepackaging; Radio frequency and microwave heating; Ohmic heating; Steam pasteurization

1. Introduction

Meat is a rich nutrient matrix that provides a suitableenvironment for proliferation of meat spoilage microorgan-isms and common food-borne pathogens, therefore ade-quate preservation technologies must be applied in orderto preserve its safety and quality. Food safety is a top priorityfor authorities and consumers worldwide. Food safety objec-tives and hazard analysis and critical control point are beingintroduced worldwide. In the European Union an extensivehygienic legislative package is now into force (European Par-liament & of the Council, 2002, 2004a, 2004b, 2004c, 2004d)and the established Microbiological criteria (EuropeanCommission, 2005a, 2005b) must be accomplished.

Nevertheless, the prevalence of food-borne pathogensand the reported number of cases and outbreaks is stillhigh, thus affecting personal lives, business and countrieseconomies. In Europe 2005, 380,000 European Union citi-

0309-1740/$ - see front matter 2007 Elsevier Ltd. All rights reserved.doi:10.1016/j.meatsci.2007.07.007

* Corresponding author. Tel.: +34 972 63 0052; fax: +34 972 63 0373.E-mail address: [email protected] (P.A. Picouet).

zens were affected by infectious zoonotic diseases, 5311food-borne outbreaks were reported involving 47,251 peo-ple and resulting in 5330 hospitalizations and 24 deaths.Campylobacter and Salmonella reported the highest num-ber of cases, 197,363 and 176,395, mainly related to freshpoultry meat and eggs, poultry and pig meat, respectively.Yersinia enterocolitica reported 9630 cases and Escherichiacoli VTEC caused 3314 cases, which were mainly associ-ated to fresh bovine meat. Listeria monocytogenes reported1439 cases, mainly related to RTE products, and Brucellamellitensis accounted for 1218 cases (European FoodSafety Authority, 2006).

Consumer demands high quality, convenient, innova-tive, regular and safe meat products with natural flavourand taste and an extended shelf-life. Moreover less salty,less acidified and less chemical preserved products arerequired. To match all these demands without compromis-ing safety, the production and manufacture of meat prod-ucts is at stage of innovative dynamics thus stimulating amajor research issue to develop and implement alternativetechnologies such as the so called non-thermal technologies
mailto:[email protected]

0

5

10

15

20

25

Total MRCM Poultry Meat Frog Legs Others

Products

Irra

dia

ted

Fo

od

in 1

000x

To

ns

2002

2003

2005

2004

Fig. 1. The use of irradiation in Europe: Quantities (in thousand tonnes)of irradiated products declare by four members states (Belgium, France,Germany and Holland) to the European commission from 2002 to 2005.Data extract from European Commission reports (COM 69, 2004, C230/07, 2006; C230/08, 2006; C122/03, 2007). MRCM: Mechanically recoveredchicken meat.

Table 1Summary of the depth and efficiency from three ionised-irradiationtechnologies used in food processing (extract from Koutchma, 2006)

Gamma ray X-ray E-beam

Power source (kW) 50 25 35Source energy (MeV) 1.33 5 510Processing speeda (tonnes/h) 12 10 510Penetration depth (cm) 80100 80100 810Dose uniformity ratio 1.7 1.5 ModerateDose rate (kGy/h) Low High High

a Processing speed to deliver a dose rate of 4 kGy.

T. Aymerich et al. / Meat Science 78 (2008) 114129 115

or alternative, quicker, sensory-milder thermal technolo-gies. Some promising non-thermal and thermal technolo-gies are being considered at industrial level fordecontamination of meat products, gamma, electron andX-ray irradiation, high hydrostatic pressure (HHP), natu-ral antimicrobials, active packaging, ohmic heating, micro-wave and radiofrequency and steam among others. Allthese alternative technologies try to be mild, guarantee nat-ural appearance, energy saving and environmentallyfriendly while knocking the pathogens and spoilage micro-organisms. Their combination, as in the hurdle theory pro-posed by Leistner (2000) may improve their effectiveness.

2. Non-thermal alternative technologies

2.1. Irradiation

The irradiation technology implies the exposure of meatproducts to ionizing irradiation to decontaminate foodproducts. It was first suggested in 1897, 1-year after Roet-gens discovered X-rays and it was patented in England in1905. From 1940 to 1960, research was conducted at thequartermaster laboratory of the US Army to provide ster-ilized cans to the US army. In 1962, the first food irradia-tion facility was built for the army and the USDA issuedthe first food irradiation rules in 1963 to decontaminatewheat and wheat powder (Ahn, Lee, & Mendonca, 2006).The first meat irradiation rules were published by theUSDA in 1985 to inactivate Trichinella spiralis in pork car-cass and in 1997, the irradiation of red ground meat wasauthorized. It was promoted by the FAO in the Codex Ali-mentarius in 2003 and was well accepted in 50 countries,especially in USA, Latin America, Egypt and China. InEurope, consumer acceptance has postponed its applica-tion and irradiation of food is restricted to dried aromaticherbs, spices and vegetable seasoning (European Parlia-ment & of the Council, 1999a, 1999b). Although on theapproximation of National laws of the member states,the EU commission has authorised the treatment of meatproducts in some countries (European Commission,2001). Fig. 1 shows the amount of irradiated meat productstreated in different European countries from 2002 to 2005.

Ionizing irradiation occurs when one or more electronsare removed from the electronic orbital of the atom. Itcan be produced by three different techniques (Table 1),gamma ray processing, high energy electron called e-beamand X-ray processing. Gamma rays are mainly producedby a source of radionuclides, Cobalt 60 with a half life of5.27 years and Cesium 137 with a half life of 30.19 years.In the industry, the majority of facilities use the Cobalt60 because it has stronger gamma ray and because it isnot soluble in water (Ahn et al., 2006). Electron beamsare produced by commercial electron accelerators andtherefore can be switch off like all electrical apparatus.They can be directly used for small items such as grainsor to remove surface contamination because they have lim-ited penetration capacity. X-rays are produced when fast-

moving electrons slam into a metal object. If the targetused is tantalum or platinum, strong X-ray with an energysuperior to 1 MeV can be produced (Table 1). The US-FDA and the European Commission approved the use ofX-ray technology with a maximum energy of 5 MeV, andthen the FDA amended the maximum level to reach7.5 MeV in 2004. The technique offers the possibility ofprocessing packaged meat products in great quantities(Borsa, 2006) although it requires a high investment andmaintenance cost. Food irradiation facilities must bedesigned and constructed in order to ensure the controlof the radiological hazard for the personal and the environ-ment. Costly reinforced concrete walls must be builtaround the main source and the treatment area. Addition-ally, the operational costs are also high. In some countriesthe same amount of money can be spent on quality con-trols and in good hygiene practice.

The molecular bonds in the microbial DNA are themain target of irradiation but DNA and RNA synthesis,denaturation of enzymes and cell membrane alterationsmay also be affected. The absorbed dose, measured in grays(Gy). 1 Gy = J/kg = 100 rad, is considered the most impor-tant parameter but effectiveness of the treatment alsodepends on the sensitivity of the microorganims, the extrin-

116 T. Aymerich et al. / Meat Science 78 (2008) 114129

sic characteristic of the environment (pH, temperature) andthe intrinsic characteristics of the food (fat content, salt,additives, etc.). In general, viruses are the most resistantto irradiation, followed by spores and yeast. Molds andGram-positive vegetative bacteria are more resistant thanGram-negative. Low activity water and low temperaturepromote resistance while presence of oxygen enhances theirradiation action. Cross-adaptation to other stress as acidhas to be considered (Ahn et al., 2006; Borsa, 2006;Koutchma, 2006; Sommers, Fan, Handel, & Sokorai,2003).

In the food sector, irradiation is defined by two pro-cesses, radiation pasteurization (radurization), which refersto the inactivation of non-spore bacteria with a lowabsorbed dose requirement (110 kGy) and the sterilizationirradiation (radapperdization) to ensure the elimination ofClostridium botulinum. For the last one the dose required(European Commission, 2003a; Koutchma, 2006; McCle-ery & Rowe, 2002) is well above (between 40 and50 kGy) the one permitted for commercial food (10 kGy).A maximum dosage of 10 kGy represents a low amountof energy (equivalent to the one needed to raise water tem-perature 2.4 C); this is why the technology is considerednon-thermal, thus preserving the freshness, the nutritionalquality of the meat and meat products when comparingwith thermal methods (Ahn et al., 2006). During the radu-rization treatment an insignificant loss of thiamine (one ofthe most sensitive vitamins) is reported (Graham, Steven-son, & Steward, 1998) but changes in sensorial and colourcharacteristics of the product may occur. In aerobic condi-tions, brown or greenish colour of fresh meat may appearand in anaerobic packaging, an increase of the red colourhas been reported (Ahn et al., 2006; Brewer, 2004). On vac-uum packaged dry cured loins and dry cured ham, Carras-co, Tarrega, Ramrez, Mingoarranz, and Cava (2005) andCava, Tarrega, Ramrez, Mingoarranz, and Carrasco(2005), respectively, described an important colour changeon samples irradiated with a dose rate of 5 kGy. To solvethe problem, several techniques like pre-slaughter feedingof antioxidants to livestock, the addition of antioxidantsextract from rosemary and onions (Nan et al., 2007) andmodified gas atmosphere packaging have been suggested(Brewer, 2004). Oxidation of lipids may create free radicals(Giroux & Lacroix, 1998), breakdown of triglycerides may

Table 2Efficiency of irradiation in meat products

Microorganism Source

L. monocytogenes in RTE meat mealsa GammaE. coli (KCTC) in marinated beef rib GammaSalmonella spp. in rabbit meat GammaFBPb in cured dry ham E-beamFBPb in loinsFBPb in RTE meal mealsc Gamma

a Frankfurter, bologna pasta, ham and deli turkey meat.b E. coli O157:H7, L. monocytogenes, S. aureus, and Salmonella spp.c Frankfurter, beef cheeseburger and vegetarian cheeseburg.

form 2-alkylcyclobutanes (used as a marker for irradiationin EU) that has been reported to present potential healthrisks (Marchioni et al., 2004). Characteristic odoursregardless of the degree of lipid oxidation and off-odourfrom sulphur bridges proteins breakdown have also beenreported (Ahn & Lee, 2006; Ahn, Nam, Du, & Jo, 2001).

The efficiency of the irradiation in meat products andready to eat meals (RTE) has been proven and it has beenreported in a series of reviews and articles (Ahn et al., 2006;Farkas, 1998; Sommers, Fan, Niemira, & Rajkowski,2004). Irradiation may effectively control the presence ofall the main food-borne pathogens such as E. coliO157:H7, L. monocytogenes, S. aureus, Salmonella spp.(Table 2) and Trichinella spiralis, also yeast and mouldare effectively eliminated from meat and meat products.

2.2. High hydrostatic pressure

In high hydrostatic pressure (HHP) treatment, alsoknown as ultra high pressure (UHP) treatments or Highpressure processing (HPP), the packaged food is placedin the pressure vessel and submitted to water pressuresfrom 100 to 900 MPa. The pressure applied is isostaticallytransmitted (Pascals law and Le Chatellier principle) insidethe pressure vessel; the food is compressed independentlyof the product size and geometry because transmission ofpressure to the core is not mass/time dependent and thusthe process is minimized. A process of 500600 MPa maytake 2.5 min to charge 5 min for pressurization and 3 minto discharge. The treatment could also be considered anon-thermal process as the adiabatic heating is only 3 Cfor each 100 MPa, thus representing an increment of15 C for a 600 MPa (6000 bar, 87,000 psi) treatment.Commercial equipments with a capacity of 10300 l areavailable and can be purchased from Nicolas CorreaHyperbaric (Spain), Stanstead Fluid Power (UK) andAvure Technologies (USA).

Even if HHP has been recognized for microorganismsinactivation since Hite (1899), the first commercial foodproducts (jellies and jams) appeared in Japan in 1990.Nowadays, there are some companies all over the world(Japan, USA, Italy, Spain, Germany and Australia) usingthis technology in meat products. Commercial cooked

Dose rate for 5 log10 reduction Reference

2.453.75 kGy Sommers et al. (2004)3.0 kGy Jo et al. (2004)3.0 kGy Bard (2005)5.05.4 kGy Cava et al. (2005)

Carrasco et al. (2005)1.83.0 kGy Sommers and Boyd (2006)


ham, cured ham, some precooked meals with turkey anddelicatessen (sausage tapas), chicken and pork cuts, pre-cooked meals with poultry, cooked and cured ham, Parmaham, mortadella, bacon, salami and other smoked or notsmoked sausages are available in the market. Generally atreatment of 600 MPa during 210 min is considered.Although initial investment is high, the processing costhas been estimated on 14 eurocent/kg of product treatedat 600 MPa, including investment and operation costs(Anon., 2002). The technology is well accepted in Europeas an alternative technology. Baron et al. (1999) reporteda 67% of acceptability from consumers of three differentEuropean countries (France, Germany and United King-dom). As for production, on commercial equipment of300 l, a 4.51 cycles/h could be done and products treatedby HHP do not need to be labelled in USA.

As a consequence of the le Chatelier principle, HHPproduces denaturalization or modification of the proteins,inactivation of enzymes, changes in the substrateenzymeinteractions and in carbohydrates and fats (Butz & Tau-scher, 2002). The hydrophobic and electrostatic interac-tions are the most affected but not the hydrogen bondswhich stabilizes a-helical and b-pleated sheets (Heremans,2001). Thus, the nutritional value, vitamins and the major-ity of small substances responsible for the flavours of theproducts are kept. This is viewed as an important benefitfor the food industry (Hoover, Metrick, Papineau, Farkas,& Knorr, 1989; Smelt, 1998; Tellez, Ramrez, Perez, Vaz-quez, & Simal, 2001) since minimal modifications in thesensorial characteristics of the product are introduced,especially in cooked and cured meat products. Non-signif-icant changes have been observed in cured ham treated at450 MPa (Morales, Calzada, & Nunez, 2006) and in curedand cooked ham treated at 600 MPa during 6 min at 30 C(Garriga, Grebol, Aymerich, Monfort, & Hugas, 2004).Saccani, Parolari, Tanzi, and Rabbuti (2004) reported thata treatment of 600 MPa during 9 min did not affect the typ-ical maturated taste of dry cured ham but it changed colour(slight discoloration) and saltiness (enhanced perception),the effect being inversely related to the age of the ham.Moreover, colour changes due to oxidation of ferrous myo-globin and fat oxidation have also been reported in freshand marinated meat (Carlez, Rosec, Richard, & Cheftel,1993; Cheftel & Culioli, 1997; Hugas, Garriga, & Monfort,2002). Hugas, Garriga, and Monfort (2002) reported thatthe overall physico-chemical composition of marinatedbeef loin, cooked ham and dry cured ham was not signifi-cantly affected after a treatment of 600 MPa during10 min at 30 C The non-proteic nitrogen fraction and ami-noacid content were equivalent while only a small decreasein phosphate content on dry cured ham was detected. Fattyacid composition and cholesterol content was kept, only x6increased its stability in marinated beef loin and cholesteroloxidation was reduced by lowering the 7-ketocholesterollevels. Contents of vitamins from group B were not modi-fied. Mineral composition was similar, only a decrease inthe calcium content was observed on cooked ham and an

increase in the iron content of beef loin, probably due toa release form heme and non-heme complexes. Concerningthe bioavailability of nutrients, an increase in the solubilityof cytoplasmatic proteins was observed while the myofibr-illar fraction decreased, although not to the same extent ascooking procedures.

HHP kills or sublethally injures cells by probably a com-bination of factors thus affecting cell membrane, cell wall,proteins and enzymes and genetic mechanisms. Cell mem-brane is known to be the primary site of pressure damagewith consequent changes in the permeability of the cells,transport systems, loss of osmotic responsiveness and inca-pacity to keep DpH. Cells wall and changes in cell mor-phology are also affected and bud scares, nodes to thecell wall and separation of the cell wall from the membranehave been observed by Ritz, Tholozan, Federighi, and Pilet(2001) and Park, Sohn, Shin, and Lee (2001) with elec-tronic microscopy. Protein denaturalization and changesin the active centers have also been observed together withgenetic mechanisms such as replication and transcriptionthat are enzyme-mediated. DNA itself is highly stabledue to the a-helical is supported by hydrogen bonds. Con-densation of nuclear material and increasing contact ofDNA with endonucleases have also been reported (Benito,Ventoura, Casadei, Robinson, & Mackey, 1999; Chilton,Isaacs, Mackey, & Stenning, 1997; Manas & Mackey,2004; Smelt, Rijke, & Hayhurst, 1994; Wouters, Glaasker,& Smelt, 1998). The threshold of inactivation depends onthe type of microorganism and its growth phase, the pres-sure applied, the time of processing, the composition of thefood, temperature, pH and activity water (Tewari, Jayas, &Holley, 1999). Generally the Gram-negatives and cells ingrowth phase are more sensitive than Gram-positives andcells in stationary phase. Some microbial spores will needa treatment over 1000 MPa (Kalchayanand, Sikes, Dunne,& Ray, 1998). Eucariote vegetative forms from fungi andmolds are inactivated with pressure of 200300 MPa whiletheir spores need a 400 MPa treatment. High variability invirus resistance has been described being poliovirus one ofthe most resistants when compared to hepatitis A and rota-virus (Khadre & Yousef, 2002; Kingsley, Hoover, Papa-fragkou, & Richards, 2002). Rich nutrient media such asmeat reinforce the resistance of the microorganisms toHHP (Hoover et al., 1989). Carbohydrates, proteins andlipids have a protective effect (Simpson & Gilmour,1997), thus results from buffer systems could not be extrap-olated to food matrices. Patterson, Quinn, Simpson, andGilmour (1995) reported the different sensitivity of L. mon-ocytogenes and E. coli O157:H7 when treated in UHT milk,poultry meat and buffer systems. The same treatment couldreduce E. coli O157:H7 in 6 logCFU in buffer while only2.5 log in poultry meat and even less in milk. A low wateractivity protects microorganisms against pressure and evenat the same aw the solute is important, in glycerol they aremore sensitive than in mono-o-disaccharide while trehalosehas a protective effect (Smelt, 1998). Moreover the celldeath increases with pressure but does not follow a first


order kinetics and a tail of inactivation is sometimes pres-ent (Garriga, Aymerich, Costa, Monfort, & Hugas, 2002;Kalchayanand et al., 1998). These resistance or sublethallyinjured cells could be able to grow during storage (Chen &Hoover, 2003; Garriga, Aymerich, Costa et al., 2002; Patt-erson et al., 1995). Challenge test in real food matrices fol-lowed during the shelf-life of the product should be

0

4

8

12

0 15 30 45 60 75 90days

Lo

g C

FU

/g

a b

Fig. 2. Behaviour of Listeria monocytogenes during storage of sliced cooked hanot (NT) to a high hydrostatic treatment of 400 and 600 MPa.

Table 3Microbial inactivation by HHP in meat products

Target Product Initial countslog (CFU/g)

Reductionlog (CFU

FBPb Meat homogenate 67 Total inactreatment

C. freundii Minced beefmuscle

7 >5log aft

P. fluorescens

L. innocua

Total microflora Minced beefmuscle

6.8 >4log aft

E. coli O157:H7 Raw minced meat 5.9 5 log after

Mesophilesbacteria

MRPMc 7.3 >4log aft

L. monocytogenes Dry cured ham 2.7 Absence a(4 C)

Salmonella spp. Cooked ham 3.8 Absence a(4 C)

Aerobic totalcount

Marinated beefloin

6.5 >4.5 after

Dry cured ham 2.5 1.8 after 1

L. monocytogenes Cooked ham 2.6 1.9 after 4Salmonella spp. 3.0 2.4 after 8

L. monocytogenes Iberian ham 6.3 3.6 after 6

L. monocytogenes Sliced beef curedham

4.0 2 log after

Toxoplasma gondii

cystsGround porkmeat

Viable tissue cysts Non-viab

a Initial temperature are reported.b E. coli, Campylobacter jejuni, Pseudomonas aeruginosa, Salmonella Typhimc Mechanically recovered poultry meat.

recommended to assure the treatment is safe for any spe-cific product to be treated (Fig. 2).

In meat products, several studies have reported the anti-microbial effect of HHP and the results obtained are sum-marised in Table 3. For a pasteurization purpose thetreatment considered is generally in the range of 300600 MPa for a short period of time, from seconds to min-

0

4

8

12

0 15 30 45 60 75 90days

Lo

g C

FU

/g

HHP400

HHP600

NT 400

NT 600

m when stored at 6 C (a) and 1 C (b) and after being submitted (HHP) or

/g)Processa Reference

tivation after 400 MPa for 10 min;25 C

Shigehisa et al. (1991)

er treatment 300 MPa 10 min,20 C

Carlez et al. (1993)

200 MPa 20 min,20 C400 MPa 20 min,20 C

er 10 days (3 C) 450 MPa for 20 min;20 C

Carlez et al. (1994)

treatment 700 MPa for 1 min;15 C

Gola et al. (2000)

er 15 days (2 C) 450 MPa for 15 min;2 C

Yuste et al. (2001)

fter 120 days 600 MPa for 6 min;31 C

Hugas, Garriga, andMonfort (2002)

fter 120 days 600 MPa for 6 min;31 C

Garriga, Aymerich, andHugas (2002)

120 days (4 C) 600 MPa for 6 min;31 C

Garriga et al. (2004)

20 days (4 C)


Aymerich et al. (2005)4 days (6 C)


Morales et al. (2006)


Rubio et al. (2007)

le 300 MPa Lindsay et al. (2006)

urium, Yersinia enterocolitica.


utes, inactivating the vegetative pathogenic and spoilagemicroorganisms (>4 log units). For sterilization the rangeis over 600 MPa and combination with high temperatureis needed because some spores are even resistant to pres-sure over than 1000 MPa when temperature is not higherthan 4575 C (Cheftel, 1995). This strategy is now consid-ered to sterilize foods (Heinz & Knorr, 2001) and it is alsothe aim of several patents. Mayer (2000) reported in hispatent that a combined heat treatment (over 70 C) withhigh hydrostatic pressure (over 530 MPa) with pausesbetween two or more cycles was able to achieve a 12Dfor Cl. botulinum. The treatment is less severe than conven-tional retorting and higher quality, texture and retention ofnutrients is achieved (Master, Krebbers, Van den Berg, &Bartels, 2004).

Prions (bovine spongiform encephalopathy) are alsohighly resistant and a pressure treatment of 7001000MPa at high temperature 60 C 2 h (Fernandez-Garcaet al., 2004) was needed to reduce the survival rate overthe infected meat product by 47%. Also Cardone, Brown,Meyer, and Pocchiari (2006) reported a reduction on thelevel of infectivity of prions from 103 to 106 mean lethaldoses (LD50) per gram of tissue when using a combinedpressure temperature treatment while no autoclave noalcali no bleach had been effective.

The Scientific Committee on AESA (Spanish FoodSafety Agency) concluded that the technology may be usedfor hygienization procedures more than for sterilization ofthe meat and meat products. They considered a treatmentof 400500 MPa to be enough to obtain the FSO (foodsafety objective) in RTE-products but suggested that a hightreatment of 700800 MPa would be needed to obtain theFSO in fresh meat products. A higher temperature duringtreatment from 30 to 50 C could be useful to obtain theFSO. Moreover, the microbial resistance and the role ofbacterial stress must be addressed in order to optimizethe treatment and hold the robustness of the technologyinto legislation. Different stakeholders must interact toconvince consumers of their convenience with objectiveand unbiased data including negative aspects andlimitations.

2.3. Biopreservation and natural antimicrobials

In biopreservation, storage life is extended and safety isincreased by using natural or controlled microflora, mainlylactic acid bacteria (LAB) and/or their antimicrobial prod-ucts such as lactic acid, bacteriocins and others (Hugas,1998). LAB has a long history of safe use in foods as nat-ural microflora of meat, milk, vegetables and fish products.They can exert its antagonism through competition fornutrients and/or production of several antimicrobial sub-stances such as organic acids (lactic and acetic), carbondioxide, hydrogen peroxide, diacetyl, ethanol, and bacteri-ocins. They can be an alternative to chemical additives andact as extra hurdles for food preservation in meat fermen-tation, and in MAP refrigeration. They could be included

in the meat batter, sprayed onto the surface or addedthrough active packaging depending on the type of productto be applied. When they are applied as starter cultures,adjuncts of fermentation or bioprotective cultures, theirsuccess depends on the ability of the culture to grow andproduce the antibacterial factors on the food under thetechnological and physicochemical environment (tempera-ture, pH, ingredients, additives, water activity, etc.). More-over, in fresh meat they must be able to compete with theendogenous microflora. This approach offers and indirectway to apply antimicrobials and seems the most acceptedway for consumers and producers in fermented meat prod-ucts and in vacuum packed meats of short shelf-life wherehigh number of LAB do not affect sensorial characteristics.When the bioprotective starter is not competitive or mayaffect sensorial properties, antimicrobials may be addedas fermentation liquor or as purified substances. In the lat-ter case dosage is more precise but is limited by regulationson food additives.

Lactic acid and their salts have been extensively used inmeat industry to increase flavour and to extent shelf-life ofthe product. Their activity against Cl. botulinum, L. mono-cytogenes, S. aureus, Salmonella and E. coli O157:H7 havebeen reported (Aymerich, Jofre, Garriga, & Hugas, 2005;Glass et al., 2002; Porto et al., 2002; Shelef & Potluri,1995). In Europe their use is regulated by the Europeandirective 95/2/CE (European Parliament & of the Council,1995). In USA it is a recognized antilisterial agent and itsuse is regulated by the Federal Register (Food Safety &Inspection Service, 2000).

Bacteriocins produced by LAB are antimicrobial pep-tides generally heat stable, apparently hypoallergenic andreadily degraded by proteolytic enzymes in the humanintestinal tract. Although some bacteriocins have beentested in food, nisin remains the only commercial oneand the only one regulated as an additive by EC (althoughnot in meat products). They have a long story of safeuse and documented effectiveness against importantGram-positive food-borne pathogens and spoilage micro-organisms.

In fresh meat, nisin has been sprayed to sanitize the sur-face of red meat carcasses (Cutter & Siragusa, 1994), todecontaminate artificially contaminated pieces of raw pork(Murray & Richard, 1997). Combined with 2% of sodiumlactate to control S. aureus NMPR3 and Salmonella Ken-tucky AT1 in fresh pork sausages (Scannell, Hill, Buckley,& Arendt, 1997) and combined with 2% of sodium chlorideas antilisterial agent in minced raw buffalo meat (Pawar,Malik, Bhilegaonkar, & Barbuddhe, 2000). Pediocin hasalso been described as an antilisterial compound in turkeyslurries when combined with sodium acetate (0.30,5%)(Schlyter, Glass, Loeffelholz, Degnan, & Luchansky,1993). In minced meat, the bioprotective effect of severalLAB and their bacteriocins such as L. sakei Lb706 andL. sakei CTC494 have been shown as effective antilisterialagents (Hugas, Pages, Garriga, & Monfort, 1998; Schillin-ger, Kaya, & Lucke, 1991).


Their use as natural biopreservatives to overcome thepostprocessing contamination of meat products (slicing,packaging, peeling and handling) has been reported. Sev-eral bacteriocins and their producers have demonstratedtheir antilisterial effect on cooked meat products. SakacinK and its producer on cooked ham and frankfurter sau-sages (Hugas et al., 1998), sakacin P and its producer invacuum-packed bologna sausages (Krockel, 1997), ente-rocins in cooked ham, pate and frankfurter sausages(Aymerich et al., 2000), nisin in frankfurter sausages andautoclaved tenderloin pork meat (Fang & Lin, 1994;Hugas, Garriga, Aymerich, & Monfort, 2002), pediocinin frankfurter sausages and sliced cooked sausages (Hugas,Garriga, Aymerich et al., 2002; Mattila, Saris, & Tyoppo-nen, 2003) and leucocins and its producer strain (Leuconos-toc carnosum 4010) in pork saveloys (Jacobsen, Budde, &Koch, 2003).

In fermented sausages, where LAB largely dominates,their biopreservative effects have also been reported.When several bacteriocinogenic starter cultures wheretested in two different technologies (with and withoutnitrite), L. sakei CTC 494 turned to be the most efficientin the first, while L. sakei Lb706 and L. curvatusLTH1174 in the second. Pediocin have been reported asan extra hurdle in fermented sausages (Foegeding, Tho-mas, Pilkington, & Klaenhammer, 1992), turkey summersausages (Luchansky et al., 1992), chicken summer sau-sages (Baccus-Taylor, Glass, Luchansky, & Maurer,1993). In salami, Lahti, Johansson, Honkanen-Buzalski,Hill, and Nurmi (2001) described the antilisterial effectof a composed starter culture of S. xylosus DD-34 andthe bacteriocinogenic strains Pediococcus acidilactici PA-2 and Lactobacillus bavaricus MI401. Enterocins A andB (Aymerich et al., 2000), CCM4231 (Laukova, Czikkova,Laczkova, & Turek, 1999; Laukova, Turek, Marekova, &Nagy, 2003), enterocins 416K1 (Sabia, de Niederhausern,Messi, Manicardi, & Bondi, 2003), enterocin AS-48 (Ana-nou et al., 2005) or Enterococcus faecium RZS C5 (Cal-lewaert, Hugas, & De Vuyst, 2000) Enterococcuscasseliflavus IM416K1 (Sabia et al., 2003). Also Gill andHolley (2000) reported the effect of lysozyme when com-bined with nisin and EDTA, as an effective agent to con-

Table 4Combined preservation treatments including antimicrobials agents and HHP

Antimicrobials Process Comments

Nisin HHP at 350 MPa Shelf-life of mechanically recover30 days at 2 C

Sakacin HHP at 400 MPa L. monocytogenes in meat homogdays at 4 C.Enterocins A and B

Pediocin

Pediocin(ALTA 2351)

Irradiation2.3 kGy

Inhibition of L. monocytogenes inor 10 C

Nisin HHP at 400 MPa Absence of Salmonella achievedPotassium lactate HHP at 400 MPa Inhibition of L. monocytogenes in

6 C

trol growth of spoilage and safety bacteria in cured meatproducts.

In general, antimicrobials provide an excellent opportu-nity to incorporate into a combined preservation system.Synergistic effects with HHP have been reported with anti-microbials, low pH, carbon dioxide, organic acids and tem-perature (Table 4). The effect of lactate, low temperaturestorage and HHP treatment on the inactivation of L. mon-ocytogenes is shown in Fig. 3. Also the effectiveness ofselected starter cultures and high hydrostatic pressure(400 MPa) after ripening was evaluated by Garriga et al.(2005). Starter cultures were able to control the growthof L. monocytogenes, Enterobacteriaceae, Enterococcusand the biogenic amine content. Salmonella spp. countsdecreased significantly during ripening independently ofthe starter culture but the HHP was necessary to ensureabsence of Salmonella in final products.

There are already a few cultures in the market intro-duced as starter or bioprotective culture with the aim ofcontributing to microbiological safety. Bactoferm F-Lcfrom Christian Hansen (Hoershom, Denmark) has beenpatented as an antilisterial culture in fermented sausages.It is a mixed culture of Pd. acidilactici and L. curvatus pro-ducing pediocin and sakacin A, respectively. They alsooffer other bioprotective cultures for vacuum packed andMAP meat products containing L. sakei (B-2) and Lc. car-nosum 4010 (B-SF-43). Danisco (Copenhaguen. Denmark)has a combined culture composed of Lactobacillus planta-rum and S. carnosus as an antilisterial culture in sliceableor spreadable sausages and for cooked ham (ALCMix1)and two more cultures (COX1 and XPA1) for minced meatand raw sausages either for boiling or frying.

ALTA 2351 and Fargo 23 from Quest International(B.V., The Netherlands) are natural food ingredients pro-duced through a fermentation process of a bacteriocino-genic Pd. acidilactici strain with antilisterial activity. Theproducts are approved in the United States and have beenintroduced in the market as a shelf-life extender in a greatvariety of meat products such as raw sausages, frankfurt-ers, hamburgers and MAP cooked ham. Today nisin isthe only bacteriocin commercially available and acceptedin the positive list of food additives (E234) (European

in meat products

Reference

ed poultry meat was extended during Yuste et al. (1998)

enates was kept

0

1

2

3

4

5

6

7

8

9

10

0 20 40 60 80

Days

Lo

g C

FU

/g

C6

C1

L6

L1

C6 HHP

C1 HHP

L6 HHP

L1 HHP

Fig. 3. Antilisterial effect of high hydrostatic pressure and lactate salts on spiked sliced cooked ham stored at two different refrigeration temperatures 6and 1 C: Control samples (C6 & C1); samples with lactate (L6 & L1); samples treated with HHP (C6 HHP & C1 HHP) samples with lactate and HHP (L6HHP & L1 HHP).


Parliament & of the Council, 1995), although its use inmeat products is not regulated. Danisco (formerly Applinand Barret) and Christian Hansen produces Nisaplinand Chrisin, respectively, they are both produced froma fermentation process done by selected strains of Lacto-coccus lactis subspecies lactis and have the same percentageof active compound, 2.5%. The use of pediocin PA-1 is pat-ented by Marugg, Ledeboer, Vandenbergh, and Henderson(1991, EP0493779A1) and enterocin A has a spanish patentdeveloped by Hugas, Garriga, Monfort, and Ylla (1991, ES2 068 157). LAB are recognized as safe on the experience ofsafe use for USA Food and Drug Administration (FDA)and the European Commission proposed the term qualifiedpresumption of safety (QPS) for microorganisms with ahistory of safe use (European Commission, 2003b; Euro-pean Food Safety Authority, 2005).

2.4. Active packaging

In the last decade new packaging systems have contrib-uted to extend the shelf-life of products. At first MAP,defined as the enclosure of food in gas barrier materialwhere the gaseous environment has been changed, wasused. The optimal atmosphere depends on parameters suchas pH, water activity, fat content and type of fat. Althoughit must be considered that high concentrations of CO2could cause collapse of the packaging and increase the lossdripping due to its solubilization in water and fat, espe-cially in foods with high amount of unsaturated fat (Dev-lieghere, Debevere, & Van Impe, 1998).

Active packaging is an innovative concept that could bedefined as a packaging system where the pack, the productand the environment interacts and change the condition ofpacked food, extending the shelf life and improving thefood safety or the sensorial properties of the product thuspreserving its quality (European Commission, 2004; Sup-pakul, Miltz, Sonneveld, & Bigger, 2003; Vermeiren, Dev-

lieghere, & Debevere, 2002). In this system the microbialsubstance would gradually migrate from the pack (con-tainer) to the food through diffusion and partitioning orrelease through evaporation in the headspace during stor-age and distribution, thus being able to reduce the post-processing contaminations in the surface of the ready-to-eat products (Han, 2005). Adhesion on packaging supportand the release (desorption) being critical for efficiency.Moreover, the concentration of the antimicrobial in foodcould be reduced when compared to spraying, immersionor direct addition to the initial meat mixture and interac-tion/inhibition with food constituents could be avoided(Coma, 2006). Principal active packaging systems includeoxygen scavengers (absorb oxygen), control of CO2 or eth-ylene concentration and generation, ethanol and antioxi-dants releasers, moisture absorption or desiccants andantimicrobial systems to control the growth of severalmicroorganisms (Gennadios, Hanna, & Kurth, 1997; Ver-meiren, Devlieghere, Van Beest, de Kruijf, & Debevere,1999). Some of them are commercially available, as shownin Table 5. The most applied active packaging systems areoxygen scavengers and/or CO2 generators which are usedto control oxidation of foods and with moisture removersto prevent spoilage by aerobic bacteria and molds. Activepackaging with a wide spectra of antimicrobials such aschlorine dioxide, silver substituted zeolite, triclosan(2,4,4 0-trichloro-2 0-hydroxydiphenyl-ether) are also avail-able (Quintavalla & Vicini, 2002). GRAS macromoleculessuch as chitosan with film-forming properties have alsoexhibited natural antimicrobial properties against fungi,yeasts and bacteria (Coma et al., 2002; Ouattara, Simard,Piette, Begin, & Holley, 2000).

One of the most promising fields is the incorporation ofantimicrobials such as bacteriocins and plants extracts tothe active packaging and their association to biodegradablepackaging such as alginate, zein (natural) or synthetic poly-vinil alcohol (PVA) in order to reduce wastes and being

Table 5Active packaging systems and their biological effects

Type of active packaging Enterprise Biological effect

Oxygen scavenger and CO2 generators Ageless-Mitsubishi, Japan Aerobic spoilageStanda Industry, FranceMultisorb Tech., USABioka Ltd., FinlandSouthCorp., Australia

Chlorine dioxide Bernard Technologies, USA Bacteria, fungi, spores and viruses

Silver substituted zeolite Monroe Engineering Products, USA Bacteria, moulds and yeastsJapan

Triclosan Microban, USA Bacteria, moulds and yeastsChitosan Bacteria (Gram-positive more than

Gram-negatives), moulds and yeastsBacteriocins (pediocin) Viskase Co. (patent) Related bacterial species


environmental friendly. Skandamis and Nychas (2002) andOussalah, Caillet, Salmieri, Saucier, and Lacroix (2006)reported the antimicrobial effect of essential oils, althoughflavour modifications are limiting their use in meat prod-ucts. Some organic acids and theirs salts together with bac-teriocins from LAB, mainly nisin, have been applied toactive packaging of meat products with or without biode-gradable, edible films (Table 6). Application of bacteriocinsin active packaging could be an alternative to increase theefficiency of these natural antimicrobials which activitycould be reduced by interaction with the food matrixes.

Four basic categories of antimicrobial films could bedefined (Cooksey, 2001):

1. Incorporation of the antimicrobial substances into asachet connected to the package from which the bioac-tive substance is released during further storage.

2. Direct incorporation of the antimicrobial into the pack-aging film. When applied in a hot extrusion material,thermoresistant and shearing resistant of the antimicro-bial must be considered.

Table 6Natural antimicrobials and their use in active packaging

Target Product Antimicrobial

L. monocytogenes Beef Alginate coating, with orga

Brochotrix

thermosphacta

Beef Nisin in meat binding, syste

L. monocytogenes Bee steak Nisin impregnated, packageSerratia liquefaciens Cooked ham Chitosan, acetic and lauric

L. innocua Pork ham Nisin and Lacticin 3147, inS. aureus

L. monocytogenes Hamburgers Bacteriocin 32Y (Lactobacilindustrial film

L. monocytogenes Model turkeyfrankfurters

Nisin and sodium diacetate

3. Coating of the packaging with a material that acts as acarrier for the additive. The substance will not be sub-mitted to high temperature or shearing forces, moreoverit could be applied as the later step.

4. Antimicrobial macromolecules with film formingproperties.

3. Thermal alternative technologies

3.1. High frequency heating

High frequency energy includes microwave and radio-frequency energy and belongs to the non-ionising radia-tions. Microwaves and radiofrequency have been used forcooking, drying, blanching, tempering, pasteurising andthawing (Decareau, 1985). The authorized frequencies(Institute of Food Technologists, 2000) are included inthe ISM (Industrial, Science and Medicine) bands wherewe have 13.56, 27.12 and 40.68 MHz for the radiofre-quency range and 433, 915, 2450 and 5800 MHz for themicrowave range.

LOG reduction(CFU/g)

Reference

nic acids 1.80 (7 days) Siragusa and Dickson(1992)

m (Fibrimex) 4.8 (7 days) Cutter and Siragusa(1998)

d 3 (21 days) Schobitz et al. (1999)acid 4.13 logCFU/cm2

(21 days)Ouattara et al. (2000)

cellulose packaging 2 and 2.8,respectively

Scannell et al. (2000)

lus curvatus), on Up to 1 (1 day) Mauriello et al. (2004)

Up to 6 (28 days) Lungu and Johnson(2005)


There are a great variety of designs for microwave ovensbut all of them share the same principles with a powersource called magnetron and a waveguide to bring the radi-ation to a cavity where the product is located. A magnetronhas a power between 300 and 3000 W and for industrialequipment various magnetrons are used to increase theglobal power. Most of the ovens have reflecting cavity wallsand produce an infinity of modes which produce a multi-mode cavity. A mono-mode or single-mode cavity whereonly one mode of propagation is permitted is a more effi-cient microwave system. The system has a better energyefficiency than the multimode one but the cavity andwaveguides have to be designed geometrically around theproduct to be processed. A radiofrequency oven is anequipment with a generator coupled with a pair of elec-trodes, called the RF applicator. For industrial equipmentthere are two different applicators on the market, the firstcalled conventional RF equipment where the electrodesand generator are closely connected and the 50 X RFequipment where the electrodes and the generator are con-nected with a high power coaxial cable and controlled by amatching box. The two systems have advantages and dis-advantages and the use of one or the other will dependof the applications.

The inactivation of microorganism with high frequencyheating is produced by heat and the alternative non-ther-mal effect of microwave has not been confirmed yet (Insti-tute of Food Technologists, 2000). Several works have beendone to understand the role of different parameters duringhigh frequency heating, such as geometry and composition,dielectric properties and thermal properties of food prod-uct (Ryynamen & Ohlsson, 1996; Wappling-Raaholt &Ohlsson, 2005). Meat products are complex food systems,mainly due to the presence of fat and proteins and a vari-able number of additives. Moisture and salt content areconsidered to be key factors in accounting for the dielectricproperties of foods. However, in meat products, other foodcomponents with low dielectric values should not beneglected due to their sudden temperature rise undermicrowave heating. Studies have shown that increase infat content results in decrease in dielectric constant and loss

Table 7Efficiency of the high frequency treatment on the decontamination of differen

Target Product log reduction (CFU

Enterococcus Vacuum package ham >4.0Streptococcus

Salmonella Fresh chicken thighs 6.4Enteritidis

E. coli O157:H7 Chicken portions 6.0

Total flora Meat balls 2E. coli O157:H7 >4S. aureus >3.5

L. monocytogenes Packaged beef frankfurters 0.94 log(CFU/pk)/

a Note: The power indicated correspond to the maximum power of the oven

factor (Gunasekaran, Mallikarjunan, Eifert, & Summer,2005). However, several recent experiments (Jeong et al.,2006; Picouet, Fernandez, Serra, Sunol, & Arnau, 2007)have shown that fat accelerates the microwave heating rateand increases the maximum temperature achieved.

High frequency heating, especially in the microwavebands, can deliver a high temperature in a very short timeresulting in nutritional and sensorial advantages (Orsat &Raghavan, 2005) over a more traditional technology likethe autoclave one. Moreover, as summarised in Table 7,the inactivation effect of high frequency has been demon-strated. Paterson, Cranston, and Loh (1995) obtained a102 CFU/cm2 reductions in bacterial numbers with amicrowave treatment of 2450 MHz. Houben, Schoenmak-ers, van Putten, van Roon, and Krol (1991) have describedthe on-line pasteurization of sausages in a radiofrequencytunnel of 27.12 MHz frequency with a power between 10and 25 kW and speed of 120 kg/h. The temperature rosefrom 15 to 80 C in the centre of the sausage in 2 min.On foie gras products, an acceptable pasteurization couldbe obtained with a gain of time of 50% and better organo-leptic qualities with microwave treatment in comparisonwith traditional one (Massoubre, 2003). Additionally, Yil-maz, Arici, and Gumus (2005) have recently compared theeffect of different cooking processes (microwave and con-ventional oven) on meat balls inoculated with E. coliO157:H7 and S. aureus and higher inactivation rates havebeen observed (see Fig. 4). These facts together with thepossibility of offering continuous systems are seen asadvantages in the food processing industry although thereare still non-uniformity problems which must be solved.Microwave heating and also radiofrequency heating tendsto create hot and cold spots that would depend on theunderstanding of parameters such as geometry, composi-tion, dielectric properties and packaging. A way to controlthe hot and cold spots generation and therefore accomplishwith the concept of quick efficient decontamination method(Lacroix, Orsat, Nattress, & Raghavam, 2000), is the use ofvapour inserted in the oven cavity to distribute the heatand packaging with valves. These designs require welltrained staff and a good maintenance and must be done

t meat products

/g) Process Reference

27.12 MHz; 600 W; 600 s Orsat et al. (2004)

2450 MHz; 800 Wa; 95 s Pucciarelli and Benassi (2005)

2450 MHz; 650 Wa; 35 s Apostolou et al. (2005)

2450 MHz; 800 Wa; 300 s Yilmaz et al. (2005)

min 2450 MHz; 550 W; 360 s Huang and Sites (2007)

.

0

1

2

3

4

5

6

7

Control Conventional Oven Microwave

Lo

g c

fu/g

Total bacteriaE. coli O157:H7S. aureus

Fig. 4. Effect of different cooking methods on meat ball inoculated withE. coli O157:H7 and S. aureus. Microwave process was 5 min treatment atmax power (800 W) with a 2450 MHz oven. The conventional process wasdone with an oven at 160 C during 6 min. ND for none detected. Dataextracted from Yilmaz et al. (2005).


in collaboration with microwave and radiofrequency man-ufacturers and food technical centres with expertise in thesubject.

3.2. Ohmic heating

Ohmic heating process uses the resistance of liquid orsolid products to convert the electric energy into heat (Butz& Tauscher, 2001). The rate of heat is directly proportionalto the intensity of the electric field and to the electric con-ductivity of the sample (Ruan, Ye, Chen, & Doona, 2004).Although, the ohmic heat technology has proved to be asuccessful technology to process liquids, the applicationto solid meat products has not yet found industrial applica-tion (Piette et al., 2004) and it is at the level of appliedresearch field.

The main inactivation mechanism in ohmic heatingseems to be the thermal one, although some reports indi-cates that other process such as a mild electroporationmechanism may occur (Institute of Food Technologists,2000; Ruan et al., 2004). There are only few studies report-ing the inactivation effect of ohmic heating on meat basedproduct. (Piette et al., 2004) reported the inactivation ofEnterococcus faecalis in bologna sausages processed in anenclosed experimental cooking unit. With this batch systemthey were able to have a reduction of 9.06 log10 CFU/g witha core temperature of 80 C and a total process time of13.78 min. When the core temperature was reduced to70 C, the total process time to reach a 9.06 log10 CFU/gvary from 31.44 to 40.36 min depending on the heatingrate. With a more industrial approach, Zuber (1999) pre-sented the results of the sterilization of a chilli con carneRTE meal with ohmic heating. The comparison with a con-ventional heating treatment gave better nutritional andsensorial qualities while maintaining the safety of the prod-uct and reducing the treatment time.

The energy conversion is very efficient as 90% of theenergy can be converted in heat (Ruan et al., 2004). Mostof the disadvantages of the technology are related to theelectrical nature of the food treated. Compounds with poorconductivity, especially the fat in meat products, do notgenerate heat as the same rate than muscle thus creatinga cold spot (Shirsat, Lyng, Brunton, & McKenna, 2004).In fact, conductivity of the products has to be in the0.0110 S/min range (Piette et al., 2004). Geometry factorssuch as the size of the piece of meat are important factorsand limit the use of the technology. For the pump able sys-tem, Zuber (1999) recommends a size of 2 cm. Also othercomposition parameters such as the acidity may affect thebest working conditions of the electrodes and reduce theefficiency of the system. Therefore product compositionhas to be adapted to the technology Zuber (1999).

3.3. Steam pasteurization

Steam pasteurization process consists in exposing meatcarcasses and meat product to water steam at 8297 Cinside chamber at atmospheric pressure during 612 s.Normally, the treatment includes the water removal, thesteam pasteurization and a rapid chilling. In some equip-ment the steam can be combined with pressure to enhancethe efficiency of the treatment. The Industrial process wasdeveloped in the US and the steam-pasteurization treat-ment of carcasses was approved by the FDA in 1995 forthe whole carcasses and parts of carcasses that are to befurther processed.

The efficiency of the treatment was exposed in a series ofarticles; Nutsch et al. (1998) reported a reduction of1.0 logCFU/cm2 of the total viable count after a treatmentof 6.5 s at 82.2 C on beef carcasses. Retzlaff et al. (2004)had a significant reduction (>1.0 logCFU/cm2) of E. coliO157:H7, Salmonella Typhimurium, and Listeria innocuain beef carcass with a 93.3 C steam treatment during morethan 6 s. Recently, Trivedi, Reynolds, and Chen (2007)show a reduction of 4.38 logCFU/cm2 on pork skin inocu-lated by Listeria monocytogenes, using commercial steamcleaner during 30 s.

On meat products and meat pieces, laboratory appara-tus were used and results have been only reported atresearch level. Avens et al. (2002) present a reduction of1.04 logCFU/cm2 of aerobic microbes in chicken carcassskin with a steam system at 96.7 C during 12 s. McCann,Sheridan, McDowell, and Blair (2006) show a reduction of2.4 logCFU/cm2 and 1.5 logCFU/cm2 for, respectively,E. coli O157:H7 and Salmonella Typhimurium in porkpiece for a steam treatment of 83 C during 15 s.

The technology has the advantage to provide a continu-ous and cheap solution to decontaminate small and largepieces of meat product in a very short time. Although foras noted McCann et al. (2006) and others a prolongedtreatment superior to 10 s give a cooked appearances tothe sample. In carcasses this limiting factor can be over-come leaving the skin. Another disadvantage of the tech-


nology is the homogeneity of the temperature of the steamhas to be carefully checked with a continuous monitoringsystem to ensure that the entire surface, especially the neck,is correctly treated (Nutsch et al., 1998).

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Decontamination technologies for meat productsIntroductionNon-thermal alternative technologiesIrradiationHigh hydrostatic pressureBiopreservation and natural antimicrobialsActive packagingThermal alternative technologiesHigh frequency heatingOhmic heatingSteam pasteurizationReferences

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Decontamination technologies for meat products