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Viewpoint Implications of nanotechnology for the agri-food industry: Opportunities, benefits and risks Caroline E. Handford a , Moira Dean a , Maeve Henchion b , Michelle Spence a , Christopher T. Elliott a and Katrina Campbell a, * a Institute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, David Keir Building, Stranmillis Road, Belfast BT9 5AG, UK (Tel.: D44 (0) 28 90976535; fax: D44 (0) 28 90976513; e-mail: [email protected]) b Teagasc, Food Research Centre, Ashtown, Dublin 15, Ireland Nanotechnology has emerged as a technological advancement that could develop and transform the entire agri-food sector, with the potential to increase agricultural productivity, food se- curity and economic growth for industries. Though as still a relatively new concept there are concerns over its safety, regu- lation and acceptance by the industry and consumers. This re- view set out to address the implications of nanotechnology for the agri-food industry by examining the potential benefits, risks and opportunities. Existing scientific gaps in knowledge are believed to be a prohibitive factor in addition to uncertainties in the level of awareness and attitudes towards the use of nanotechnology by the industry. Introduction Nanotechnology is a multidisciplinary field that covers a vast range of processes, materials, and applications encom- passing physical, chemical, biological, engineering and electronic sciences. It focuses on the characterisation, fabri- cation and manipulation of substances at sizes in the nano- scale range, approximately between 1 and 100 nm. The smaller particle size, in combination with an increased sur- face area, exhibits unique and novel properties thus creating vast potential for applications (EFSA, 2009; Rashidi & Khosravi-Darani, 2011; Weiss, Takhistov, & McClements, 2006). A nanomaterial is defined as any material that has one or more dimensions in the nanoscale range, while a nanoparticle is a discrete entity that has all three dimen- sions in the nanoscale (Food and Agricultural Organisation of the United Nations (FAO)/World Health Organisation (WHO), 2010). Nanomaterials and nanopar- ticles can encompass the following nanoforms, which derive their names from their individual shapes and dimen- sions, i.e. nanotubes, nanofibres, nanorods, nanofilms, nanolayers, nanocoatings, nanosheets (Cushen, Kerry, Morris, Cruz-Romero, & Cummins, 2012). Nanotechnology has already been used in construction materials for floors, walls, and machines, new devices and techniques in electronics, cosmetics, sporting equip- ment, wastewater treatment, medicine, and more recently in agriculture, and the food industry (Doyle, 2006). Howev- er, the implications of nanotechnology in the agri-food sector can be far reaching. Nanomaterials are naturally occurring in many plant and animal products, including the major constituents of milk (i.e. casein micelles, whey proteins, fat globules and lactose), as well as the fibrous structures in fish and meat, the crystalline structures in innate starches, and the molecular structure of cellulose fi- brils in plant cells (Magnuson, Jonaitis, & Card, 2011; Morris, 2011). Engineered nanomaterials, for a variety of agri-food applications such as food additives, flavourings, novel foods, food packaging, feed additives and pesticides, are being developed. For food applications, nanotechnology can be applied by two different approaches, either from the “top-down” or by the “bottom up” (Ravichandran, 2010). The top down approach involves a physical or chemical process of breaking down larger particles of food matter into smaller particles of nanometres in dimension (Cushen et al., 2012). Grinding or milling are examples of mechanisms used to produce such nanomaterials. Dry * Corresponding author. http://dx.doi.org/10.1016/j.tifs.2014.09.007 0924-2244/Ó 2014 Elsevier Ltd. All rights reserved. Trends in Food Science & Technology 40 (2014) 226e241

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ViewpointImplicationsofnanotechnologyfortheagri-foodindustry:Opportunities,benetsandrisksCarolineE.Handforda,MoiraDeana,MaeveHenchionb,MichelleSpencea,ChristopherT.ElliottaandKatrinaCampbella,*aInstituteforGlobalFoodSecurity,SchoolofBiological Sciences, Queens University Belfast, DavidKeirBuilding,StranmillisRoad,BelfastBT95AG,UK(Tel.:D44(0)2890976535;fax:D44(0)2890976513;e-mail:[email protected])bTeagasc, Food Research Centre, Ashtown, Dublin 15,IrelandNanotechnology has emerged as a technological advancementthat coulddevelopandtransformtheentireagri-foodsector,with the potential to increase agricultural productivity, food se-curityandeconomicgrowthfor industries. Thoughasstill arelatively new concept there are concerns over its safety, regu-lation and acceptance by the industry and consumers. This re-view set out to address the implications of nanotechnology forthe agri-food industry by examining the potential benets, risksandopportunities. Existingscienticgaps inknowledgearebelieved tobe aprohibitive factorin addition to uncertaintiesinthe level of awareness andattitudes towards the use ofnanotechnologybytheindustry.IntroductionNanotechnologyis amultidisciplinaryeldthat covers avast range of processes, materials, and applications encom-passing physical, chemical, biological, engineering andelectronic sciences. It focuses on the characterisation, fabri-cation and manipulation of substances at sizes in the nano-scale range, approximatelybetween1and100nm. Thesmaller particle size, in combination with an increased sur-face area, exhibits unique and novel properties thus creatingvast potential for applications (EFSA, 2009; Rashidi &Khosravi-Darani, 2011; Weiss, Takhistov, &McClements,2006). Ananomaterial isdenedasanymaterial that hasoneor moredimensions inthenanoscalerange, whileananoparticleisadiscreteentitythat hasall threedimen-sions in the nanoscale (Food and AgriculturalOrganisationof the UnitedNations (FAO)/WorldHealthOrganisation(WHO), 2010). Nanomaterialsandnanopar-ticles can encompass the following nanoforms, whichderive their names from their individual shapes and dimen-sions, i.e. nanotubes, nanobres, nanorods, nanolms,nanolayers, nanocoatings, nanosheets (Cushen, Kerry,Morris,Cruz-Romero,&Cummins,2012).Nanotechnologyhasalreadybeenusedinconstructionmaterials for oors, walls, and machines, newdevicesandtechniques inelectronics, cosmetics, sportingequip-ment, wastewater treatment, medicine, andmorerecentlyin agriculture, and the food industry (Doyle, 2006). Howev-er, the implications of nanotechnology in the agri-foodsector can be far reaching. Nanomaterials are naturallyoccurringinmanyplant and animal products, includingthemajorconstituentsofmilk(i.e. caseinmicelles, wheyproteins, fat globules andlactose), as well as thebrousstructures in sh and meat, the crystalline structures ininnatestarches,andthemolecularstructureofcellulose-brils in plant cells (Magnuson, Jonaitis, &Card, 2011;Morris, 2011). Engineerednanomaterials, for avarietyofagri-foodapplicationssuchasfoodadditives, avourings,novel foods, food packaging, feed additives and pesticides,are being developed. For food applications, nanotechnologycan be applied by two different approaches, either from thetop-downorbythebottomup(Ravichandran, 2010).Thetopdownapproachinvolves aphysical or chemicalprocess of breakingdownlarger particles of foodmatterinto smaller particles of nanometres in dimension(Cushenet al., 2012). Grindingor millingare examplesof mechanisms usedtoproducesuchnanomaterials. Dry * Correspondingauthor.http://dx.doi.org/10.1016/j.tifs.2014.09.0070924-2244/2014ElsevierLtd.Allrightsreserved.TrendsinFoodScience&Technology40(2014)226e241millinghasbeenusedfor makinghighwater-bindingca-pacity wheat our and has successfullybeenappliedtogreen tea powder to enhance its antioxidant activity(Ravichandran, 2010). For green tea powder, this techniqueisusedtoreducethepowdersizeto1000nm, andsothehighratioofnutrientdigestionandabsorptionleadstoanincreaseintheactivityof anoxygen-eliminatingenzyme(Ravichandran, 2010). Homogenization is an alternativetopdownsizereductionprocesswhichappliespressuretoreducethesizeoffatglobules.Thismechanismisusedinthe dairyindustryworldwide toaddress milkseparationandbenetconsumers(Cushenetal., 2012). Bycompari-son, the bottom up approach involves manipulating individ-ual atomsandmoleculesintonanostructures(JosephandMorrison,2006).Nanostructuresarecomprisedofdiscretefunctional parts, either insideoronthesurface, ofwhichone or more are in the nanoscale range (FAO/WHO,2010). Thebottomupapproachcancreatemorecomplexmolecular structures of biological compounds. Methodsappliedinthebottomupapproachincludecrystallisation,layer-by-layer deposition and self-assembly (Cushenet al., 2012). For instance, theorganisationof caseinmi-celles or starch and the folding of globular proteins and pro-tein aggregates are self-assembly structures which formstableentities(Ravichandran,2010).Nanotechnology has emerged as the technologicaladvancement to develop and transformthe entire agri-foodsector,withthepotentialtoincreaseglobalfoodpro-duction, inadditiontothe nutritional value, qualityandsafety of food (Mousavi &Rezaei, 2011). Applicationsmaybeclassiedasnano-inside(i.e. inthefoodproductas inprimaryproductionor foodprocessing) andnano-outside (i.e. food packaging) (Henchion et al., 2013). Nano-sensors and nano-based smart delivery systems are some oftheapplicationsofnanotechnologythat arecurrentlyem-ployed in the agricultural industry to aid with combating vi-rusesandothercroppathogens, aswell astoincreasetheefciency of agrochemicals at lower dosage rates(Mousavi&Rezaei, 2011). Nanotechnologyoffersseveralperspectives for food applications due to the greater surfacearea of nanoparticles per mass unit making them more bio-logicallyactive thanlarger sizedparticles. For instance,nanoparticlescan be used as bioactive compoundsin func-tional foods (Ezhilarasi, Karthik, Chhanwal, &Anandharamakrishnan, 2013). Bioactive compounds arehealth-promotingingredients that canbe foundnaturallyin foods such as polyphenols, phytosterols, phytoestrogens,vitamins, minerals, fatty acids probiotics and prebiotics.These compounds exert physiological effects that mightcauseariskreductionof certainchronicdiseases linkedto oxidative stress, such as cardiovascular disease andvariousformsof cancer (Chen, Remondetto, &Subirade,2006). Nanosizingcangreatlyimprove the properties ofbioactive compounds such as delivery properties, solubility,targetability, and efcient absorption through cells, andprolonged compound residence times in the gastrointestinaltract (Ezhilarasi et al., 2013). Withregardstofoodpack-aging, nanotechnologycanincreaseproduct shelf lifebyusingpackaging with antimicrobial properties to protectfoodagainst pathogens(Duran&Marcato, 2013). Withinthefoodindustry, nanotechnologyhasshowna widerangeofnovel applicationsincludingtheuseofnanoemulsions,nanocomposites, nanocarriers (nanocapsules) andnanol-tration, in addition to the development of smart packaging,nanosensors and nanobiosensors for quality control andfoodsafety(Rashidi&Khosravi-Darani,2011).Applicationofnanotechnologyintheagri-foodsectorisstillarelativelynewconcept; themainreasonsforitslateincorporationaremainlyduetoissuesrelatingtoproductlabelling, potential consumer health risks, and a lack of unify-ing regulations and guidelines onnanotechnologygover-nance(Coles &Frewer, 2013). Nevertheless, it is widelyrecognised by many countries worldwide that nanotech-nologywill bringsignicant benets, andresearchinthisarea is attracting large scale investments by leading food com-panies, support fromacademic science, and increasinggovernmental nancial investment andconceptual backing(FSAI, 2008; Gruere, 2012; Momin, Jayakumar, &Prajapati, 2013). According to the United States Departmentof Agriculture, nanotechnologys international market size isforecasted to be U.S. $1 trillion per year by 2015. The value ofnanotechnologyintheglobal foodmarket is indicatedtoreachupto$3.2billionUSDby2015(Duran&Marcato,2013).Theaimofthisstudyistoreviewcurrentandpotentialapplications of nanotechnologyintheagri-foodindustry,illustratingkeybenets andopportunities for innovationbut also considering the challenges ahead, including the po-tential risks of nanomaterials to human health and the envi-ronment and policy for regulatory issues. New foodtechnologies, such as nanofood, can prove to be very sensi-tive issues with the public, and public perception can have astrongimpact, bothdirectandindirect, ontheprogressofnewtechnologies (Siegrist, 2010). Adirect effect mightbe outright rejection whereas indirect effectscould includethe imposition of stricter regulations by governmentalagenciesperhapsleadingtohigherproductioncosts. Con-sumer attitudes andriskperceptions regardingnanotech-nology are however not addressed in this article. Forreading in this area see Besley (2008); Cobb (2005);Fischer et al. (2013); Frewer et al. (2011); Greehyet al.(2013);Siegrist,2010amongstothers.Trendsinnanotechnologyandagri-foodresearchTheconceptsthatstartednanotechnologywererstdis-cussed in 1959 by the renowned physicist Richard Feynmanin his talk Theres Plenty of Room at the Bottom, in which hedescribed the possibility of synthesis via direct manipulationof atoms. The termnanotechnology was rst used byNorio Taniguchi in 1974. Nanotechnologyemerged as aeldinthe1980sandfromthistimetherehasbeenanin-creaseinscienticpublicationsandawarenessinthearea227 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241with an intensication of research in the 2000s (Fig. 1) duetoampliedscientic, political, andcommercial attentionthat led to both controversy and progress. Similarly,commercializationof products basedonadvancements innanoscale technologies began emerging (Materials UK,2010). However, nanotechnology research in relation tofoodandrelatedapplicationscommencedinthelate1990sandat lessthan2%ofresearchpublicationsisconsidereda relatively small sector of the nanotechnology eld (Fig. 1).Applicationsofnanotechnologyintheagri-foodsectorTheidenticationofemergingopportunitiesforthein-dustryaresummarisedinFig.2.PrimaryproductionA number of reviews (Agrawal & Rathore, 2014;Chaudhry &Castle, 2011; Chen &Yada, 2011; Ditta,2012; Duran & Marcato, 2013; Garcia, Forbe, &Gonzalez, 2010; Grobe & Rissanen, 2012; Khot,Sankaran, Maja, Ehsani, &Schuster,2012;Sekhon,2014)have discussed the emerging applications ofnanotechnology for primary production. Nanotechnologyis expected to facilitate the next development stage ofgenetically modied crops, input to animal productionand sheries, chemical pesticides and precision farmingtechniques.Precision farmingisoneofthemostimportanttechniques utilised for increasing crop productivity bymonitoringenvironmental variablesandapplyingtargetedaction(Chen&Yada,2011).Applications of nanotechnology in agriculture arecurrently at the research and development stage and somaytakemanyyearsbeforebeingcommercialisedworld-wide. Such applications are mostly intended to addresssomeofthechallengesandlimitationsfacinglarge-scale,capital andchemical-intensivefarmingoperations. Poten-tial applications of nanotechnologyinanimal productioninclude improvedefcacyand nutritionof animal feeds(e.g. fortied with nanosupplements, antimicrobial addi-tives, detoxifying nanomaterials) and nanobiosensors foranimal diseasediagnostics. At present, thereareveryfewexamples of commercially available products incorporatingnanosized additives explicitly designed for animal feed. Ex-amplesaremycotoxinbinderssuchasnanoclaytoprotectFig. 1. Number of nanotechnology publications per year in the Scopus database using key terms as indicated (a) nanotechnology (b) nanotechnologyandfood(c)nanotechnology andagriculturalrelatedapplications(d)nanotechnology andfoodrelatedapplications.228 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241animalsagainst mycotoxicosis. Nanoparticles, comprisingof a polystyrene base, polyethylene glycol linker andmannosetargetingbiomolecule, that adheretoE. coli aredesignedtobeadministeredthroughfeedtoremovefood-bornepathogensinthegastrointestinal tractsof livestock(FAO/WHO, 2010). Aquaculture is the worlds fast growingareaofanimalproduction,anditisprojectedtobeoneofthe rst industries to integrate and commercialise nanotech-nologyproducts. Potential applicationsincludenanodeliv-ery of veterinary products in sh food, antibacterialsurfaces in the aquaculture system, and nanosensors for de-tecting pathogens in the water. Although potentially bene-cial, there are existing knowledge gaps regarding theimpacts of nanoparticles on aquatic organisms (Sekhon,2014). In plant-based agriculture, emerging applicationsinclude nanoformulated agrochemicals (e.g. fertilisers, pes-ticides, biocides and veterinary medicines) for improved ef-ciency, reduced use of farm chemicals, new toxinformulations for more effective pestmanagement, and bet-tercontrolofapplications(e.g.slowreleaseofpesticides).Forexample,nanosensorscanbeusedforthedetectionofpathogens, pesticides and other chemicals. Nanosensorshavebeenappliedinpesticideresiduedetectionsuchasorganophosphate in fruit, plants and water (Duran &Marcato, 2013). Khot et al. (2012) has proposed that nano-sensors offer highsensitivity, lowdetectionlimits, superselectivity, fast responses, and small sizes. However,some issues have been identied regarding this application,such as accessibility of nanomaterials sensitive to commonpesticide residues, simplicity of sensor fabrication tech-niquesandinstrumentation, desiredreliabilityandrepeat-ability in trace level detection, the cost, and nally,concerns relating to nanomaterial exposure and the environ-ment.Furtherresearchisrequiredtoensurecompletesuc-cess for thesetypesof nanotechnologyapplication(Khotetal.,2012).Smart eldsensingsystemsareincreasinglyimportantapplications for thereal timemonitoringof cropgrowthand eld conditions including nutritional status, light, tem-perature, moisturelevel, soil fertility, insects, weeds andplant diseases to maximise yields for sustainability inchanging climatic conditions and to maximise yield tofeedagrowingworldpopulation. ChenandYada(2011)hasreportedthatnetworksofwirelessnanosensorsplacedacross cultivated elds provide detailed information oncrop and soil conditions, enabling the best agronomic deci-sions to be made while minimising resource inputs. This in-cludesinformationontheoptimal timesfor plantingandharvesting crops, as well as the time and level of water, fer-tiliser,pesticides,andothertreatmentsthatarerequiredtobeadministeredgivenpreciseplantphysiology,pathology,andenvironmentalconditions(Chen&Yada,2011).Wire-less nanosensors have alreadybeen used in certain parts ofthe U.S. and Australia. For instance, a Californian vineyard,Pickberry, inSonomaCountyhasinstalledWi-Fi systemswiththeaidoftheinformationtechnologycompany, Ac-centure. Thecost of installingthis systemis rationalisedbythefact that it facilitatesthebest grapestobegrownwhichinturnproduces better-qualitywines, whichcom-mandapremiumprice(Joseph&Morrison,2006).Another emergingplant-basedapplicationisnanoscalecarriers(i.e. encapsulationandentrapment, polymersanddendrimers) for the efcient delivery of agrochemicals.Nanoscale delivery vehicles appear to be useful inFig.2.Identicationofemergingopportunitiesfromthesystematicreview;applicationsofnanotechnologyintheagri-foodindustry.229 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241agronomic applications by improving stability againstdegradation in the environment thereby improving its effec-tiveness while decreasing the amount to be applied. This re-duces agricultural chemical runoff and alleviatesenvironmental problems(Ditta, 2012). Thesecarrierscanbe designed in such a wayto anchor plant roots or the sur-roundingsoil structuresandorganicmatter, providedthatmolecularorconformational afnitybetweenthedeliverynanoscalestructureandtargetedstructuresandmattersinsoilcouldbeused.Thesemechanismsenabletheslowup-take of active ingredients, thus reducing the amount of agri-cultural chemicals tobeused, inadditiontominimizinginputsandwasteproduced(Ditta,2012).Nanoencapsulationof pesticidesinvolvesmanipulatingtheouter shell propertiesof acapsuleallowingslowandcontrolledrelease of the activeingredient, andthereforedelivering more effective control over certain pests at lowerdosage rates and over a prolonged period of time. Nanopes-ticidescanincreasethedispersionandwettabilityofagri-culturalformulations(i.e.decreasedchemicalrun-off)andunwantedpesticidemovement. Otherpotential benetsofnanoencapsulated pesticides include increased solubilityand decreased contact of active ingredients with farmworkers (Agrawal &Rathore, 2014; Khot et al., 2012).Globally, pesticides containing nanoscale active ingredientsare commercially available, with many of the worlds lead-ingagrochemical rmsrecognisingtheir potential useful-ness and conducting research into the development ofnovelnanoencapsulatedpesticides.Forexample,Syngentahas incorporated nanoemulsions into its pesticide products.PrimoMAXXisoneofitssuccessful growthregulatingproducts, whichifappliedbeforetheonset ofstresssuchas heat, drought, disease or trafc can strengthenthe phys-ical structure of turf grass, thus enabling it to withstand on-going stresses throughout the growing seasons (Agrawal &Rathore,2014).NutritionNanofoodimplies that foodhas beencultivated, pro-duced, processedorpackagedusingnanotechnologytoolsortechniquesortowhichnanomaterialshavebeenadded(Sekhon, 2010). The intentions of nanofood are to improvethequality,safetyandnutritionalvalueoffood,aswellastoreducecosts. Consumerscanbenet fromthisapplica-tionintermsofmeetingindividual dietaryandhealthre-quirements or taste preferences, while benets to foodcompaniesincludeproductdifferentiation,newmarketop-portunities,andeconomicgains.Severalreviews(Alfadul &Elneshwy, 2010; Chaudhry&Castle, 2011;Chaudhryetal.,2008;Duran&Marcato,2013; Ezhilarasi et al., 2013; Garciaet al., 2010; Grobe& Rissanen, 2012; Iles, Martinovic, & Kozak, 2011;Momin et al., 2013; Ranjan et al., 2014; Rashidi &Khosravi-Darani, 2011; Sekhon, 2010) have identiedthat theemergingapplicationsofnanotechnologyinfoodprocessingarefocussedonthedevelopment ofnanosizedfood ingredients and additives, and delivery systems for nu-trients andsupplements inthe formof nutraceuticals. Adiverserangeof processes arebeingutilisedtoaidwiththis, suchasnanoemulsions, surfactantmicelles, emulsionlayers, reverse micelles and functionally designednanocapsules.Sekhon(2010) has indicatedthat akeyapplicationofnanotechnologyinfoodprocessinginvolves thedevelop-ment ofnanostructuredfoodingredientswhichoffersim-provements to consistency, taste and texture.Nanoemulsion technology is frequently used to createlow-fat mayonnaise, spreadsandicecream, whichmanu-facturersclaimtobeascreamyasthefullfatalternatives,thusofferingconsumershealthieroptions(Cushenet al.,2012; Sekhon, 2010). For example, mayonnaise can benanotexturedusingoilinwateremulsioncontainingnano-droplets of water inside oil droplets. The mayonnaise offerstasteandtextureattributesthat aresimilar tothefull-fatequivalent but with signicant reductions in the fat content.Unileverisproducinganicecreamwithreductionsinfatfrom8-16%e1%whilenot compromisingontheavour.Consumerscanalsobenet frommorerapidandsimplerthawingof frozenfoods inthemicrowave, as developedbyNestleusingnanoemulsiontechnology. It haspatentedwater-in-oil emulsions (10e500 nm), and through the addi-tionofpolysorbatesandothermicelle-formingsubstances,aims tocontributetoauniformthawingof frozenfoods(Alfadul &Elneshwy, 2010; Mominet al., 2013; Ranjanetal.,2014).Foodcompaniescangreatlybenet fromaddingnano-particles to their food and beverage products in terms of im-provementstoavour,colour,owpropertiesandstabilityduringprocessing, orextensionofshelflife. Forinstance,aluminosillcate materials are commonly used as anticakingagents in granular or powdered processed foods, whileanatasetitaniumdioxideis afoodwhiteningandbright-ening additive that is commonly used in confectionary,some cheeses and sauces (Alfadul & Elneshwy, 2010). Ac-cording to the Project on Emerging Nanotechnologies(PEN, 2014) titaniumdioxideiswidelyusedincommer-cially available food and beverages, including chocolate(Hersheys, Kraft, Lindt, Mars Inc), cheese (Albertsons,Kraft), ready prepared mashed potato (Betty Crocker), cof-feecreamer (Nestle), yoghurts(DannonOikos), poptarts(Kelloggs), mints(Mentos,TicTac), sportsdrinks(Coca-Cola)andsaladdressing(Unilever).Nanotechnology offers opportunities to alter and manip-ulatefoodandbeverageproductstoallowformoreeffec-tive delivery of nutrients such as protein, vitamins andminerals, inadditiontoantioxidants, tospecicallytargetnutritionalandhealthbenetstoconsumers. Thisapplica-tion also enables food companies to gain a competitiveadvantage by satisfying individual dietary requirementsandconsumers varieddemands for foods. Animportantcurrent nanotechnology application is nanoencapsulationof food ingredients and additives. Nanocarrier systems230 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241including emulsions, micelles, liposomes, biopolymermatricesandassociationcolloidshavebeendevelopedforuse in food and beverage products. Nanoencapsulationcancontrol the release of certainactive ingredients (i.e.proteins, vitamins, minerals, enzymes andpreservatives),mask undesirable odours and avours such as sh oils,enhancetheshelf-lifeandstabilityof theingredient andthenishedfoodproduct, andalsoimprovetheuptakeofencapsulatednutrientsandsupplements(Ezhilarasi et al.,2013; Sastry, Anshul, &Rao, 2013; Ranjanet al., 2014).The modiedcharacteristics of nanocarriers enable theiruse in a vast array of food and beverage products. Forexample, Alfadul andElneshwy(2010) has reportedthatGeorge Weston Foods, one of the leading bakeries in West-ernAustralia, has successfullyincorporatednanocapsulescontainingtunashoil intotheirTipTopUpbreadforadditional healthbenets. Thenanocapsulesaredesignedtobesecretedoncetheyenterthestomach,therebyavoid-ingtheunpleasanttasteoftheshoil.AnotherexampleisShemenIndustrieswhichhasusedminutecompressedmi-celles, called nanodrops, in the development of canolaactiveoil. Themicellesworkasaliquidcarrier, enablingthe penetrationof vitamins, minerals andphenolic com-pounds that are insoluble inwater or fats. The micellesareaddedtofoodproducts,andsopassthroughthediges-tivesystemefciently,withoutbreakingup,totheabsorp-tionsite(PEN,2013).Nutritional additives are an increasing source of theadditionofnanoparticlestofood. TheEuropeanCommis-sionConcertedActiononFunctionalFoodScienceinEu-rope has dened functional foods as a food thatbenecially affects one or more target functions in thebodybeyondadequatenutritional effectsinawaythat isrelevant toeither animprovedstate of healthandwell-being and/or reduction of risk of disease (EC, 2010).Nanoencapsulation technologies are being employed toprotectbioactivecompoundsincludingvitamins,minerals,proteins, lipids, carbohydrates and antioxidants for themanufactureof functional foods withimprovedfunction-alityandstability, thusofferingvastpotentialforimprove-ments to public health and nutrition (Ezhilarasi et al.,2013).NutraleaseLtdhasdevelopednovelcarriersfornu-traceuticalstobeincorporatedintofoodsystems, therebyenhancing the bioavailability of the product. Lycopene,beta-carotenesandphytosterolsaresomeofthenutraceut-icalsincorporatedinthecarriers, andareusedinthepro-duction of healthy foods, especially to prevent theaccumulationof cholesterol (Gruere, 2012; Ranjanet al.,2014).Theaddedhealthbenetsarising fromthisapplica-tion are therefore particularly benecial for consumers withhealth concerns. Food companies can also benet fromproductdifferentiationandnewmarketopportunities.Rashidi and Khosravi-Darani 2011 has proposed that mi-celles are capable of encapsulating nonpolar moleculesincludingavourants, lipids, antimicrobials, vitamins andantioxidants. Various nano-micelle based carrier systemshavebeendevelopedfornutraceuticalsandnutritionalsup-plementsandareavailable on themarket. For example,Li-vOn Laboratories has developed Lypo-Spheric vitamin C,usingliposomesasthesupplement deliverysystem. Lypo-Sphericvitamin Cis able to produce serumlevels ofvitaminCthatarenearlytwicethelevelofanyotheroralformof vitaminC. HealthPlus International, Inc havealso developed an innovative nutritional product line, knownasSprayForLife. Thetechnologyoffersbenetsofintro-ducingnutrientsintothebodyinawaythat enablesmorerapid,uniformandcompleteabsorptionthanpills,capsulesor other liquids (PEN, 2013). BioDelivery Sciences Interna-tional hasintroducedtheirBioralnanocochleatenutrientdelivery systemfor micronutrients and antioxidants. Thenanocochleates (w50 nm in size) are based on a phosphati-dylserine carrier derived from soya bean, generally regardedassafe(GRAS).Thenanocochleatesystemappearstopre-ventdegradationofmicronutrientsandantioxidantsduringmanufacture and storage (Momin et al., 2013; Ranjanet al., 2014). Five reviews (Alfadul &Elneshwy, 2010;Chaudhry et al., 2008; Ranjan et al., 2014; Rashidi &Khosravi-Darani, 2011; Sekhon, 2010) discussed theGermancompany,Aquanova,whichhas developedanano-carrier systemusing 30 nmmicelles to encapsulate twoactive substances for fat reductionandsatiety; this is aninnovation for intelligent weight management for con-sumers. Marketedas NovaSOL, it uses CoQ10 totargetfat reduction and alpha-lipoic acid for satiety, thus enablingconsumerstofeel fullerforlongerandassistinginweightloss. This technologyhas been usedto addantioxidantsintofoodandbeverageproducts throughtheintroductionof nutrients such as vitamin A, C and E, therefore targetingthe health and dietary requirements of consumers. NovaSOLalso offers substantial advantages to food companies such ascheaper ingredients, faster production process, enhancedshelf life, higher colour stability, improved uptake andbioavailability, andreadytouseliquidform,thusresultinginoverall reductions inenergyusage, wastageandcosts.Other examples of these include Nano Calcium/Magnesiumfrom Magi-I-Cal.com USA, and the nano-selenium-enrichedNanotea from Shenzhen Become Industry & Trade Co., Ltd.(Chaudhryetal.,2008).A recent trend reported by Alfadul and Elneshwy (2010)isthenanoencapsulationofliveprobioticmicrobesforthepromotionofgastrointestinalhealth.Theycanbeincorpo-ratedintovariousfoodanddrinkproducts, includingfer-mentedmilk, yoghurts, cheese, puddings andfruit baseddrinks. Nanoencapsulationtechnologyisappliedtoaidinthe development of designer probiotic bacterial prepara-tions whichcanbe transitedtothe gastrointestinal tractwhere they interact with specic receptors and can improveintestinal microora and thus support good consumerhealth(Sherwood&Gorbach,2000).In2010Alfadul andElneshwyindicatedthat manyofthe large food companies worldwide (i.e. Heinz, KraftFoodsandNestle) wereinvestinginnanotechnologyand231 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241wereontheir waytocommercialisingfoodandbeverageproducts. To date this has not been fully realised. Thedevelopment of interactivefoods whichcanbemodiedin terms of their colour, avour or nutritional properties ac-cording to an individuals dietary requirements, allergies, ortaste preferences are another application discussed byAlfadul andElneshwy(2010). Numerous products basedon nanocluster delivery systems are available commerciallyworldwide. For example, RBCLife Sciences, Inc hasdeveloped a nutritional supplements line called Nano-Ceuticals. This technology has been used to create aslimmingproduct basedoncocoananoclusters, whicharecoatedonthesurfaceof engineeredNMstoenhancethechocolateavourthroughtheincreaseinsurfaceareathattargets the taste buds. This product offers consumers aneffectivesolutiontoweight loss, whileappealingtotheirtastepreferences(Ranjanetal.,2014).Ananotubeisadiscretehollowbreentity, whichhastwo dimensions in the nanoscale (FAO/WHO, 2010).Self-assemblyofhydrolysedcalciumbindingmilkproteina-lactalbumin into nanotubes is another recent develop-ment (Momin et al., 2013). These food-protein derivednanotubesshowgoodstabilityandofferpotentialapplica-tionsinfood, nutrientsandpharmaceutics. a-lactalbuminhasanimportantroleinlactoseformation,whichisessen-tialformilkproduction;itisalreadyusedasafoodingre-dient in infant formula. Infant formula is designed to bear acloseresemblancetohumanbreastmilk, andsoextensiveresearchhasbeen dedicatedto improving theproteinqual-ityof infant formula, sothat it ismorelikehumanmilk(Lien, 2003). The relatively high content of essential aminoacidsina-lactalbuminmakesitdesirableforimprovedin-fant formulaproteinsystems; byofferingsimilar proteincontent tothat of humanmilkhelpingtomeet thenutri-tionalneedsofinfants(Lien,2003).FoodprocessingThefoodprocessingsystemisfacedwithanumberofchallenges relating to the control of chemical contaminants,microbiological hazards and pathogens in order to promotefood safety. A number of research initiatives are in the pro-cessofinvestigatingtheuseofnanoparticlesasantibacte-rials for improving food safety. Silver nanoparticles arebeing incorporated into food processing systems to killfoodpathogensandbacteria(Alfadul &Elneshwy, 2010).Silverseffectiveantimicrobial properties areowedtoitsintenseantimicrobialactivityandlowtoxicitytomamma-lian cells and tissues (Araujo et al., 2013). Therefore silvernanoparticlesarebeingconsideredasanimportant meansofovercomingthegrowingproblemofantibacterialresis-tance. At present, these are beingusedas antimicrobialagents in food processing, with the aimof developingfood-relatedapplicationssuchasmicrobe-resistant fabricsornon-biofoulingsurfaces(Alfadul&Elneshwy,2010).In food manufacturing, the greatest energy requirementsarefromtheprocessheatingandcoolingsystems, whichare an essential part for maintenance of food safety.Nanotechnology-based equipment insulation coatingshave been developed to enable manufacturers to reduceheat loss andlower their energycosts (Nanotechnology,2010). Nansulate has developed thermal insulation coatingsusing award winning, patented technology, which integratesa safe, nanosized internal structure into a lowvolatileorganiccompoundwater-basedacryliclatexcoating.Nan-sulateoffers manufacturers aneasymethodof coatinganumberofdifculttoinsulatefoodandbeverageprocess-ing equipment (i.e. heat exchangers, ovens, dryers andcookers), aswell asprotectingequipment fromcorrosionandmouldgrowth. Furthermore, theclear coatingsallowfor easy visual inspection of the substrate surface. Theoverall benets tofoodmanufacturers includesignicantcost savings and improved prot margins (IndustrialNanotech,Inc.,2014).Anothernanotechnology-basedcoatingsystemisBioni,which was also developed to satisfy the requirements of thefoodindustry. Thepatentedsolutionusesatwolayersys-temthat canbe applieddirectlytomouldaffectedsub-strates, and other surfaces. The systemalso provides apermanent protection against growth of new mould, mildewor bacteriaonthecoatinglm, thereforeprovidingcost-savingbenets. Afurther advantagetoBioni isthat it iseco-friendlyasitdoesnotrequireanyotherchemicalsfordisinfectant andpre-treatment ofaffectedsurfaces(Bioni-USA,2013).FoodpackagingNanopackagingapplications as foodcontact materialsaregrowingrapidly(Fig. 1); thisisnowconsideredtobeone of the most active areas of nanotechnology in thefoodsector(Ranjanet al. 2014). In2011, nanopackagingwas projectedtoaccount for 25%of all foodpackagingwithin the next ten years (Lyons, Scrinis, &Whelan,2011). However, industrial applications of foodpackagesbased on nanomaterials are strongly dependent on explora-tion of regulatory aspects which should be issued onconsideration of both their efciency in preserving thephysical, chemical, microbiological andsensorial qualityoffoodbut alsotheirpossibleandunanticipatedrisksforthe environment and human health (Apan, Cozmuta,Peter, Nicula, &Cozmuta, 2014). Manufacturers claimthat nanopackagingcanextendproduct shelf-life, aswellasmaintain, improveormonitorthequalityandsafetyoffoods.Forinstance,theuseofnanoparticlesinfoodpack-aging can improve the mechanical and heat resistance prop-erties, therebyaffectinggasorwatervapourpermeability,andthusincreasingshelf life. Several reviews(Chaudhry&Castle, 2011; Duran&Marcato, 2013; Garcia, 2010;Han, Yu, Li, &Wang2011; Mominet al., 2013; Rashidi&Khosravi-Darani, 2011; Restuccia et al., 2010; Rhim,Park, & Ha, 2013; Silvestre, Duraccio, & Cimmino,2011; Sozer & Kokini, 2009) have reported three main cat-egoriesofnanopackaging:improvedpackaging,active and232 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241intelligent packaging, andbiodegradable nanocompositesfoodpackaging. Improvedpackaginghas beendescribedbySilvestreetal.(2011)asincorporatingnanoparticlesinthe polymer matrix materials with improved packagingpropertiesintermsoftemperature/moisturestability,exi-bility, durabilityandgasbarrierproperties(e.g. nanocom-posites, silicatenanoparticles, andnanosilver). Hanet al.(2011)hasalsosuggestedthattheapplicationofnanopar-ticles infoodpackaginghasadditional functionssuchasantibacterial properties. Elgin, IL Multilm Packaginghas developedanultra-thincoating, knownas N-Coat,whichis appliedona48gaugepolyester lm, resultinginaclear laminatewithanexcellent gasbarrier that cancompete with most metallised structures. N-Coathasbeenprimarilydevelopedfor nuts, coffee anddryfoods(PEN,2013).Active and intelligent food packaging are novel conceptsof packaging compared with traditional materials. Polymernanocompositesintegratingmetalormetaloxidenanopar-ticles have been developed for active packaging. Theseinclude silver, gold, zinc oxide, silica, titaniumdioxideandironoxides(Chaudhryetal.,2008).Hanetal.(2011)has indicatedthat activepackaginghas theabilitytore-move undesirable tastes and avours, and improve thecolourorodourofthepackedfood. Forexample, carbonblacknanoparticles incorporatedintopolymer packagingcanabsorbodours releasedfromthe foodor packaging.An emerging active packagingapplication integrates nano-particleswithantimicrobial oroxygenscavengingproper-ties; this packagingis designedtostopmicrobial growthonce the package is opened by the consumer and rewrappedwithanactive-lmportionofthepackage(Mominet al.,2013). A number of food contact materials have been devel-opedusingnanosilver, whichclaimstopreservethefoodfor longer andinhibit thegrowthof microorganisms. Forexample,BlueMoonGoodsLLChasintroducednewsilvernanoparticle fresh box super airtight food storage con-tainers that can reduce bacteria by up to 99.9%. Foodscan easily be stored for up to four times the length of tradi-tional food containers, thus offering consumers benets offresher, higher quality food for a longer period of time, andsubsequently, reduced food wastage. Other examplesinclude FresherLongerMiracle Food Storage Con-tainersandFresherLongerPlasticStorageBagsfromSharper ImageUSA, Nano Silver Food ContainersfromA-DOGlobal and Nano Silver Baby Mug CupfromBabyDreamCo. Ltd(PEN, 2013). Nanosilverhasalso been used to provide an antibacterial coating on kitch-enwareandtableware(ChangminChemicals, NanoCareTechnology Ltd, Pro-Idee GmbH & Co. KG) and as an inte-rior coatingof domesticrefrigerators (LG, SamsungandDaewoo) tokill bacteriaasaneffectivedisinfectant, thusbenetingconsumers interms of reducedrisks of food-borneillness(PEN, 2013). Intelligentorsmartfoodpack-aging incorporates a nanobiosensor for sensing andsignallingmicrobial andbiochemical changes, releaseofantimicrobials, antioxidants, enzymes, avoursandnutra-ceuticals toextendshelf life. Adiverserangeof deviceshavebeendevelopedtodetectfoodspoilageorganismsinfood packaging (i.e. nanowires and antibodies), thusenablingversatilityandmuchcheaper production(Duran&Marcato, 2013). Forexample, Kraft Foodshavedevel-oped an electronic tongue which has been incorporatedintotheirpackaging. Thisintegratesanarrayofnanosen-sorswhicharehighlysensitivetothegasesreleasedwhenfoodisspoiled. Thesegasesresult inacolour changeofthesensorstripto warntheconsumerthatthefoodisuntfor consumption(Mominet al., 2013). AgroMicronhavealso developed the NanoBioluminescence Detection Spray,which encompasses a luminous protein which is intended tobindtothesurfaceofbacteriasuchasSalmonellaandE.coli(Duran&Marcato,2013).Biodegradable nanocomposites food packaging incorpo-rates inorganic particles, such as clay, into the biopolymericmatrix, whichcanimprovethedeliveryofmicronutrients(Rhimet al., 2013). The nano-layeredstructure alsore-stricts the access of gases, and offers considerable improve-ments in terms of gas barrier properties of nanocomposites.Biodegradable materials have potential use in a wide rangeof food packaging applications, including processed meats,cheese, confectionary, cereals, boil-in-the-bag foods, aswell asextrusion-coatingapplicationsfor fruit juicesanddairy products, or co-extrusion processes for the productionofbottlesforbeerandcarbonateddrinks(Chaudhryetal.,2008).Forexample,Voridanhasdevelopedananocompo-sitecontainingclaynanoparticles, termedImperm. Thisisideal for beer, asthe resultantbottle is lighter andstrongerthanglassandislesslikelytoshatter. Further, thenano-composite structure minimises loss of carbon dioxidefrom the beer and keeps oxygen out of the bottle, thereforeretainingthefreshnessofthebeerandextendingitsshelflife(Hanet al., 2011). Thistechnologyhasbeenadoptedbyvarious companies includingAegixOX(HoneywellSpeciality Polymers) who has successfully engineered plas-ticbeer bottles that integratenanocomposites toenhancethebarrierpropertiesandextendedshelf lifebyupto26weeks. ThistechnologyhasbeenusedintheHitePitcherbeerbottlefromHiteBreweryCo. inSouthKorea(PEN,2013). Durethan KU2-2601 (Bayer AG) is anotherexample, whichis ahybridplastic that is enrichedwithnumerous silicate nanoparticles. The plastic incorporatesNanocorsclaytoproducealmthat islighter, strongerandmoreheat resistant thantraditional packagingmate-rials. The lm is intended to prevent the entrance of oxygenandothergases, andtheexit ofmoisture, thuspreventingfood spoilage (Gruere, 2012; Han et al., 2011). Conversely,DuranandMarcato(2013) hassuggestedthat biodegrad-able materials demonstrate poor barrier and mechanicalpropertiesandrequiresubstantialimprovementsbeforere-placingtraditionalpackagingmaterials.Nanopackaginghas the potential toprovidemanufac-turers withavast rangeof benets, includingtheability233 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241to keep packaged food fresher for longer (Rhimet al.,2013). Thismayenablefoodtotravel furtherandremaininstoragefor anextendedperiodof time, thus resultingin a more reliable food supply. By increasing the shelflifeof foodproducts, manufacturers will alsobeabletosell foodthat wouldhave otherwise beendiscardedduetospoilage, andhencecontributingtoreductionsinfoodwaste. Innovativeandnovelpackagingthatislightweight,strongerandfunctionalcanalsosignicantlyreducetrans-portation costs and packaging materials in the environment.Smart labelson foodpackagingis likelyto appeal to man-ufacturers due to the ability to effectively monitor thesafety, qualityandsecurityoffoodandbeverageproductsduringtransportationandstorage, therefore reducingtherisks of food-borne illness. Consumers can also benetfrom attractive new products on the market, which are saferandofbetterquality.OpportunitiesandanticipatedbenetsAnumber of reviews (Bradley, Castle, &Chaudhry,2011; Chaudhry &Castle, 2011; Cushen et al., 2012;Kuan, Yee-Fung, Yuen, & Liong, 2012; Meetoo, 2011; Mo-minetal., 2013;Rashidi&Khosravi-Darani, 2011;Ravi-chandran, 2010; Sekhon, 2010, 2014; Sonkaria, Ahn, &Khare, 2012) have recognised the vast opportunities ofnanotechnology in agriculture and in all aspects of thefood industry, including preservation, processing, pack-agingandmonitoring(Fig. 2).Therearenumerouspoten-tial benets arising from the application ofnanotechnologyinfood, whichmakeit of real relevancefordevelopingcountries, aswell asfordevelopednations(Fig. 3). Nanotechnologyenables moreeffectiveagricul-tural productionmethods, withaloweruseofagrochemi-cals(e.g. pesticides, fertilisersandveterinarymedicines),which can alleviate environmental pollution and lessenchemical run-off. A range of benets are offered to farmers,includingreductionsinagricultural losses, enhancedpro-ductionefciency,lowerresourcecostsandimprovementstoprot margins. Extendedshelf lifeof foodproductsisalsopossiblethroughinnovativepackagingthat incorpo-ratesantimicrobial properties. Thisapplicationoffersvastpotentialto thefoodindustryby contributing toreductionsin food waste, as well as a better quality and safer food sup-ply.Inaddition, theuseofnanosensorsinfoodpackagingfor detectionoffoodspoilageisimportant for combatingpathogenic microorganisms, and consequently reducingfoodborneillnessesinconsumers.Smart labelsonfoodpackagingcanalsoaidmanufac-turers in ensuring authenticity, traceability and safety oftheirfoodproducts. Therearealsoopportunitiesfornovelfoodandbeverageproductswithimprovedcolour, avour,texture or nutritional value to meet each consumers desiresFood Nanotechnology BenefitsRisksLower pesticide use Improved traceability & safety of food productsReductions in fat, sugar, salt & preservatives Enhanced nutritional value of food/beverages Novel flavours & texturesMaintenance of food quality & freshness More hygienic food processing Extended product shelf lifePotential human health Oxidative damage & inflammation of GI Concerns for workers health & safetyPotential harmful effects to the environment Lesions of liver & kidney CancersAcute toxic responses Fig.3.Themainprojectedbenetsandrisksofnanotechnology applicationsinfoodandrelatedproducts.234 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241ordietaryandhealthrequirements.Forexample,nanotech-nology can be used to enrich foods with fruit and vegetablesto deliver high nutrient density in such foods (Ravichandran,2010). Nanotechnology can be utilised to dissolve additives,such as antioxidants, phenolic compounds, vitamins andminerals. Furthermore, through nanoencapsulation technolo-gies additional nutrients can be added to food and beverageproducts, without altering avour or quality. The delivery ofcertain ingredients and additives to a specic target sitewithinthebodyisalsopossible, thereforeprovidingcon-sumers with additional health benets. The benets of nano-encapsulationtechnologies are extendedtomanufacturersthroughprotectionof foodingredients duringprocessing,andextensionofproductshelflife, whichcanreducefoodwasteandimproverevenues.Inviewof theexpectedbenets(Fig. 3), tworeviews(Bradleyetal.,2011;Chaudhry&Castle,2011)haverec-ognisedthevast potential for improvements tofoodandwater safetyandpublicnutritionindevelopingcounties.Moreover, nanotechnologyoffers huge potential for pro-ducersintermsofexporting, throughincreasingthelocalprocessing of basic commodities such as tea, coffee, spices,sugar, bananas and rice, and thus increasing volumes of ex-portsandsubsequentlyprot margins. Insummary, nano-technologyhasthepotential toenhancethesustainabilityof the agri-food sector through delivery of economic, envi-ronmental and social benets to a range of actors from con-sumers/thepublicrightbacktofarmers.PotentialrisksSafetyDespitenanotechnologysvastopportunitiesandpoten-tial applications in the agri-food sector, there are increasingconcernsrelatingtosafetyandhealth(Fig. 3). Increasingscientic evidence has demonstrated that exposure to nano-particles(i.e. carbonblack, silicates, titaniumdioxideandiron oxide) may lead to oxidative damage and inammatoryreactions of the gastrointestinal tract. Further, longtermexposure has been linked to acute toxic responseincludinglesionsofthekidneyandliver,aswellasnumerousformsof cancer (Borm et al., 2006; Momin et al., 2013; Silvestreet al., 2011). Several reviewsinvestigatingthetoxicologyandsafetyaspects of nanoparticles (Bouwmeester et al.,2009; Bradley et al., 2011; Chaudhry &Castle, 2011;Chaudhry et al., 2008; Cockburn et al., 2012; Cushenet al., 2012; Grobe&Rissanen, 2012; Hanet al., 2011;Ileset al., 2011; Kuanet al., 2012; Kuzma, Romanchek,&Kokotovich, 2008; Magnuson et al., 2011; Mominet al., 2013;Silvestreet al., 2011)haveindicatedthat theincorporationof nanomaterials intofoodmaypresent anentirenewarrayof risksfor consumers. Themost likelyroute of entry of nanoparticles to the gut is through the con-sumptionoffoodanddrinks. Themainconcernsofnano-particlesinrelationtohumanhealthincludetheincreasedtoxicologicaleffectsofnanoparticlesatsmallerconcentra-tions due to the much larger surface area, enhanced toxicityowing to improved bioavailability, greater access to the hu-man body, compromised immune systemresponse, andpossiblelongerpathologicaleffects(Mominetal.,2013).Discussion within the reviews suggests that scienticknowledgegapsexist inourunderstandingoftheproper-ties, behaviour and effects of nanomaterials, which cancause great difculties for risk assessors and risk managers,and severely hinder risk assessment. Moreover, there islimitedknowledge oncurrent usage levels andexposurefrom applications of nanoparticles in food and food-relatedproducts. Asystematicapproachwas adoptedbyCockburnet al. (2012) for thesafetyassessment ofengi-neered nanomaterials for food application, proportionateto their physiochemical characteristics and therefore poten-tial for toxicological concern. A decision tree is utilised fortoxicological testing of engineered nanomaterials and atieredapproach for subsequent hazard identication andcharacterisation. Thesafetytestingstrategyis consideredappropriatetovariationsinengineerednanomaterial size.Further, Magnuson et al. (2011) conducted an appraisalof the literature to determine the current state of knowledgeregardingthesafetyofnaturallyoccurringandengineerednanomaterials for food and food-related applications. Asystematicapproachtoassessthereliabilityoftoxicologystudies of nanomaterials was developed, whichhas beenpreviously published by Card, Jonaitis, Tafazoli, andMagnuson(2011). Thereviewidentiedalackofstudiesconductedthusfartoassessthetoxicityofnanomaterialsfollowing oral exposure, and much of the publishedresearch comes from in vitro studies or from in vivo studiesusing dermal or inhalation exposure routes (Magnusonetal.,2011).Thepossibleeffectsofnanoparticlesthroughthegastrointestinaroutearemostlyunknown. Inthefoodsector, toxicology research is almost non-existent, andfewstudieshaveprovedtobeusefulintermsofassessingtoxicity. As a result, any individual risk assessment is likelytobesubjecttoahighdegreeofuncertainty.Theoutcomeofthisreviewhaspointedtowardstheneedforadditionaltoxicology studies of adequate design and duration ondifferent types of NMs to provide more conclusive evidenceregarding the toxicity of nanomaterials used in food. Exist-ingtoxicitymethodologiesappliedtoconventional mate-rials may require modication to consider the uniquecharacteristicsof nanoparticles. Inrelationtoriskassess-ment, it isalsoimportant tonotethat toxicityislikelytovaryamongspecicnanoparticles, thusariskassessmentmustbeperformedonacasebycasebasis.Thereareanumber of on-goingEUresearchprojectsaimed at addressing all aspects of nanosafety includingtoxicology, ecotoxicology, exposure assessment, riskassessment, mechanisms of interaction, and standardisa-tion.Examplesofon-goingEUprojectsincludetheNano-Lyse project which is dedicated to the development ofanalytical tools for the detection and characterisation of en-gineered nanoparticles in food, and the NanoReTox projectwhich seeks to address the human health and environmental235 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241implicationsofexposuretoengineerednanoparticles(EUNanosafetyCluster,2014).FoodpackagingconcernsSeveral reviews (Chaudhry &Castle, 2011; Duncan,2011; Han et al., 2011; Kuzma et al., 2008; Silvestreet al., 2011)havereporteduncertaintiesregardingthepo-tential adverseeffectsof nanopackagingmaterialsonhu-manhealth. Discussionwithinthesestudiesindicatesthatthemainriskofconsumerexposuretonanoparticlesfromfoodpackagingmaterialsisindirectlythroughthe possiblemigration into foodstuffs, or ingestion of edible coatings. AnarrativereviewbyKuzmaet al. (2008) demonstratedaneedforconsiderationofthetoxicityofclaynanoparticlesandtheir abilitytomoveout of thelmintofoodunderdifferentconditionsforriskassessment.Clayinthemacroformis knownto be nontoxic; however, the toxicityofnanoparticles is not well established. Nanoparticles ofclayare knowntobe highlyreactiveduetotheir muchgreater surface area and so, concerns have been raisedthat thisreactivitycouldleadtomoretoxicformsofclayparticles duringproductionor use. Migrationstudies arecurrentlylimited, despitethefact that anumber of foodpackagingmaterials containingnanoparticles are alreadycommerciallyavailableinsomecountries.Thefewmigra-tion experimental and modelling studies that have beenconductedthusfarsuggest thatthelikelihoodofnanopar-ticlemigrationfrompolymer packagingtobeeitherverylowornil, andtherefore, donot poseanysignicant risktotheconsumer(Chaudhry&Castle,2011).Nevertheless,discussionwithinthereviews(Chaudhry&Castle, 2011;Duncan, 2011; Han et al., 2011; Kuzma et al., 2008;Silvestre et al., 2011) has pointedtowards the needforfurtherresearchandinvestigationtoprovidemoreconclu-sive evidence. In relation to risk assessment of nanomateri-alsafteringestion, thishasbeenstudiedforonlyafewofthenanoparticles usedinfoodpackaging. Silvestreet al.(2011)hasproposedthat thereisalackofunderstandinginrelationtohownanomaterialswill act oncetheyenterthehumanbody.Questionslike, howandifthenanopar-ticleswillbeabsorbedbydifferentorgans,howwillthebodymetabolisethem,andhowandinwhichwaywillthebodyeliminatethemarestill subject touncertainty.Thereis aparticular concern regarding the possible migra-tion of nanoparticless into the brain and unborn foetus. Theoutcome of this narrative reviewrecommends anurgentneedforresearchinbothoftheseareastoeitherconrmor discard the theory of nanoparticles association withseveral brain diseases. The health implications of othernanoparticles used in food packaging are underinvestigation.RegulatoryaspectsThesuccessoftheadvancementsofnanotechnologyintheagri-foodindustrywill bedependent ontheconsider-ation of regulatory issues. Legislation is essential tomanage potential adverse effects, mitigate risks, and protectconsumers. Various government agencies worldwide arebecomingincreasinglyinterestedintheuseof nanotech-nology in the agri-food sector. Problems arising from nano-foodapplicationsareshowninthepracticallynon-existentlaws to regulate this use (Coles & Frewer, 2013). There arecurrentlynointernational regulationsofnanotechnologiesor nanoproducts (Momin et al., 2013). Chaudhry andCastle(2011)hassuggestedthatcurrentregulatoryframe-worksfor foodandfoodpackagingmaterialsindifferentjurisdictions including the EU, the U.S. and AustraliaeNewZealand are extensive enough to encompass nanotech-nology applications in the food sector. Theseincluderegu-lationsregardinggeneralfoodsafety,foodadditives, novelfoods, specic healthclaims, chemical safety, foodcontactmaterials, waterquality, generalproductsafety, aswellasother specicregulationsonthecertainuseof chemicalsin food production (i.e. fertilisers, pesticides, etc.). Bycontrast, amorerecent narrativereviewbyMominet al.(2013)indicatesthat existing laws areinadequate to assessrisks posed by nanofoods and nanopackaging due to currentuncertaintiesarisingfromthedifcultytodetectandmea-surenanomaterialsinfood,meaningthatthereiscurrentlylimitedinformationavailableconcerningaspects of toxi-cologyandtoxicokinetics. Inaddition, nanomaterials arenot assessedasnewchemicalsaccordingtomanyregula-tions, current exposureandsafetymethodsareunsuitablefornanomaterials,andmanysafetyassessmentsusecon-dential industry studies. Nevertheless, the on-going EUSmartNano project aims to develop an innovative, cost-effectivetechnologyplatformthat arebasedonready-to-use, application-specic cartridges for the detection, identi-cationandmeasurement of engineerednanoparticles infoodmatrices. Theprimarypurposeofdevelopingatech-nologyplatformforthemeasurementofengineerednano-particlesistoassessthefateandpotential safetyrisksofengineered nanoparticles in food and food-related products(EUNanosafetyCluster, 2014). Afurther issuerelatesto(Coles &Frewer, 2013; Cushen et al., 2012; Grobe &Rissanen, 2012; Kuan et al., 2012; Magnuson et al.,2013) alackof clear, uniform, international denitionofnanomaterials and nanotechnologies, which can lead tomisinformationandinconsistencies whencommunicatingrisks. There are many existing denitions of nanotech-nology, which consider the specic properties of nanomate-rials (derived from their nanoscale range, shape andpotentiallyreactivesurfaces, etc.) andtheir nanofeatures.However, in 2011 the ECrecommended a denition ofnanomaterials, whichis intendedtobeusedbyMemberStates, EU agencies and companies. The EC denes a nano-materialasanatural,incidentalormanufacturedmaterialcontaining particles, in an unbound state or as an aggregateorasanagglomerateandwhere, for50%ormoreoftheparticles in the number size distribution, one or moreexternal dimensions is in the size range 1e100 nm. In spe-cic cases and where warranted by concerns for the236 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241environment,health,safetyorcompetitivenessthenumbersizedistributionthresholdof 50%maybereplacedbyathreshold between 1 and 50% (European Commission,2012). Effortstoestablishamorecomprehensiveinterna-tional denitionfor nanomaterials areinprogress (Coles&Frewer,2013).The EU is the global leader in the development and im-plementationoflaws fornanofoodapplications(Iles etal.,2011). Magnuson et al. (2013) is good source for a compre-hensive list of current EU regulations and directivesrelatingtonanomaterials. Iles et al. (2011) reportedthatthe EC has acknowledged which scientic knowledgegaps(i.e. healthandtheenvironment) must beaddressedin orderto provide supportfor the legal framework.More-over, the EU regulations for food and food packaging haverecommendedthatthereisarequirementfortheintroduc-tionof newnanotechnologyspecicsafetystandardsandtestingprocedures(Mominetal.,2013). Intheimmediatefuture, it isanticipatedthat asuccessionofnewEUlawswill beadoptedtoenablemoreeffectiveregulationofthenanofoods market and protect consumers (Magnusonet al., 2013). ChaudhryandCastle (2011) has proposedtheestablishmentofagloballyharmonisedregulatorysys-temto ensure pre-market evaluation of nanofoods andnanoproducts, as wellas to set liabilities,and specifyclearlimits for any nanoadditives in food and food-related appli-cations. International harmonisation of legislation is bene-cial totheagri-foodindustrytofacilitateininternationaltrade. Effectiveregulationof nanotechnologyintheagri-foodsectorwill alsoenableproductstobelaunchedwithtrust andcondence, inadditiontoprotectingconsumersfrompotential safety risks. Alternatively, it is possiblethat regulation of nanotechnologies and nanomaterialscould increase consumer concerns regarding its use infood, raisingquestionsregardingitssafety. Itisimportantfor the industry to appreciate consumer concerns, andincorporate public opinions regarding nanotechnologysuseinfoodatanearlystageoftheirdevelopmenttoavoidaGMrepeat, whichwaslargelyrejectedbytheEuropeanmarket (Biebersterin et al., 2013; Brown & Kuzma,2013). Industrylednanotechnologyglobal networksmayoffer opportunities for communication for the agri-foodsector.NanotechnologyforasustainablefoodsystemTheglobalisationofthefoodsystemmeansthatsupplyanddemandis mostlydictatedbyglobal market drivingforces. Increased food demands are drivenby a rapidlygrowingglobal population, withthecurrent populationofapproximately 7 billion people projected to reach 9.3billion people by 2050 and 10.1 billion by 2100 (UN,2011). Global foodproductionwill havetoincrease50%bytheyear 2030anddoubleby2050tomeet theantici-pated demands (Parry &Hawkesford, 2010). Changingconsumptionpatternshaveplacedfurther pressureontheindustryforaglobalfoodsupplysystem,withanincreasein the demand for meat and cereal products worldwide. To-tal meat production needs are projected to reach 455million tonnes by 2050, while cereal production is expectedto be three billion tonnes by 2050, with the greatest demandcomingfromdevelopingcountries,whichnowaccountfor61% of the global cereal consumption (Parry &Hawkesford,2010;Tilman,Balzer,Hill,&Befort,2011).International tradeinfoodstuffshasgrownrapidlyandchanged profoundly over recent decades, in response totheglobal populationgrowthwithchangingdiets; this isa key driver of globalisation. The modern consumer-drivenfoodindustryiscontinuouslyseekingnewwaystodevelopinnovativeandnovel products that will not onlyoffernewtastesandtextures, butarealsohealthful, morenutritious, of improved quality and cost effective, thusfacilitating a more sustainable, safe and nutritious foodsupply.At present, theworldwideagricultural systemisfacedwithanumberoflong-termchallenges, includingclimatechange,increasingcompetitionforenergy,landandwater,urbanisation, and environmental problems such as chemicalrun-off (i.e. pesticides and fertilisers). Nanotechnology canplayafundamentalroleincontributingtoamoreefcientandsustainable agricultural andfoodproductionsystem,withopportunitiestoincreasefarmproductivity, alleviateenvironmental issues, and reduce resource costs. Theseinclude techniques that will preserve landandwater byincreasingcropyieldwhile usinglower resource inputs,as well as techniques aimedat protectingthe qualityofthe environment. For example, Nanotechnology can beapplied for the efcient delivery of agrochemicals (i.e. pes-ticides, herbicidesandfertilisers) byusingnanoscalecar-riers; they have controlled release mechanisms whichallowthe active ingredient to be taken up slowly, thusimproving its effectiveness, while reducing the amountapplied(Chen&Yada, 2011; Ditta, 2012). Reductionsinagrochemicaluse willprovide additionalbenetstopublichealth. Nanotechnology can also be utilised to provideeffective solutions to animal production, by minimising los-ses fromanimal diseases includingzoonoses, as well asimproving production efciency, animal health and welfare,feednutritional efciency, andproduct qualityandvalue(Chen&Yada,2011;Ditta,2012).Moreover, indevelopingcountries, nanotechnologyhasthepotentialtosustainfoodproductioninawaythatwillreducepoverty, improvepublichealthandnutrition, andhence increase foodsecurity(Chen&Yada, 2011). Im-provements to public nutrition can be achieved byincreasingthebioavailabilityofnutrientsintypicaldietarycomponentsorfoodaid,throughtechniquessuchasnano-encapsulationtoimprovetheabsorptionofnutrientsinthebody. Nanoparticles can also be incorporated into food andbeverage products, sothatnutrients arereleaseduponcon-sumption.This applicationwouldbebenecial inproductssuch as orange juice, which have substantially depletedvitaminClevelsafter juicing. Moreover, nanotechnology237 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241offers vastpotentialfor industry in developing countries interms of exporting, through increasing the local processingof basic food commodities such as tea, coffee, spices, sugar,bananas and rice, and therefore increasing volumes andvalues of exports and subsequently prot margins(Bradleyetal.,2011).Nanopackagingcanalsoaidthe globalised,tradeorien-tated, andsupermarket dominatedfoodsystembyextend-ing product shelf life, facilitating the long-distancetransportation, trackingthesupplychain, andmonitoringthe qualityandsafetyof the foodsupply(Lyons et al.,2011). The primary objectives of nanopackaging are toreducetheamount of resourcesused(e.g. energy, antibi-otics, preservatives, pesticides) andthequantityof pack-aging materials in the environment, which cansubsequentlyhelptoalleviateenvironmentalpollution.Byextendingtheshelf lifeof products, thiscanalsosigni-cantly reduce loss in the supply chain as a result of productspoilage/waste, therebyresultinginpossiblereductionsinfoodpoverty. Nanopackagingalsooffersotheradvantagesin terms of preserving the taste, colour and avour offoodproducts, aswellasdelayingthedeteriorationofthenutritionalvalue.CurrentgapsinknowledgeWhiletheliteratureassessmenthasidentiedanumberof potential applications and benets of nanotechnologyin the global agri-food industry, it has also become evidentthatthereareexistingscienticgapsinknowledgefortheindustry to make an informed choice of its use. Thesegaps aremainlyinrelationtoknowledgeof theapplica-tions, andconsumer andenvironmental safety, whichareimpedingregulationandmarket uptake, andthus requirefurtherresearch. Aclear, uniformdenitionofnanomaterialsandnano-technologies is lacking. The EC has established a deni-tionof nanomaterials for use byMember States, EUagencies and companies. Efforts are currently underwayto implement a more comprehensive internationaldenition. Validatedtechniquesforthedetectionandcharacterisa-tion of nanomaterials in food matrices are required. Theon-going EU NanoLyse project, as part of a wider Nano-safety cluster, is dedicated to the development of analyt-ical methods for thedetectionandcharacterisationofengineered nanoparticles in food (EU NanosafetyCluster,2014). Additional toxicological studies that are of sufcientdesignanddurationondifferenttypesofnanomaterialsespeciallynanosilverarerequiredtoestablishpotentialhealthriskstohumans. Adsorption, distribution, metabolismand eliminationprolesof nanomaterialsmaydiffer fromlarger parti-cles, andit isunclearastohowingestednanoparticleswillbehaveoncetheyenterthehumanbody. More exposure assessment methodologies are neededtoassess thelongtermhealthconsequences of inges-tion of nanoparticles via food, which are at presentunknown. There is a lack of risk assessment data, and guidance onrisk assessment methodologies is unclear andinconsistent. Similartogeneticmodication,theapplicationofnano-technologyintheagri-foodsectorraisesquestionsofanethical nature. If nanoparticles are incorporated intofoodstuffs, should these foodstuffs have labelling to indi-catewhatnanohasbeenusedandforwhatpurposes.Astudy by Brown and Kuzma (2013) found that consumerswant food products that use nanotechnology (whether itsinthefood orthepackaging) tobe labelled accordingly,and they are willing to pay more for this labelling.Siegrist andKeller (2011) highlight that if labellingismandatory, it mayresult inhigher perceivedrisks andlowerperceivedbenets.Theyalsoarguethatprovidinginformationonthelabelalonethattheproductcontainssyntheticnanoparticlesmaynotprovidesufcientinfor-mation to result in informed decision-making as it wouldrepresentanover-simplicationoftheprocessandasso-ciatedissues. Thusthereisanargument forindustrytoengageinvoluntarymeasures that provideinformationtoconsumerstosupportinformeddecisionmaking.Theuse of QRcodes, andaugmentedrealityapplications,forexamplemaybebenecial. Enhancement of knowledge and awareness of the multi-disciplinarynanotechnologyapplications inbothagri-culture and farming systems from fertilisers tonutrition to monitoring soil quality and plant and animalhealthandthepotentialopportunitiesandrisksinthosesystemsisrequired. Aquaculture plays an important role in sustainableglobal food production but knowledge on nanotech-nologyapplications andopportunities insheries andaquaculture is limited. More research is needed intothefateandbehaviour of nanoparticlesinaquaticandterrestrial systems as well as their interactions withorganisms. There are uncertainties over the adequacy of currentglobal regulations of nanotechnology applications forfoodandrelatedproducts.Thedevelopmentandimple-mentationoflegislation attheinternationallevel is alsoofgreatimportancetosetliabilities,andestablishclearlimitsforanynanofoodsandnanoproducts. An improved awareness of nanotechnology throughnanoeducationprogrammes commencingat theschoollevelthroughtobusinessandregulationisrequired. An integrated safe nanobased global platform isneededfor better coordinationandcommunicationbe-tween various organisations involved in the developmentand use of nanotechnology products/devices. This couldbe achieved through global and regional nanotechnologynetworks.238 C.E.Handfordetal./TrendsinFoodScience&Technology40(2014)226e241ConclusionAn overview of the current and potential applications ofnanotechnologyinfoodandrelatedproductsindicatesthatthey offera rangeof benets to the entireagri-food sector,fromimprovedprecisionfarmingpractices, tofoodprod-uctswithenhancedavour, textureandnutrition, aswellas novel packagingwhichcanextendproduct shelf life,andincreasethequalityandsafetyof food.Manyofthesebenets will enhance the range, quality and quantity of foodproducts, enable newinternational market opportunities,and improve protmargins. They also offer great potentialfor improvements to food and water safety and nutrition indevelopingcountries.Thecurrentlevelofnanotechnologyin the global food sector is still relatively small, withmost products still at the R&D stage, and limited successfulapplicationsof nanotechnologytofood. At present, thereare substantial uncertainties regarding food companieslevel ofawarenessandattitudestowardstheuseofnano-technologyfor foodapplications. Existingscienticgapsinknowledgeinrelationtopotentialhealthrisksandenvi-ronmental safety are impeding the implementation of effec-tivelegislation. 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