The fungal problem in cheese industry Cathrine Finne Kure1 and Ida Skaar
2
Mouldgrowthoncheeserepresentsbothaqualityandafood safetyproblem,andposessignificanteconomiclosses.
Severalmouldgeneramaydestroycheese;however,normally justafewfungalspeciesdominateonaspecifictypeofcheese.
PenicilliumisthemajorgenusfollowedbyAspergillus.Cheese- contaminatingmouldspeciesmayproducemycotoxins,and someofthetoxinssuchasochratoxinA,cyclopiazonicacid andsterigmatocystinhavebeenshowntobestableunder normalprocessingconditions.Themainmouldcontamination sourceistheenvironmentintheproductionfacilities.Visible mouldgrowthoncheeseintheplantshouldbeavoidedinorder topreventproblemmouldstospread.Foridentificationofthe contaminationsource,identificationatorbelowspecieslevelis necessary.
Addresses
1Nofima,NorwegianInstituteofFood,FisheryandAquaculture Research,P.O.Box210,N-1431Aas,Norway
2NorwegianVeterinaryInstitute,Ulleva˚lsveien68,P.O.Box 750Sentrum,N-0106Oslo,Norway
Correspondingauthor:
Kure,CathrineFinne([email protected])
CurrentOpinioninFoodScience2019,29:14–19 ThisreviewcomesfromathemedissueonFoodmycology EditedbyMarinaVCopetti
ForacompleteoverviewseetheIssueandtheEditorial Availableonline13thJuly2019
https://doi.org/10.1016/j.cofs.2019.07.003
2214-7993/ã2019TheAuthors.PublishedbyElsevierLtd.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creative- commons.org/licenses/by-nc-nd/4.0/).
Introduction
Fungi are a major cause of spoilage in food since they haveagreat versality for growingsubstratesand condi- tionswhereothermicroorganismsarenotabletogrow[1].
Fungalspoilageofcheeseisaproblemandcausequality reductionduetovisibleorinvisibledefectssuchas off- odour and off-flavour. Some of the fungi growing on cheese may also produce mycotoxins, which lead to a foodsafetyissue.
Despite a lot of work in the dairies to reduce mould growth, fungal spoilage of cheese has significant eco- nomiclossesdueto productlossesandwaste,reduction ofthequality,additionalwork, andfoodsafety issuesif mycotoxinsareproduced.
Cheesecanbedividedintogroupsdependingonthewater activity(aw).Inaddition, therearecheeses ripenedwith moulds,likeblueorwhitemouldcheesesthatareripened withPeniclliumroquefortiandPenicilliumcamemberti,respec- tively. However, even if fungal contamination happens moreeasilyonsoft cheeses (highaw),fungi arecapable togrowonallsortsofcheeses.
Associated mycobiotaoncheese
Fungi responsible for problems in cheese production are diverse and belong to several genera asAcremonium,Alternaria, Aspergillus,Aureobasidium,Botrytis,Cladosporium,Epicoccum, Eurotium, Exophiala, Fusarium, Gliocladium, Lecanicillium, Mucor, Penicillum, Rhizopus, and Wallemia [2]. However, thegenusmostfrequentlyisolatedfromspoiled cheeseis Penicillium followed by Aspergillus [2,3–6]. Different Penicilliumspecieswhichare isolatedfromcheeseislisted inTable1.Becauseofavarietyofcheesetypeswithdifferent characteristics,thelarge variety of different fungal genera that can spoil cheese is not surprising. Many studies show thatevenifthereisalargevarietyofgeneraandspeciesthat occasionallyareisolatedfromaspecifictypeofcheese,there are still only a few species that are regularly dominating [4,6,7]. A certain food product has their own associated mycoflora[7]anddifferentcheesetypesmaythereforehave theirveryspecificmycofloraonvisiblemouldycheese.
Penicillumisthe dominationgenus(91%)on spoiled hard, semi-hardandsemi-softcheesesfromdifferentcountries[8].
Themost frequentlyisolated species were reportedto be Penicilliumcommune(42%),Penicilliumnalgiovense,Penicillium verrucosum, Pencicllium solitum, P. roqueforti, Penicillium crustosum, Penicillium atramentosum, Penicillium chrysogenum, andPenicilliumechinulatum.LaterKureetal.[9]alsoidentified P.communeasoneofthemostfrequentlyoccurringspecieson visiblemouldysemi-hardcheese togetherwiththeclosely relatedPenicilliumpalitans,andP.roqueforti[10].Garnieretal.
[3]identifiedP.communeandPenicilliumbialowienzenseasthe most common filamentous fungi in various French dairy products,whileP.crustosumandP.solitumwerethedominat- ingPenicilliumspecies associated with Italian hard cheese [11].
AlsoanewPenicilliumspeciesnamedPenicilliumgravinivaseiis isolatedfromItaliancheese[12].
Cheeseisnormally keptrefrigerated,someare vacuum packaged or gas flushed, hence the cheese spoiling mouldspecies in thosecases aredominated bypsycro- torelantspeciesthatcangrowatlowO2concentrations [13]. Both P. roqueforti and P. commune meet these criteriawhichmakethemamongthedominatingcheese spoilagemoulds.
Blue and white mould cheeses are mainly ripened with P. roqueforti and P. camemberti respectively, and often togetherwithGeotrichumcandidum.Eventhoughthesurface iscoveredbydesiredmoulds,theremaybespoilagemoulds too.AlsoonthesecheesetypesdifferentPenicilliumspecies areisolated[14].Othergeneraisolatedfrommouldripened cheese includeAlternaria,Aspergillus, Cladosporium,Mucor and Rhizopus [15,16]. Bekada et al. [16] isolated Mucor racemosus from Camemberti cheese and Mucor has been observedasso-called‘cat-hair’defectonsoftcheeses[17].
AtleastsixdifferentMucorspecieshavebeenisolatedfrom cheese,includingMucorcircinelloides,Mucorracemosus,Mucor hiemalisandMucorplumbeus.
Marı´n et al. [18] studied the environmental factors, in particularthewatercontent,thataffectthegrowthofthe mould species dominating on spoiled cheese. The results showed that decreased water content had an inhibitory effect on the growth of M. circinelloides and M.racemosus,whilePenicilliumandAspergillusweremore tolerant to water restriction. The environmental condi- tionsinfluencethedynamicsoffungalpopulationswhile growing on cheese, favouring certain fungal genera in differentstagesofthecheesemakingandripening[18].
Contamination sources
Mould contaminationof cheese can appear atdifferent stages of the production. The milk used for cheese
production is mostly pasteurised or heat treated before cheese making. Mould spores are in general not heat resistant,andhencethemilkdoesnotconsistanimpor- tantsourceofcontamination[2].However,heat-resistant sporescanoccasionallycausespoilage inheatprocessed cheeses suchas cream cheese [13].Rawmilk cheese is producedfromunpasteurisedmilk andmouldsporesin therawmilkmaythuslaterappearasvisiblemouldson thecheese[6].
The air in the production plant is contaminated with mouldsporesatdifferentlevels[6,19],andtheairrepre- sents one of themajor contaminationsources. Airborne sporescancontaminatethecurdinthevesselsandvats.
Mouldsporesthatenterthesurfaceofthecheesemaybe allowedtogrowonthecheeselaterintheprocessifthe growthconditionsaresuitable.Thecheesewillnormally beimmersedinbrineforacertainperiod(Figure1).As thebrinecanbeareservoirofmouldslikeP.commune[6]
itneedstoberinsedregularlytoremovemouldspores.In some dairies,pressurised airisusedtopress thecheese outofthevats.Thesocalled‘dairymould’G.candidum wasisolatedfrompressurisedairandwasreportedtobe themajorcontaminationsourcein thatdairy[19].
The level of mould spores in the packaging room is particularlycriticalfor vacuumpackedcheesesincethis isthelaststepbeforeripeningandrefrigeration.Species as P. commune, P. palitans and other xerofilic fungi can growatrefrigeratedtemperature.Aslongasthepackage is closed there will be no growth, but the spores will survive and may grow if the cheese is cut into smaller piecesandkeptwithoutvacuum.Cheesethatisripened withoutpackagingissensitiveforcontaminationfromthe airduring ripening[20].
In one study, the contamination source of cheese was identified to thecoatingprocess wherebrusheswhirled conidiaintotheairandcontaminatedthenextuncoated cheeses[21].Inanotherdairy,handlingofmouldycheese wasshowntobetheproblem[21].Despitehighpressure in the packaging room located far away from the place where mouldy cheeses were handled, identical isolates could be traced from mouldy cheese and the airin thepackagingroom.
Topreventmouldsporesfromvisiblemouldycheeseto spread in the production rooms, it is crucial to handle mouldy cheese extremely carefully. In some dairies cheeseswithvisiblymouldgrowthis‘cleaned’forsurface moulds [20]. This allows the problem mould for that cheese type to spread in the air and contaminate new cheesesthroughtheairand thesmear.Althoughtheair normally contains several different mould genera and species, only a low proportion of the airborne conidia constitutes the associated mould flora of the cheese produced in the plant [5]. However, if visible moulds
Table1
Penicilliumspeciesoncheesebycountry
Species Country References
Penicillium atramentosum
Norway,France [8]
P.bialowienzense France [3]
P.brevicompactum France [2,3,13]
P.chrysogenum Denmark,USA,Spain [6,8] P.commune Denmark,Greece,
France,UK,Australia, Germany,Azores,USA, Belgium,Japan,New Zealand,Czech Republic,Netherlands, Norway,Spain
[3,6,8,9,10]
P.crustosum Denmark,Italy,France, Azores,UK,Norway
[8,9,11]
P.echinulatum Australia,SouthAfrica, [8]
P.expansum Norway [9,10,13]
P.gravinivasei Italy [12]
P.palitans Norway [9,10]
P.nalgiovense Denmark,Greece, Slovakia
[8] P.roqueforti Denmark,germany,
Autralia,Greece,Malt, CostaRica,Norway
[8,9,10]
P.solitum Denmark,Greece,Italy, Norway,Spain,
[6,8,9,10,11]
P.verrucosum Denmark,Greece,Spain, [8]
P.viridicatum Australia [48]
from the cheese are allowed to spread to the air, the concentrationofproblemmouldsintheair,andthusthe productionenvironment,increasesandconsequentlyalso themouldcontaminationproblem.
Methodsfordetection ofmouldsand preventativemeasures
To assess the mould level and the composition of the mycobiota,appropriate methods need to be used[22].
Bothsurfacesamplingandairsamplingarenecessaryto do. DG18 (Dichloran Glycerol Agar) and MEA (Malt Extract Agar) are recommended as growth media for enumeration of fungal spores in air with both non- volumetricandvolumetricsampling[23].Theairsampler hasshown to give highernumber of species and mean numberofcolonyformingunits(CFU)/platethansettle plates;however,thetwomethodsshowedsimilarprofiles of dominating fungalgenera and speciesin air in adry curedmeatprocessingplant [24].Bothmethodscanbe usedto monitorthemycobiotaof theindoorair.
Thelevelofmouldsporesintheprocessingsites,storage rooms and air — and other filtration systems is recom- mendedsitestobemonitoredinordertoknowthenormal level of spores and consequently be in a position to discoverchangesthatmightpredictmouldcontamination problemsonthecheeseifthelevelishigherthannormal [23]. However, there might be rise in level of general numberofmouldsporeswithoutincreaseinthelevelof problemmoulds,hencemethodsthatmonitorthelevelof problem moulds will be most suitable.To monitor the levelofspoilagemouldsspecialisedgrowthmediashould beused.Dichlorancreatinemedium(CREAD)hasbeen provenasasuitableselectivegrowthmediumtomonitor thelevelof problemmouldsin dairies[25,26].
Inorderto identifythecontaminationsource, thefungi shouldbeidentifiedtoatleastspecieslevel.Sometimesit isnecessaryto identifybelowspecieslevel totrackthe mouldstrainsintheproductionplants[27,28].Different molecular methods have been used for this purpose [21,28,29]. MLST (multilocus sequence typing) is fre- quentlyusedinmedicalmycologyfortypingofmoulds, however in food mycology, the application is limited [22]. At present, the whole genome sequencing (WGS) of moulds is not practical as atool for problem solving in food plants. However, the development of WGSis fast, and it is expected thatWGS will become standard typing methods in a near future [22]. Using moleculartypingmethodstotracethespoilagemouldin the production plants it was demonstrated that mould sporescouldbetransportedfromroomtoroomwithstaff orequipment[28].Amplifiedfragment lengthpolymor- phism (AFLP) was found to be a useful method to identifycheese-contaminatingfungibelowspecieslevel, andasthesame strainsweredetectedrepeatedlyovera periodofmorethanayearitwasproventhattheproblem causingstrainwaswellestablishedin theplant [28].
Inorderto reduce mouldcontaminationofcheese, itis needed to work systematically with preventative mea- sures and measures that inhibit or reduce the mould
Figure1
MILK STARTER CULTURE
RENNET
FERMENTATION AND RENNETING IN VATS
PRESSING IN VATS OR PRESSING TOWERS
PRESSING IN CHEESE CONTAINERS
RELEASING CHEESE FROM CONTAINERS
BRINING
CHEESE FACTORYCHEESE FACTORY ORSEPARATE FACILITY ABOUT 20 HOURS 8 – 12 WEEKS 23 – 28 WEEKS («BEST BEFORE DATE»)
WRAPPING IN PLASTIC FILM
RIPENING
CUTTING TO CONSUMER PACKAGES
PACKAGING
Current Opinion in Food Science
Flowdiagramsemi-hardcheeseproduction.
growth.Preventativemeasuresincluderegularlycleaning anddisinfectionofequipment,includingconveyerbelts andvats,andtheproductionenvironment.Theairinthe production facility should have as low level of mould sporesaspossible,hencepreventativemeasuresasstrict zonal regulationsof theplant,filtration of theair,high- pressureairinroomswherethecheeseiskeptforalong period(duringripening)orjustbeforepackaging,maybe necessary.
HazardAnalysisCriticalControlPoint(HACCP)canbe used to identifycriticalcontrol pointfor mycotoxigenic moulds in food production [30]. For quality reducing mouldspeciesthepre-requisitesareimportant.Asystem- aticoverviewofpre-requisitesandproceduresthatimpact thelevelof moulds sporesin theproductionplantswill help to identify critical routines and procedures. A HACCP casestudywasusedin aGreekdairyplantfor incorporation of microbiologicalandmolecularmethods in HACCPmonitoringschemeofmouldandyeast[31].
Implementationofaconstantmonitoringoftheairqual- ityandtherecognition,asacriticalpoint,ledtoalower fungalairload.
Antifungal effectsonmould growth
After packaging, thesurface of thecheese maycontain non-visiblemouldsporesthatcangrowiftheconditions allow it. Hard cheese is often vacuum packed, while some,especiallygratedcheese,ispackedwithgas.Mod- ifiedgasatmospherepackaging(MAP)canpreventmould spores from sporulation since the majority of cheese spoilagemouldshaveanabsoluterequirementofoxygen [13]. Nevertheless,awide variety of mouldspecies are abletogrowunderreducedO2partialpressure(aslowas 1%),andforsomespoilagemoulds0%O2isnecessaryto preventgrowth[32].Mostspoilagemouldsaresensitive to high levels of carbon dioxide. Van Long et al. [32] indicate that CO2 levels above 50% was necessary to achieve fungal growthinhibition and up to90% carbon dioxidewasneededtoinhibitgrowth.Thesensitivityto carbon dioxide and the levelof O2required for growth vary among the spoilage species (unpublished data).
Hence the packaging method needs to be thoroughly testedtodeterminetheoptimalgasforpreventionofthe spoilage mouldforeachspecific product.
Toxin production
Secondary metabolites (mycotoxins) are low molecular weight metabolites produced by filamentous fungi.
Mycotoxins are foundin cheese primarilyas aresultof either indirect contamination,resultingfromthemanu- facture of cheese from animals which have ingested contaminated feed or directly resulting from mould growthoncheese[33,34,35].Thecheese-contaminating mouldspeciesmayproducemycotoxinsasochratoxinA, citrinin,cyclopiazonicacid,patulin,roquefortinC,myco- phenolicacid,PR-toxin,penicillicacid,isofumigaclavine
AandB,andandrastinA–D[36].Someofthesetoxins,as PR-toxin, are unstable in cheese matrix and is readily inactivatedorconvertedtoothercompounds[37].How- ever, othertoxins asochratoxinA(OTA), cyclopiazonic acidandsterigmatocystinhavebeen showntobestable under normal processing conditions [36]. The risk of mycotoxins in cheese is increasing when toxigenic moulds are allowed to grow during manufacturing and storage.
Themycotoxincyclopiazonicacid(CPA)hasbeenfound insamplesofwhitemouldcheese[38,39]andotherchees varieties[40].Insomeofthesamples,highconcentrations of CPA were found in commercially available cheese.
CPA is produced by certain Penicillium and Aspergillus species [13,36]. In samples with high CPA level, the toxinwasonlydetectedintheouterlayerofthecheese.
Fontaineetal.[41]didnotfindaflatoxinsinblueveined cheese, but 97.7%and 37.2%of thesamplescontained roquefortineCandmycophenolicacid,respectively.Pat- tonoet al.[42]examinedsemi-hardcheeseforthepres- enceofOTAandpatulin.TheyfoundOTAinboththe rindandtheinnerpartofthecheese,whilepatulinwas found mainly in the rind. Lo´pez-Dı´az et al. [43] found roquefortine C in anartisanal blue cheese.Coton et al.
[44]foundOTA andcitrinininComte´ cheese.
AflatoxinM1incheeseoccursduetotheuseofcontami- natedmilk[45].The presencevariesdueto thecheese typeandthereductionofthelevelincheesedependson different processing parameters as temperature, pH, pressing timeand soon. Forinstance, oaxacacheesein MexicoCitywassurveyedforpresenceofaflatoxinsand their hydroxylated metabolites [46]. Aflatoxin B1 and aflatoxicol weremostfrequentlydetectedin additionto eightotheraflatoxinvarieties,fortunatelyinrelativelylow levels.InastudyofcheeseinSerbia,however,Aflatoxin M1 was detected in samples of white cheese and hard cheese, and 13% of the samplesexceeded theadopted limit of 0.25mg/kg in theEuropean Union (Regulation 1881/2006)[47].
Conclusion
Tosummarise,mouldgrowthoncheeserepresentsbotha qualityand afoodsafetyproblem, andposessignificant economiclossesduetodisposalofproductsandincreased work load. Several mould genera may destroy cheese;
however,normallyjustafewfungalspeciesdominateona specific type of cheese. Penicillium is the major genus followed by Aspergillus. Cheese-contaminating mould speciesmayproducemycotoxins.Sometoxinsarefortu- natelyunstableincheesematrixandisreadilyinactivated orconvertedtoothercompounds.However,othertoxins as ochratoxinA,cyclopiazonicacidand sterigmatocystin have been shownto bestable undernormal processing conditions.Themainsourceformouldcontaminationof
cheese is the environment in the production facilities;
hence,thelevelofmouldsporesinthefacilitiesiscrucial.
Visiblemouldgrowth oncheese in theplant shouldbe avoidedinordertopreventproblemmouldstospread.In order to survey the level of fungal spores both surface samplingandairsamplingisnecessary.DG18(Dichloran GlycerolAgar)andMEA(MaltExtractAgar)arerecom- mendedgrowthmediaforenumerationofairbornefungal spores with both non-volumetric and volumetric sam- pling. For identification of the contamination source, identification at or below species level is necessary.
Further work should focus on methods for monitoring ofproblemmouldsandmethodsforidentifyingproblem moulds below specieslevel. The dairiesneed methods thatcanbeimplementedatsites.
Conflictofintereststatement Nothingdeclared.
Acknowledgement
ThisworkwasfinancedbyNorwegianAgricultureandFoodIndustry ResearchFundsgrantNo.262306.
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