Microbial quality of ice cream sold

openly by retail outlets in Turkey

1*

H. YAMAN , M. ELMALI , Z. ULUKANLI , M. TUZCU , K. GENCTAV

DepartmentofFoodHygieneandTechnology,FacultyofVeterinary,UniversityofKafkas,36100Kars,Turkey

DepartmentofBiology,FacultyofScienceandArts,UniversityofKafkas,36100Kars,Turkey

DepartmentofVeterinaryDivision,HighSchoolofVocational,UniversityofKafkas,36100Kars,TurkeyTel:+904742426800ext.1124Fax:+904742426853
*Correspondingauthor:Dr.HilmiYAMANEmail:hilmiyaman@hotmail.com

SUMMARY
Thisstudyaimedtoinvestigatemicrobiologicalqualityoficecreamsamples
soldopenly(insmallportionsfrombulkcontainersexposedtotheopenair)by
retailmarketsinTurkey.Thesamples(n=73)wereanalyzedtodeterminethe
hygienicstatusoftheicecreamsandalsoforthepresenceofsomeGram
positiveandGramnegativepathogenicbacteria.Hygienicparametersincluded
thetotalaerobicmesophilicbacteria(TAB),Enterobacteriaceae,coliforms,
Enterococcusspp.,yeastandmouldcounts.Thepathogensincluded
Staphylococcusaureus(S.aureus),Bacilluscereus(B.cereus),Escherichia
coli(E.coli),E.coliO157:H7,Salmonellaspp.,Yersiniaspp.Ofthe73ice
creamsexamined,4.1%ofthesampleshadunacceptablehygienicquality
5

accordingtothecriterion(10 cfu/g)recommendedinTurkishFoodCodex
(TFC),78%ofthesamplescontainedtheEnterobacteriaceaewhichhada
2

higherdetectionratethancoliforms(52%),rangingfrom10 to10 cfu/g.The

numbersofcoliformswerenotinaccordancewiththestandardofTFC(95
MPNcfu/ml).ConsideringthepercentagedistributionofEnterococcusspp.in
2

samples,47%oftheicecreamsampleswerewithintherangeof10 and10
2

cfu/g.Totalyeastandmouldcountsvariedbetween10 10 cfu/gand18%of
sampleswouldnotbeacceptable,basedonTFClevel.Thecountsregardingthe
yeastandmouldicecreamsamplessuggesttheneedforadequateheattreatment
andappropriatestorageconditions.E.coliwasfoundin15outof73icecream
samples,butinterestinglytherewasnoindicationforthepresenceofE.coli
O157:H7.Outof73icecreamsamples,9.6%gavepositiveresultforYersinia
spp.Five(6.8%)icecreamsampleswerefoundtobepositiveforthepresence
ofSalmonellaspp.while,24samplesyieldedpositiveforS.aureuswhichisin
2

therangeof10 to10 and15%ofthesamplesdonotcomplywiththeTFC

2

standards(10 cfu/g).B.cereuswaspresentin19%oficecreamsamples.The
detectionlevelforB.cereus(+)samplesinthisworkcannotberegardedas
potentialhazardaccordingtoTFC(No:24511)whichisrecommendedtobe
4

lowerthan1.0x10 cfu/g.Thisstudyhasindicatedthatthehygienicqualityof
theinvestigatedopenicecreamssampleswereinaqueate.Consideringthe
Enterobacteriaceae,coliforms,Enterococcusspp.,yeastandmouldcounts,and
thepresenceofS.aureus,E.coli,Salmonellaspp.,icecreamssoldinopenmay
posepotentialriskforpublichealthespeciallyforvulnerablepeople.Thisstudy
supportsthenecessityofprovidinghygienicprecautionsbyproducersand
retailersandtheircontrolperiodicallyinTurkey.

KEY WORDS : Ice cream, Food Safety, Pathogens,

Micro-biological Quality, Public Health

RSUM
Qualitmicrobiologiquedeglacesvenduesenvracdanslespiceries
enTurquie
Lobjectifvisparcetterechercheestlanalysedelaqualitmicrobiologique
dchantillonsdeglacesvenduesouvertement(lesglacessontvenduesende
petitesportionsdansdesgrandsrcipientsexpossenpleinair)parlespiceries
enTurquie.Les73chantillonsonttanalysspourlesbactriespathognes
GrampositifetGramngatif.Lesparamtreshyginiquesrecherchsont
t:lafloretotalearobiemsophile,lesEnterobacteriaceae,lescoliformes,
lesEnterococcusspp.,lednombrementdeslevuresetmoisissures.Les
pathognesrecherchssontlesStaphylococcusaureus(S.aureus),lesBacillus
cereus(B.cereus),lesEscherichiacoliO157:H7,les
Salmonellaspp,etlesYersiniaspp.Surles73chantillonsanalyss,4.1%de
ceuxciontdpasslesnormeshyginiquestabliesparlecodexdelali
mentationturc(TFC.78%deschantillonscontiennentdesEnterobacteria
ceae.Lepourcentageobservdescoliformesnecorrespondpasauxnormesdu
CodexdelAlimentationTurc(95MPNcfu/ml).Lorsquonprendencon
sidrationlepourcentagedeladispersiondelEnterococcussppdansles
chantillons,47%deschantillonsdeglaceavaientlesvaleurscomprisesentre
2

10 et10 cfu/g.Lednombrementdeslevuresetdesmoisissurestaitcompris
2

entre10 et10 cfu/get,selonlesnormesduCodexdelAlimentationTurc,18

%deschantillonsneseraientpasacceptables.Nousavonsnotlaprsence
dE.colidansles15chantillonsdes73analyssmaisilnyavaitaucunsigne
delaprsencedE.coliO157:H7.
9.6%des73chantillonsontdonnunrsultatpositifpourYersiniaspp.Pour
laprsencedeSalmonellaspp,5chantillons(6,8%)deglaceontdonnun
rsultatpositif.24chantillonsontdonnunrsultatpositifpourlaprsencede
2

sanitaires.Cetterechercheadmontrquelesqualitshyginiquesdes
chantillonsdeglacesvenduesouvertementtaientinsuffisantes.Laprsence
dEnterobacteriaceae,decoliformes,dEnterococcusspp,etdecertaines
bactriespathognespeutreprsenterunrisquepotentielpourlasantpublique,
surtoutpourlesenfantsetpourlespersonnessensibles.Cetravailmontrela
ncessitdamliorerlespratiqueshyginiqueschezlesproducteursenTurquie
etdeffectuerdescontrlesrguliers.

S.aureus;cettebactrieatobservedesteneursallantde10 a10 cfu/get

2

15%deschantillonsntaientpasconformesauxnormes(10 cfu/g)duCodex
delAlimentationTurc(TFC).B.Cereustaitprsentdans19%des
chantillonsdeglacemaisaunniveauinfrieurauxrecommandations

MOTS CLS : glaces (crme glace), scurit

alimentaire, bactries pathognes, qualit
microbiologique, sant pu-blique, hygine.

ofmilk,cream,evaporatedorcondensedmilk,

Introduction
Icecreamisapopularproductconsumedparticularlyin
summeraswellasthroughoutallyearandcontinuestobea
dominantinterestoflargesegmentsofthepopulation[18].
Theingredientsoficecreammaybevariouscombinations

driedmilk,coloringmaterials,flavors,fruits,nuts,sweet
eningagents,eggsandeggsproducts,andstabilizers.Any
ofthesemaycontributemicroorganismsandaffectthe
qualityoftheproductasjudgedbyitsbacterialloadorits
contentofvariousspecificspeciesofbacteria[9,26].Time
dependentheatingduringtheicecreammakingreduces
largelythevegetativeformsofthemicroorganisms.Onthe

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458

otherhand,sporebearingmicroorganismsmaywellpose
risksthroughconsumptionofthiskindofmilkproducts.
Furthermore,thepresenceofpathogensinicecream
samplesismostlybymeansoftoolsandequipments,water,
workers,environment,packagingmaterialsand
contaminationsduringthetransportationanddistributionof
icecream[4,6,22].
Thepresenceofpathogenicmicroorganismsinicecreamsuch
asSalmonellaspp.[5,8],Staphylococcusaureus,Escherichia
coli[5,8,12,14,22,25]havebeenwelldocumented,but
examinationofpathogenicbacterialikeBacilluscereus,Yers
iniaenterocolitica,Listeriamonocytogenes,Brucellaspp.and
E.coliO157:H7havebeenrarelystudied.Thesestudiesindi
catedthenecessityforamoresteadymicrobialexaminationof
icecreamssinceicecreamisparticularlyconsumedbychil
drenofvulnerableagegroups[15,28].Icecreamsamplesin
thisworkwerethereforeexaminedintermsofmicrobialcounts
thatallowthequantitativecheckingofprincipalhygienic
parametersincludingthetotalaerobiccounts,coliforms,
Enterobacteriaceae,Enterococcispp.andyeastandmould.
Additionally,examinationofthepathogenicbacterialikeE.
coli,E.coliO157:H7,Yersiniaspp.,Salmonellaspp.,

S.aureus,B.cereus,werealsoperformed.

sampleswascarriedoutinaccordingwiththemethodof
WARKEETAL.[28].Traditionalmicrobiologicalmethods
andmediawereusedfortheisolationandenumarationoftotal
aerobicmesophilebacteria,coliforms,Enterobacteriaceae,
Enterococcispp.,yeastmouldandthepathogenicbacterialike
E.coli,E.coliO157:H7,Yersiniaspp.,Salmonellaspp.,S.
aureus,B.cereus(Table1).
ThenumberofE.coliwasdeterminedbythemostprobable
number(MPN)techniquewiththreetubesusingBrilliant
GreenBile2%Broth(Oxoid,CM31).ThepresenceofE.coli
intubeswasconfirmedbystreakingonEndoAgar(Oxoid,
CM479).Colonieswithcharacteristicgreenishmetaliccolor
wereconfirmedasE.coliwiththeindole,methylred,Voges
Proskauer,andcitrateutilization(IMVIC)tests.Fortheidenti
ficationofS.aureus,typicalandatypicalpresumptiveStaphy
lococcispp.colonieswereexaminedbyGramstain,coagulase,
catalase,andlatexagglutination(Oxoid,FT0203)tests.
ToidentifyB.cereus,presumptivepinkpurple,opaqueB.
cereuscoloniesweresubjectedtoconfirmatorytestsofGram
stain,catalase,motility,nitratereduction,tyrosinedecompo
sition,anaerobicfermentationofglucose,VogesProskauer
reactionandproductionofacidfrommannitolandarabinose.

ForSalmonella,typicalSalmonellaspp.colonieswere
subjectedtothefurtherbiochemicalandserologicalcharac
terizationtestsusingTripleSugarIronagar(TSIA)(Merck
103915)andLysineIronAgar(LIA)(Merck111640),and
agglutination(OxoidFT203)test.

Materials and methods

Atotalof73icecreamsamples(100geach)werecollected
andexaminedduringJulyandAugust,2004inKars,Turkey.
Thesamplesweretransportedtothelaboratoryinacoolbox
andstoredat20Cpriortoexamination.Thepreparationofthe

ForE.coliO157:H7,colourlessandsorbitolnegative
presumptivecolonieswerestreakedonFluorocultViolet
RedBileagar(Merck1.04030)andincubatedat42Cfor
2448h.ThenGramstain,catalase,andIMVICtestswere

performedtotheisolates.Thoseconfirmedwith
biochemicaltestswerethencheckedwithDryspotE.coli
O157latexagglutination(Oxoid,200075)test.Inparallel,
isolatesidentifiedasE.coliO157werealsotestedwith
antiseraO157andH7(Oxoid,DenkaSeikan210753and
211057)asdescribedbythemanufacturer.
ForYersiniaspp.,suspectedcoloniesweresubjectedtoGram
stainandfurtherbiochemicalcharacterizationtestsofcatalase,
oxidase,urease,motilityinSIM(OxoidCM435)medium,
growthonKliglerIronAgar(KIA)(Oxoid,CM33).

63.3%,44%,and49.27%inthecitiesofKars,Ankara,Aydn
andAntalyaofTurkey,respectively.[5,8,16,25].
UnsatisfactorylevelsofTABhavealsobeenreportedinmany
othercountries.InthestudyofMasud[19]fromPakistan,72
6

%ofthesampleshadTABcountsover10 cfu/g.Fromthe
cityofBangaloreinIndia,SaradaandBegum[23]found53%
5

ofthesampleshadcountsof10 cfu/g.MAIFRENIETAL
[17]fromUdineinItalyreportedthat8%ofthesampleshad
5

TABcountsexceeding10 cfu/g.WARKEETAL.[28]from
Indiaalsoreported33%ofthesampleshavingexcessive
6

Results and Discussion

TheresultsofthisstudyarepresentedinFigure1and2.The
2

aerobmesophilebacteria(TAB)rangedbetween10 10 cfu/
1

g .Icecreamisconsideredhavingunacceptablehygienic
5

qualitywhentheTABexceeds10 cfu/g accordingtothe

TurkishFoodCodex(TFC)foricecream(No:24511)[2]
(Table2).Only4.1%ofthesamplesinthecurrentstudy
exceededthisvalue.Inpreviousstudies,lowlevelsofTAB
werereportedbySAGDICETAL.[22]andKanbakanetal.
1

[13]intherangeof2.1x10 2.6x10 cfu/g (Isparta,Turkey)

4

and1,7x10 1,7x10 cfu/g (Denizli,Turkey),respectively.

Onthecontrary,unsatisfactorydetectionratefoundforTABin
thepresentworkwaslowerthantheresultsreportedas33.3%,
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countsof10 cfu/ml,whichdidnotcomplywiththeIndian
standard.Theresultsfoundinthosestudiesandpresentwork
indicatethaticecreamssoldinsmallportionsfrombulk
containers,exposedtotheopenair,havehighmicrobialload,
indicatinglowhygienicqualityoftheproductsinmany
countries.Thesehighcountsmayoriginatefromtheinitial
microfloraofrawmilkandtheotheringredientsandtheir
quality,theenvironment,insufficientheattreatmentandpoor
personalhygiene.Ithasbeenpreviouslystatedthatproduction
oficecreamlocallyonasmallscaleratherthanindustriallyis
alsoamajorfactorassociatedwithcontaminationoficecream
[4,8,13].

Seventyeightpercentageofthesamplescontainedthe
Enterobacteriaceaewhichwasahigherratethanfaecal
coliforms.IncidenceofEnterobacteriaceae(53%)inice
creamsampleswasalsoreportedbyEROLETAL.[8].
Enterobacteriaceaeinfoodproductsindicatesfaecal
contamination.Therefore,microbiologicalqualityofthe
samplesinthisstudyseemstobelow.Poormicrobiolog

MICROBIAL QUALITY OF ICE CREAM SOLD OPENLY BY RETAIL OUTLETS IN TURKEY

459

Bacteria
MediaUsed
Incubation
Incubation

Temperature(C)
Time(days)

Aerobmesophile
PlateCountAgar(Oxoid,CM463)
30C
23
bacteria

Enterococcispp.
KanamycineAesculinAzideAgar
37C
12

(Oxoid,CM591)

Enterobacteriaceae
VioletRedBileGlucoseAgar(OxoidCM485)
37C
12

Coliforms
VioletRedBileLactoseAgar(OxoidCM107)
37C
12

Escherichiacoli
BrilliantGreenBile2%Broth(Oxoid,CM31)
37C
12

EndoAgar(Oxoid,CM479)
42C
12

Escherichiacoli
ModifiedNovobiocinECBroth(mEC+n,Merck1.10765)
42C
1

CTSMAC(OxoidCM813withSR172E)
42C
12
O157:H7

FlurocultVioletRedBile(Merck1.04030)
42C
12

Staphylococcusaureus
BairdParkerAgar(OxoidCM275)
37C
12

Bacilluscereus
CereusSelectiveAgar(Merck1.05267)
30C
12

BufferedPeptoneWater(OxoidCM509)
37C
1
Salmonellaspp.
RappaportVassiliadisBroth(Merck1.07700)
43C
1

SalmonellaShigellaAgar(Merck1.07667)
37C
12

Yersiniaspp.
TryptoneSoyaBroth(OxoidCM129)
4C

7,14,21

CefsuladinIrgasanNovobiocinAgar(OxoidCM653)
25C
2

Yeastmould
RoseBengalChloramphenicolAgar(Oxoid,CM549)
25C
45

TABLE1.Traditionalmethodsandmediausedfortheisolationandenumerationofbacteria
FIGURE1.Thepercentageandviablecountrangesofbacteriaandthe
presenceofsomepathogensinicecreamsamplessoldopenly*.

icalqualityofthesamplesmaybeduetoinsufficientheat
treatment,unhygienichandlingoftheicecreamsbeforeand
duringstorage[11],anduseofpoorqualitywatersinceit
hasbeenrevealedthatpoorqualityofwaterusedtowash
theservingscoopcanbecomesignificantsourceof
contaminationfortheaerobicmesophilicbacteria,coliforms
andE.coli[7,13,29].

TAB:Totalaerobmesophilebacteria,COL:Coliforms,ENTB:Entero
bacteriaceae,ENTC:Enterococcusspp.
5

*TurkishFoodCodexrequiresmaximum1.010 cfu/mlforTAB,95MPN
4

cfu/mlforCOL,1.010 cfu/mlforB.cereus,110 cfu/mlforS.aureus,

2

1.010 cfu/mlformould,1.010 cfu/mlforyeast.Itdoesnotstateany

criteriaforENTB.andENTC.(TCFNo:24511).

FIGURE2.Thepercengate(%)ofentericpathogenicmicroorganismsinice
creamsamples.

Coliformsweredetectedfrom52%ofthesamplesintherange
2

of10 to10 cfu/gandtheirnumberswerenotinaccordance

withtheTFCstandardof95MPN/ml(Table2).Manyreports
dealingwiththeoccurrenceofcoliformsinicecreamhave
beenaccumulated.Inthosestudies,variousratesofcoliforms,
whichdidnotcomplywiththeTFCstandardinTurkey,were

reportedas13.3%,40%,88.4%,96%and83%bySAGDIC
ETAL.[22],LELOGLUETAL.[16],TOKLUAND
YAYGIN[25],KANBAKANETAL.[13],andKIVANCET
AL.[14],respectively.Likewise,insomedeveloping
countries,suchasPakistanandIndia,severalratesofcoliforms
werealsoreportedas66%[19].and100%[28],respectively.
Thepresenceofcoliformsinicecreamsamplesmayindicate
insufficientheattreatment,unhygienicorlowhygienic
materialsortoolsused,waterbeingcontaminatedorgood
manufacturingpracticebeingnotfollowed.

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460

werecontaminatedwithE.coliandvariousincidenceratesof
3.33%,22%,and70%werealsoreportedbyEROLETAL.
[8],KIVANCETAL.[14],andTOKLU&YAYGIN[25]in
differentcitiesofTurkey.ConsideringtheEnterobacteriaceae,
coliformsandthepresenceofE.coliinsamplesmayindicatea
lackofgoodmanufacturingpracticeduringtheproductionand
icecreamproducedindomesticorcateringpremisesmaybe
relativelyimportantvehiclesforthecausesofgastrointestinal
diseases.Theseresults,therefore,revealsaneedforimple
mentingregulatorymeasureslikegoodmanufacturingprac
tices,hygienicdistributionandretailstoragepracticesfor
ensuringmicrobiologicalsafetyoficecreamsoldinopen
containers.Likewise,personalhygieneshouldbeemphasized
asKANBAKANETAL.[12]statedthatcoliformcontamina
tiononthehandsofpersonnelinsalesdepartmentwashigher
thanonthehandsoffactoryworkersandhandwashingwith
soaponlymaynotbeenoughforthecleaningofhands.

Microorganisms
Max.Numbers

Aerobmesophilebacteria(cfu/ml)
5

1.0x10

Coliform
95

E.coli
9
Salmonellaspp.
Absentin25g

Ofthe73icecreamsamplesexamined,9.6%gavepositive
resultforYersiniaspp.Thedetectionratewasextremelylower
thanthefindingsofWARKEETAL.[28],whoreportedthat
100%oftheirsampleswerecontaminatedwithYersiniaspp.,
buthigherthantherateof2.5%reportedbyPEDERIVAAND
GUZMAN[21].Experimentalstudieshaveshownthatthe
growthofYersiniaspp.aretemperaturedependentandthisis
explainedbytheselectiveeffectofrefrigerationtemperature
whichismorefavorableforthegrowthofYersiniaspp.than
otherpathogenslikeE.coli,S.Typhimurium,S.aureus[1].
ThelowincidenceofYersiniaenterocoliticainthisstudy,in
comparisonwithotherpatho

L.monocytogenes
Absentin25g

Staphylococcusaureus(cfu/ml)
2

1X10

Bacilluscereus(cfu/ml)

1.0x10
Mould(cfu/ml)
2

1.0x10
Yeast(cfu/ml)
3

1.0x10
a

BasedonMPNTable(/ml), Appliestoflavoredicecream.*Modified
fromTurkishFoodCodexStandardsforplainandflavoredicecream(No:
24511).
Table2.TheTurkishFoodCodexmicrobiologicalstandardsforicecream

E.coliisanindicatorforfaecalcontaminationandthepossi
bilityofthepresenceofentericpathogens.E.coliwasfoundin
15outof73icecreamsamples,ThecountofE.coliwasfound
2

tobehigherthan1.1x10 MPN/ginallpositivesamplesand
washigherthanthatofTAMSUTANDGARCIA[24]and
Eroletal.[8].However,therewasnoindicationforthe
presenceofE.coliO157:H7inourstudy.Thismaybedueto
lowincidenceofE.coliinmilkandmilkproducts.Onthe
contrary,higherincidenceratesthanourresultwerealso
reported.MASUD[19]foundthat46%ofthesamples(n=50)

gens,maypresumablybeduetotheinefficientstorage
conditionswhichmayfavortheovergrowthofother
microorganismsincludingpathogens.Transmissionofthis
psychotropicbacteriumviafoodchainhasnotbeen
reported[28]butPEDERIVAANDGUZMAN[21]stated
thaticecreammayconstituteapossibletransmissionpath
forY.enterocolitica,andmightleadtogastroenteritis
outbreaksamongchildrenconsuminggreatamountsofice
cream,paticularlyduringthehotseason.Therefore,
contaminatedicecreamsamplesmaybeariskytypeof
foodforpublichealthintermsofcarryingtheYersiniaspp.
AsshowninFigure2,five(6.8%)sampleswerefoundtobe
positiveforthepresenceofSalmonellaspp.Thedetectionrate
forSalmonellaspp.wasnotinagreementwiththeresultsof
MAIFRENIETAL.[17],KIVANCETAL.[14],WARKEAL
[28],ASLANTAS[3],andKANBAKANETAL.[13]who
reportednoSalmonellaspp.intheiricecreamsamples.
However,comparingtoourresults,lowerfrequencyofSalmo
nellaspp.contaminationhasbeenalsoreportedinVenezuella

andCamerun,rangingfrom1%to5%[24,30],respectively.
Likewise,detectionrateofSalmonellaspp.inourstudywas
significantlylowerthantherateof53%reportedbyDIGRAK
ANDOZCELIK[5].ThepresenceofSalmonellaspp.inice
creammaypossiblybeduetotheeitherfresheggsoregg
powderusedintheicecreamproductionasbeingstatedin
previousworks.ThepresenceofSalmonellaspp.mayposea
greatriskforpublichealthsinceSalmonellaoutbreaksfromice
creamhavebeenreportedpreviously[10,20,27].
ConsideringthepercentagedistributionofEnterococcusspp.
2

countsinthesamples,47%werewithintherangeof10 and
4

10 cfu/g,withthemostbeingdetectedat10 cfu/g.In
3

previousworks,thecountsof<1.0x10 cfu/ginsome(8994
%)icecreamsampleswerereported[17].Inarecentwork,
EROLETAL.[8]foundEnterococcusspp.countsranging
2

from10 to10 cfu/g,withthemostbeingdetectedat10

cfu/ginAnkara,Turkey.Theirincidencefrequencyof87%
forEnterococcusspp.werecomparativelyhigherthanour
result.ThecountforEnterococcusspp.isbeingconsideredas
oneoftheparametersusedforfoodhygienequality.Low
RevueMd.Vt.,2006,157,10,457462

hygienicqualityofthesamplesregardingEnterococcusspp.
occurrenceinthepreviousandcurrentworkmayhavebeen
resultedfrominsufficientheattreatmentexposedtomilk
duringtheproductionorfrompostcontamination.
Inthepresentstudy,24samplesyieldedpositiveforS.aureus
2

rangingfrom10 to10 cfu/gand15%ofthesamplesdonot

2

complywiththeTFCstandardof10 cfu/g.TheabsenceofS.
aureusinicecreamsampleshasbeenrarelyreportedinseveral
studies[4,17,22,29].Ontheotherhand,lowerorhigher
incidenceratesofS.aureusthanourresultinthisstudyhave
beenreported.InAnkaraandElazig,Turkey,S.aureuswas
presentin10%oftheopenicecreamsamplesatthecountsof
3

10 cfu/g.InAydin,Turkey,LELOGLUETAL.[16]found
2

thisrateas20%atthecountsabovethesafelimitlevelof10
cfu/ml.Higherdetectionratesof62.3%and100%,atthe
countsabovethesafelimitlevelwerealsoreportedby
KIVANCETAL.[14]andWARKEETAL.[28],
respectively.ThepresenceofS.aureusmayberesultedfrom
eitherinsufficientpasteurizationofmilk,orhumanexposure.
Inhumans,themainreservoirofS.aureusisthe

MICROBIAL QUALITY OF ICE CREAM SOLD OPENLY BY RETAIL OUTLETS IN TURKEY

461

nasalcavity.Theorganismfindstheirwaytotheskinand
intowoundseitherdirectlyorindirectly.Themostcommon
skinsourcesarearms,hands,andface.Inadditiontoskin
andnasalcavities,S.aureusmaybefoundintheeyes,
throatandintestinaltract.Fromthesesources,theorganism
findsitswayintoairanddust,ontoclothing,andinother
placesfromwhichitmaycontaminatefoods[11].Itis
obviousfromthepreviousandthepresentdatathatice
creamsamplesarefrequentlysubjectedtoStaphylococci
spp.contaminationwhichmayindicateinadequatepersonel
hygieneofworkersorsalespeople.
Atpresent,thereisnocriterionforB.cereusintheTCFfor
plainicecreamasthereisforflavoredicecream.B.cereuswas
detectedin19%oftheicecreamsamplesuptothecountsof
4

10 cfu/g.ThiswaslowerthanofapreviousreportofWARKE
ETAL.[28]whofoundtheincidencerateof40%forB.
cereusintheirsamples.ThedetectionlevelforB.cereus(+)
samplesinthisworkcannotberegardedaspotentialhazard
accordingtotheTFCstandards,whichisrecommendedtobe

toxificationsresultingfrompathogenicmicroorganisms,
workersandsalespeopleinbothicecreamproducingcatering
premisesshouldberegularlycheckedforsustainingthe
favorablehygienicstatus

Acknowledgements
TheauthorswishtothanktheStatePlanningOrganization
(DPT)forsupportingthisstudyintheregionofKars,Turkey,
asthisworkcannotbeaccomplishedwithouttheirhelp.

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2

Totalyeastandmouldcountsvariedbetween10 10 cfu/
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factorynumberswerealsoreportedinpreviousstudies.Erol
etal.[8]foundahigherportion(56.6%)oftheirsamples
beingunsatisfactory.Inanotherstudy,60%ofthesamples
4

containedtheyeastandmouldbetween10 and10 cfu/ml.

[28].Thecountsofyeastandmouldinthesamplessuggest
theneedforthecontrolofadequateheattreatmentofice
creamandappropriatestorageconditionsincatering
premises.
Inconclusion,thecurrentinvestigationhasindicatedapoor
overalllevelofhygieneintheserviceofopenlysoldicecream
inKars,Turkey.Thecountsofmicroorganismsabovethe
recommendedcriteriaandthepresenceofsomegroupsof
pathogenicbacteriamayposeariskforpublichealthpartic
ularlyforchildrenandvulnerableelderlypeople.Itisclear
fromthepreviousandcurrentstudiesthatthereisanecessity
fordevelopingthehygienicstatusoflocallyproducedice
creamindomesticorcateringpremisesinTurkey.Thus,good
hygienepractisesshouldimprovethehygienicqualityofice
creamespeciallyinallsteps,postpasteurisationandatreatil
level.Anincreasedlevelofstafftrainingandtransferof
knowledge,especiallyinrelationtofoodsafety,handling,
maintainingandcleaningofmachineandtoolsmayimprove
thesituation.Furtherimprovementsshouldbesoughtin
personnelhygieneandthegeneralhygieneconditionsof
premises.Themandatoryadoptionofafoodsafetymanage
mentsystembasedontheHazardAnalysisCriticalControl
Point(HACCP)shouldimprovethequalityoficecream.The
qualityoftherawmaterialpriortoprocess,manufacturingand
storageoftheproductsunderappropriateconditionsshouldbe
givenapriorityandalsoinordertopreventtheinfectionsand

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