Table Of ContentBMJ2012;344:e363doi:10.1136/bmj.e363(Published24January2012) Page1of10
Research
RESEARCH
Consumption of fried foods and risk of coronary heart
disease: Spanish cohort of the European Prospective
Investigation into Cancer and Nutrition study
OPENACCESS
Pilar Guallar-Castillón associate professor12, Fernando Rodríguez-Artalejo professor12, Esther
Lopez-Garciaassistantprofessor12,LuzMLeón-Muñozpostdoctoralresearchfellow12,PilarAmiano
epidemiologist32,EvaArdanazepidemiologist,headofsection42,LarraitzArriolaepidemiologist 32,
AurelioBarricarteepidemiologist,headofservice42,GenevieveBucklandnutritionalepidemiologist6,
María-Dolores Chirlaque specialist in preventive medicine and public health72, Miren Dorronsoro
unitchief32,José-MaríaHuertaresearchassociate72,NereaLarrañagaepidemiologist32,PilarMarin
registerednurse42,CarmenMartínezseniorscientist92,EstherMolinaresearchassociate92,Carmen
Navarroseniorscientist,headofdepartment728,JRamónQuirósepidemiologist10,LaudinaRodríguez
medical doctor10, María José Sanchez professor and director of research92, Carlos A González
senior scientist, unit chief6, Conchi Moreno-Iribas epidemiologist245
1DepartmentofPreventiveMedicineandPublicHealth,SchoolofMedicine,AutonomousUniversityofMadrid,28029Madrid,Spain;2CIBERde
EpidemiologíaySaludPública,Spain;3PublicHealthDivisionofGipuzkoa,InstitutoInvestigaciónIISBioDonostia,BasqueGovernment,Donostia,
Spain;4PublicHealthInstituteofNavarra,Pamplona,Spain;5DepartmentofPediatrics,DepartmentofObstetricsandGynecology,andPreventive
Medicine,AutonomousUniversityofBarcelona,Barcelona,Spain;6UnitofNutrition,EnvironmentandCancer,CancerEpidemiologyResearch
Programme,CatalanInstituteofOncology,HospitaletdeLlobregat,Barcelona,Spain;7DepartmentofEpidemiology,MurciaRegionalHealthCouncil,
Spain;8DepartmentofPublicHealthandPreventiveMedicine,UniversityofMurcia,Spain;9AndalusianSchoolofPublicHealth,Granada,Spain;
10PublicHealthandHealthPlanningDirectorate,Oviedo,Asturias,Spain
Abstract 1.07(0.83to1.38),andinthefourthquarterwas1.08(0.82to1.43;P
ObjectiveToassesstheassociationbetweenconsumptionoffriedfoods fortrend0.74).Theresultsdidnotvarybetweenthosewhousedolive
andriskofcoronaryheartdisease. oilforfryingandthosewhousedsunfloweroil.Likewise,noassociation
wasobservedbetweenfriedfoodconsumptionandallcausemortality:
DesignProspectivecohortstudy.
multivariatehazardratioforthehighestversusthelowestquarteroffried
SettingSpanishcohortoftheEuropeanProspectiveInvestigationinto
foodconsumptionwas0.93(95%confidenceinterval0.77to1.14;Pfor
CancerandNutrition.
trend0.98).
Participants40757adultsaged29-69andfreeofcoronaryheart ConclusionInSpain,aMediterraneancountrywhereoliveorsunflower
diseaseatbaseline(1992-6),followedupuntil2004.
oilisusedforfrying,theconsumptionoffriedfoodswasnotassociated
MainoutcomemeasuresCoronaryheartdiseaseeventsandvital withcoronaryheartdiseaseorwithallcausemortality.
statusidentifiedbyrecordlinkagewithhospitaldischargeregisters,
Introduction
populationbasedregistersofmyocardialinfarction,andmortality
registers. Fryingisoneofthemostcommonlyusedmethodsforcooking
ResultsDuringamedianfollow-upof11years,606coronaryheart inWesterncountries.Whenfoodisfrieditsnutritionalcontent
diseaseeventsand1135deathsfromallcausesoccurred.Compared changes—thefoodloseswaterandtakesupfat,increasingits
withbeinginthefirst(lowest)quarteroffriedfoodconsumption,the energydensity.12Fryingmodifiesboththefoodsandthefrying
multivariatehazardratioofcoronaryheartdiseaseinthesecondquarter mediumbecauseoilsdeteriorateduringfrying,especiallywhen
was1.15(95%confidenceinterval0.91to1.45),inthethirdquarterwas reused,throughtheprocessesofoxidationandhydrogenation,
Correspondence to: P Guallar-Castillón [email protected]
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RESEARCH
leadingtoalossofunsaturatedfatsandanincreaseintrans Participantswereaskedaboutfoodconsumedinatypicalweek
fats.1Thusfriedfoodabsorbsdegradationproductsofthefrying duringtheprevious12months.Foodsconsumedatleasttwice
oil.3Atthesametime,fryingmayalsoimprovepalatabilityby amonthwererecorded.Thedietaryhistoryquestionnaire
makingfoodcrunchy.45 recordedinformationonupto662differentfoods,including
Friedfoodshavebeenassociatedwithvariouscardiovascular thoseconsumedindividuallyandthoseconsumedaspartof203
riskfactorsincrosssectionalstudies.InSpain,thePizarrastudy recipesandregionaldishes.Ofthesefoods,212werefried.We
of1226adultsshowedthatconsumptionoffoodfriedwith calculatedenergyandnutrientintakeusingtheEPICfood
reusedoilswasassociatedwithahigherprevalenceofarterial compositiontable.21
hypertension.6Furthermore,acrosssectionalanalysisofthe Informationoncookingmethodswascollectedaspartofthe
SpanishcohortoftheEuropeanProspectiveInvestigationinto dietaryhistoryquestionnaire.Thesamefoodmaybecookedby
CancerandNutrition(EPIC)studyconcludedthatconsumption severalmethodsaspartofasinglerecipe.Forexample,inthe
offriedfoodswaspositivelyassociatedwithgeneralandcentral preparationofpaella(atypicalSpanishrecipe),riceisbothfried
obesity.7Similarly,intheSUN(SeguimientoUniversityof andboiled.Thus,friedfoodwasdefinedasfoodforwhich
Navarra)cohortinSpain,morefrequentconsumptionoffried fryingwastheonlycookingmethodused.Suchfoodcouldbe
foodsatbaselinewasassociatedwithahigherriskofbecoming deepfriedorpanfriedanditcouldbebattered,crumbed,or
overweightorobeseduringasixyearfollow-up.8Lastly,in sautéed.Toestimatetheabsorptionoffatfromfrying,weused
anothercrosssectionalstudyin2090Italianadults,consumption anabsorptioncoefficientforeachfriedfood.18Wealsorecorded
offriedfoodwasassociatedwithlowerhighdensitylipoprotein thetypeofoilusedfordressing,cooking,andfrying.
cholesterollevelsandalargerwaistcircumference.9
Assessment of non-dietary variables
Onlyafewstudieshaveevaluatedtheeffectoffriedfoodson
riskofcardiovasculardisease.Acase-controlstudyinCosta Informationondemographicvariables,educationallevel,
Ricafoundnoassociationbetweenconsumptionoffriedfoods smoking,andphysicalactivitywasobtainedthroughinterview
andriskofnon-fatalacutemyocardialinfarction.10Another atrecruitment.Physicalactivitywasassessedwithavalidated
case-controlstudy,INTERHEART,observedapositive questionnairethatincludedactivityatwork,athome,andduring
associationbetweenfriedfoodsandacutemyocardial leisuretime.22Participantswerealsoaskediftheyhaddiabetes
infarction.11 mellitus,hypercholesterolaemia,hypertension,cancer,orangina,
Therefore,althoughinterestintheassociationsofdietary orhadexperiencedmyocardialinfarctionorstroke.Inaddition
patternsandspecificcookingtechniqueswithriskofdiseaseis theywereaskedtoreporttheirmenopausalstatusandanyuse
increasing,12littleisknownaboutthehealtheffectsoffried oforalcontraceptivesorhormonereplacementtherapy.Trained
foods.Weevaluatedprospectivelytheassociationbetween observersusedstandardisedprocedurestomeasureweight,
consumptionoffriedfoodsandtheriskofcoronaryheartdisease height,andwaistcircumference.Thebodymassindexwas
intheEPIC-Spaincohort. calculatedasweight(kg)dividedbyheightsquared(m2).
Methods Ascertainment and validation of coronary
heart disease
ThemethodsoftheEPICprojecthavebeenreported
Atbaseline,prevalentcoronaryheartdiseasewasselfreported.
elsewhere.713-16Forthepresentanalysisweusedthedatafrom
Duringfollow-up,weascertainedincidentcoronaryheartdisease
theSpanishcohortofEPIC,whichincluded41438healthy
withatelephonequestionnaire(atthreeyearsafterrecruitment)
adults(15632men),aged29-69.Studyparticipantswere
andthroughrecordlinkagewiththreesourcesofinformation:
recruitedbetween1992and1996infiveSpanishregions.Three
hospitaldischargedatabases,populationbasedmyocardial
oftheseregionsarelocatedinthenorth(Asturias,Gipuzkoa,
infarctionregistries(availableinMurcia,Navarra,and
andNavarra)andtwointhesouth,includingtheMediterranean
Gipuzkoa),andregionalmortalityregistriesandthenational
shore(GranadaandMurcia).Selectionoftheseregionsaimed
mortalitydatabase(managedbytheNationalStatisticalInstitute,
tomaximisevariabilityindietbecausefoodandnutrientintake
Madrid,Spain),whichprovidedinformationondateandcause
hastraditionallybeendifferentbetweenthenorthandthesouth
ofdeath.
ofSpainandbetweentheinnerregionsandcoastalareas.To
increasevariabilityindiet,participantswerealsorecruitedin Coronaryheartdiseasewasclassifiedaccordingtothe
urbanandruralareasfromvariouseducationalandsocial InternationalClassificationofDiseases,ninthrevision(ICD-9
sectors.Studyparticipantsincludedmostlyblooddonors,civil codes410-414)and10threvision(ICD-10codesI20-I25).A
servants,andthegeneralpopulation.Participationratesvaried teamoftraineddoctorsandnursesvalidatedcoronaryheart
from55%to60%betweenregions.Theexposuresofinterest diseaseeventsagainsthospitalrecordsandautopsyreports.
wereassessedatbaseline,andparticipantswerefollowedup Coronaryheartdiseaseeventswereclassifiedonthebasisof
until31December2004.Allparticipantsgavewritteninformed symptoms,signs,biomarkers,andfindingsonelectrocardiogram
consentbeforeenrolment. oratautopsy,accordingtostandardcriteria.23Adefinite
coronaryheartdiseaseeventwasdefinedasonemeetingall
Assessment of food consumption relevantcriteriaforafatalornon-fatalacutemyocardial
Usingacomputeriseddietaryhistoryquestionnaire,17previously infarction,oranginarequiringrevascularisation(coronaryartery
validatedinSpain18-20andadministeredbytrainedinterviewers, bypassgraftorpercutaneoustransluminalcoronaryangioplasty).
Wedefinedprobableandpossibleacutecoronaryheartdisease
weobtaineddataonusualfoodconsumptionforeachparticipant.
eventsascaseswhereelectrocardiogramfindingswere
Weusedhouseholdmeasures,standardunits,andacollection
non-specificorthebiomarkerswereequivocalormissing.13
of35setsofphotographsofsimplefoods,mixedfoods,and
drinkstoquantifytheportionofeachfood(g/day)consumed.
Statistical analysis
Eachinterviewondietaryhistorylastedabout40-50minutes.
Ofthe41438participantsinthecohort,weexcludedthe
followingfromtheanalyses:193forhavingcoronaryheart
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RESEARCH
diseaseatbaseline;167foranimplausiblyhighorlowdietary diagnosedhypertension.Amongwomen,thefrequencyof
consumption,definedas3standarddeviationseitherwayfrom menopausalstatusdecreasedwiththeconsumptionoffriedfood
thecohortmean(<788kcal/dayor>5710kcal/day);and321 (table2).
forlackingdataonimportantvariablessuchasdateofcoronary Duringamedianfollow-upof11years,606definitecoronary
heartdiseaseevent(n=12),smoking(n=22),diabetesmellitus heartdiseaseeventsoccurred(466myocardialinfarctionsand
(n=71),hypercholesterolaemia(n=197),andhypertension 140anginasrequiringrevascularisation).Therewerealso712
(n=60).Thustheanalyseswerecarriedouton40757 definite,possible,orprobablecoronaryheartdiseaseeventsand
participants. 1135deathsfromallcauses.
WeusedCoxregressiontoobtainhazardratiosforcoronary Fordefinitecoronaryheartdiseaseevents,noassociationwith
heartdiseaseaccordingtosexspecificquartersoffriedfood friedfoodconsumptionwasobservedinanalysesadjustingfor
consumption.Thequarter(first)withlowestconsumptionwas energyintake,age,sex,andcentre(table3⇓,model1).The
usedasreference.IntheCoxmodels,agewastheunderlying hazardratioofcoronaryheartdiseaseforthehighestversusthe
timevariable,withentrytimedefinedastheparticipant’sage lowestquarteroffriedfoodconsumptionwas0.94(95%
atrecruitmentandexittimeastheageatthecoronaryheart confidenceinterval0.72to1.23;Pfortrend0.52).Similarresults
diseaseevent,death,or31December2004,whichevercame wereobtainedafteradditionaladjustmentforthemain
first.Toreduceviolationsoftheproportionalhazards confounders(table3,model2):1.11(0.84to1.46;Pfortrend
assumptionwealsostratifiedmodelsbyageatrecruitment(five 0.60).Finally,noassociationwasobservedbetweenfriedfood
yeargroups),sex,andcentre.Webuiltthreemodels,with andincidentcoronaryheartdiseaseafteradjustingforpossible
progressiveadjustmentforpotentialconfounderstodetermine mediatorssuchasbodymassindex,waistcircumference,and
theirinfluenceontheresults.Model1wasadjustedforenergy hypertension(table3,model3).Comparedwiththefirst(lowest)
intakeandmodel2wasadditionallyadjustedforeducational quarteroffriedfoodconsumption,themultivariatehazardratios
level,smoking,physicalactivity(atwork,athome,andduring ofcoronaryheartdiseasewere1.15(0.91to1.45)inthesecond
leisuretime),diabetesmellitus,hyperlipidaemia,cancer,oral quarter,1.07(0.83to1.38)inthethirdquarter,and1.08(0.82
contraceptiveuse,menopause,hormonereplacementtherapy, to1.43)inthefourthquarter(Pfortrend0.74).Lastly,afterfull
ethanolintake,andconsumptionofnon-friedfoods(vegetables, adjustment,a100gincreaseintheconsumptionoffriedfood
fruits,nuts,dairyproducts,meat,andfish).Model3was didnotshowanassociationwithriskofcoronaryheartdisease
additionallyadjustedforpossiblemediatorsofthestudy (hazardratio1.00,0.90to1.11).Theresultsweresimilarafter
associationreportedintheliterature:bodymassindex,waist censoringthefirsttwoyearsoffollow-upandafterexcluding
circumference,andhypertension.Wecategorisedcontinuous thosewhoreportedachangeintheirdietduringtheprevious
variablesintoquarters,exceptforage,whichwasanalysedas year.Theresultsdidnotvarybetweenthosewhousedoliveoil
acontinuousvariable.ThePforlineartrendwascalculatedby forfryingandthosewhousedsunfloweroilorothervegetable
modelingthequartersforfriedfoodasacontinuousvariable. oils(Pforinteraction0.22),orbetweenthesexes(Pfor
Moreover,wealsocalculatedhazardratiosofcoronaryheart interaction0.19).
diseaseandofallcausemortalityfora100gincreaseinfried
Similarresultswerealsoobtainedinthecombinedanalysisof
foodconsumptionanalysedasacontinuousvariable.
definite,possible,andprobablecoronaryheartdiseaseevents.
Newanalysesweredoneaftercensoringthefirsttwoyearsof Comparedwiththefirst(lowest)quarteroffriedfood
follow-upandafterexcludingthosewhoreportedachangein consumption,themultivariatehazardratioofcoronaryheart
theirdietduringthepreviousyear.Totestwhetherthestudy diseaseinthefullyadjustedmodel(model3)was1.08(0.88to
associationvariedwithtypeofoilusedforfrying(oliveoil 1.34)forthesecondquarter,1.06(0.84to1.33)forthethird
versussunfloweroilorothervegetableoils),weusedthe quarter,and1.04(0.81to1.34)forthefourthquarter(Pfor
likelihoodratiotest,whichcomparedmodelswithandwithout trend0.83).
interactionterms(productsofthequartersforfriedfoodand
Friedfoodconsumptionalsofailedtobeassociatedwithall
typeofoil).Wealsousedthesameproceduretotestwhether
causemortality.Comparedwiththelowestquarteroffriedfood
resultsvariedbysex.
consumption,thoseinthehighestquarterhadahazardratioof
StatisticalsignificancewassetatP<0.05.Theanalyseswere 0.93(0.77to1.14;Pfortrend0.98).Moreover,noassociation
carriedoutwithSAS,version9.1forWindows.Thismanuscript wasobservedbetweena100gincreaseinintakeoffriedfood
followstherecommendationsoftheStrengtheningtheReporting andtotalmortality(1.00,0.92to1.08;table3,model3).
ofObservationalStudiesinEpidemiology(STROBE)
Ofthetotalamountoffriedfoodconsumed,24%(34g/day)
initiative.24
wasfish,22%(31g/day)meat,21%(30g/day)potatoes,and
11%(15g/day)eggs.Noassociationwasobservedbetween
Results
eachofthesefriedfoodgroupsandincidentcoronaryheart
Anaverage138goffriedfoodwasconsumeddaily,including disease(table4⇓).Comparingthehighestandlowestquarters,
14gofoilusedforfrying.About7%ofthetotalamountof themultivariatehazardratioforthefullyadjustedmodelwas
foodconsumedwasfried.Friedfoodconsumptionrangedfrom 1.13(0.89to1.44;Pfortrend0.26)forfriedfish,1.09(0.82to
0-817g/dayformenand0-657g/dayforwomen.Sixtytwoper 1.43;Pfortrend0.32)forfriedmeat,0.90(0.70to1.15;Pfor
centofparticipantsusedoliveoilforfryingandtherestused trend0.45)forfriedpotatoes,and0.87(0.68to1.13;Pfortrend
sunfloweroilorothervegetableoils. 0.30)forfriedeggs.Thesefriedfoodsalsofailedtoshowan
associationwithallcausemortality(table4).
Participantswithahigherfriedfoodintakewereyounger,ofa
higherlevelofeducation,moreoftensmokers,andlessoften
Discussion
sedentaryatwork(table1⇓).Moreover,theyhadalower
prevalenceofdiabetesmellitusandhyperlipidaemia,ahigher ThisanalysisoftheSpanishcohortoftheEuropeanProspective
energyandethanolintake,andalowerconsumptionofnon-fried InvestigationintoCancerandNutritionfoundnoassociation
vegetables,fruit,driedfruitandnuts,milkproducts,and betweenconsumptionoffriedfoodandriskofcoronaryheart
non-friedfish(table2⇓).Theyalsohadalowerfrequencyof diseaseorallcausemortality.
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Comparison with other studies Othermechanismsmaybeoperatingduringthefryingprocess.
Forexample,inaninvitrostudyfriedeggsincreasedthe
Fewstudieshaveevaluatedthisassociation.Ourresultsare
productionofangiotensinconvertingenzymeinhibitorypeptides
consistentwiththoseofacase-controlstudyofnon-fatal
morethanboiledeggsdid.33Ontheotherhand,fryingalso
myocardialinfarctioninCostaRica,whichobtainedanodds
increasesthelevelsofcholesteroloxidationproducts34and
ratioof1.06(0.59to1.91;Pfortrend0.65)forthehighest
versuslowestfifthoffriedfoodconsumption.10However,in reducesparaoxonaseactivity,anenzymethatinhibitsoxidation
oflowdensitylipoproteincholesterol.35
theCostaRicaninvestigation,palmandpartiallyhydrogenated
soyoilwereusedforfrying,whereasinthisstudymainlyolive ThisanalysisoftheEPIC-Spaincohortsuggeststhattheabove
andsunfloweroils—themostcommonlyusedoilsin mentionedmechanismsmayoffseteachotherinthegeneral
Mediterraneancountries—wereused. population,withtheresultthatfryingwithmainlyoliveoilor
sunfloweroilisnotassociatedwithahigherriskofcoronary
OurresultsdifferfromthoseoftheINTERHEARTstudy,where
heartdisease.Fryingwithothertypesoffatsmaystillbe
friedfoodconsumptionwasassociatedwithahigherriskof
acutemyocardialinfarction.11However,somemethodological harmful.
differenceslimitthecomparisonofresults.Forinstance,
Limitations and strengths of the study
INTERHEARTdidnotassessquantitativelytheintakeoffried
food;moreover,itrecordedtheconsumptionofonlyninefried Thisstudyhassomelimitations.Firstly,dietwasmeasuredonly
foodsanditdidnotreportthetypeofoilusedforfrying. atbaseline.Secondly,someresidualconfoundingcannotbe
InacrosssectionalanalysisoftheMultiEthnicStudyof ruledout,sincediabetesmellitus,hypertension,and
Atherosclerosis(MESA),noassociationwasfoundbetween hypercholesterolaemiawereselfreported.InSpain,however,
consumptionoffriedfishandsubclinicalatherosclerosis, evidenceexistsofthediagnosticvalidityofselfreported
assessedbythethicknessofintima-mediainthecommon diabetesmellitusandhypertension.3637Thirdly,somedegreeof
carotid.Norwasfriedfishconsumptionassociatedwith under-reportingoffriedfoodconsumptionispossible,given
significantchangesinserumlevelsoftotalcholesterol,low thatpeopleperceiveitasunhealthy;andnon-differential
densitylipoproteincholesterol,highdensitylipoprotein under-reportingwouldbiasthehazardratiotowards1,hiding
cholesterol,ortryglicerides.25TheCardiovascularHealthStudy, apossibleassociation.Fourthly,wedonotknowthetypeof
acohortof3919olderpeople(≥65years)followedfornine fryingprocedure(deeporpan)carriedout,theextentthatoils
years,alsodidnotfindanassociationofconsumptionoffried werereused,andthetimeandtemperatureusedforfrying.Itis
fishorfishsandwicheswithmortalityfromcoronaryheart possiblethatthesefactorsaredifferentiallyassociatedwith
diseaseorcardiacarrhythmia,orwithincidenceofnon-fatal coronaryheartdisease.Fifthly,wecannotseparatetheeffectof
acutemyocardialinfarction.26 aspecificfoodfromtheeffectofthecookingmethodused.For
instance,wecannotseparatetheeffectoffryingwithoil(for
Possible mechanisms of the study example,oliveoil)fromthecardioprotectiveeffectofomega
association 3fattyacidsinfish.Sixthly,resultsarebasedonwhatpeople
atebetween1992and1996.Unfortunately,sincethennostudies
Thefryingprocessiscomplexandasyetisnotwellunderstood.
havebeenpublishedontheconsumptionoffriedfoodbythe
Laboratoryinvestigationsshowthatfriedfoodsmayactthrough
Spanishpopulation.Datafromhouseholdconsumptionsurveys,
manymechanisms,suchthattheresultingeffectoncoronary
however,indicatethatthemacronutrientintakehasnotchanged
heartdiseaseisdifficulttoanticipate.Fryingchangesthequality materiallyfrom1991to200638;also,overalladherencetothe
andcompositionoffood.Forexample,fryingusuallyaugments
Mediterraneanpatternseemsfairlystableintheperiod1998to
thefatcontent,andforsomefoods,suchaspotatoes,thedietary 2005,39althoughanincreaseintheconsumptionofnon-alcoholic
fibreisincreasedowingtotheformationofresistantstarch.1
beveragesanddairyproductsandadecreaseinconsumptionof
Fryingcanspecificallyincreasetheamountoftransfattyacids
potatoesandlegumeshasbeenobservedoverthepasttwo
infoods.27Theamountdependsonthefryingtechnique(deep decades.38Finally,althoughaverageconsumptionoffriedfood
orpanfrying),thedegreeofthermaldegradationoftheoil,the
inthehighestquarterwasfairlyhigh,ourresultscannotrule
typeoffood,and,aboveall,thetypeofoil(thedegreeofoil
outthatafriedfoodintakehigherthanthatobservedinthis
unsaturationincreasestheformationoftransfattyacids).28
studyisassociatedwithcoronaryheartdisease.
However,somefoodssuchascertaintypesoffishshowminimal
Thisanalysisalsohasimportantstrengths,suchastheuseofa
variationsinthecontentoftransfattyacidsafterfrying,
regardlessofwhetheroliveoilorsunfloweroilisused.29Onthe validateddietaryhistorywithquantitativeinformationonthe
consumptionofalargenumberoffriedfoods,thelargesample
otherhand,theuseofsolidfatsforfryingcanalsoincreasethe
size,longfollow-up,andadjustmentfornumerouspotential
contentoftransfattyacids.
confounders.
Theassociationbetweenconsumptionoffriedfoodsand
endothelialdamageiscontroversial.Inacrosssectionalanalysis
Conclusions
oftheMultiEthnicStudyofAtherosclerosis(MESA),
consumptionoffriedfishwasinverselyassociatedwiththe InaMediterraneancountrywhereoliveandsunfloweroilsare
levelofsolubleintercellularadhesionmolecule-1,amarkerof themostcommonlyusedfatsforfrying,andwherelarge
endothelialactivation.Theauthorsdidnotexpectthisfinding, amountsoffriedfoodsareconsumedbothatandawayfrom
sinceitwasnotobservedforconsumptionofnon-friedfish.30 home,noassociationwasobservedbetweenfriedfood
Incontrast,mealsrichinoilspreviouslyusedfordeepfrying consumptionandtheriskofcoronaryheartdiseaseordeath.
infastfoodrestaurantshavebeenassociatedwithendothelial OurresultsaredirectlyapplicableonlytoMediterranean
damage.31Inanotherstudy,however,foodsrichinoils countrieswithfryingmethodssimilartothoseinSpain.Firstly,
previouslyusedforfryingandhighinoxidationproducts oil(mainlyoliveandsunflower)ratherthansolidfatisusedfor
increasedpostprandialtriglyceridaemiabutdidnotaffect fryinginSpain.Itiswellestablishedthatoliveoilislessprone
endothelialfunction.32 tooxidationthanotheredibleoilsorfats.4041Secondly,
consumptionoffriedfoodsinSpainisnotaproxyforfastfood
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intake.Fastfoodsaregenerallypreparedbydeepfryingwith 11 IqbalR,AnandS,OunpuuS,IslamS,ZhangX,RangarajanS,etal.Dietarypatternsand
theriskofacutemyocardialinfarctionin52countries:resultsoftheINTERHEARTstudy.
oilsusedseveraltimes,andareconsumedmostlyawayfrom
Circulation2008;118:1929-37.
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reducingintakesofsaturatedfatinthepreventionofcardiovasculardisease:wheredoes
fromhome,andbothdeepfryingandpanfryingareused.
theevidencestandin2010?AmJClinNutr2011;93:684-8.
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foodsconsumedathome;however,thecardiovasculareffects thecardiovascularcomponentofaprospectivestudyofnutritional,lifestyleandbiological
factorsin520,000middle-agedparticipantsfrom10Europeancountries.EurJEpidemiol
offoodfriedwithoverlyreusedoilsmeritfurtherresearch. 2007;22:129-41.
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InvestigationintoCancerandNutrition.IntJEpidemiol1997;26(suppl1):S6-14.
inSpain,whereasinothercountriessuchastheUnitedStates 15 BinghamS,RiboliE.Dietandcancer—theEuropeanProspectiveInvestigationintoCancer
theyprovideanimportantpercentageofenergyintake.42 andNutrition.NatRevCancer2004;4:206-15.
16 RiboliE,HuntKJ,SlimaniN,FerrariP,NoratT,FaheyM,etal.EuropeanProspective
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thestudy.PG-CandFR-Aconceivedthestudyanddraftedthe
19 EPICgroupofSpain.Relativevalidityandreproducibilityofadiethistoryquestionnaire
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CM,EM,CN,JRQ,LR,andMJSprovidedtheoriginaldataand inSpain.III.Biochemicalmarkers.EPICGroupofSpain.EuropeanProspective
informationontherespectivepopulationsandhelpeddesignandanalyse InvestigationintoCancerandNutrition.IntJEpidemiol1997;26(suppl1):S110-7.
21 SlimaniN,TorrentM,FarriollN.EuropeanProspectiveInvestigationintoCancerand
thestudy.AB,MD,CN,JRQ,MJS,andCAGweretheprincipal Nutrition(EPIC):foodcompositiontables—Spain.InternationalAgencyforResearchon
investigatorsforEPIC.Allauthorsinterpretedtheresultsandcontributed Cancer,1991.
22 HaftenbergerM,SchuitAJ,TormoMJ,BoeingH,WarehamN,Bueno-de-MesquitaHB,
towritingthemanuscriptandtakeresponsibilityfortheintegrityofthe
etal.Physicalactivityofsubjectsaged50-64yearsinvolvedintheEuropeanProspective
dataandtheaccuracyofthedataanalysis. InvestigationintoCancerandNutrition(EPIC).PublicHealthNutr2002;5:1163-76.
23 LuepkerRV,AppleFS,ChristensonRH,CrowRS,FortmannSP,GoffD,etal.Case
Funding:ThisstudywasfundedbyresearchgrantsfromFIS(PI04-0257, definitionsforacutecoronaryheartdiseaseinepidemiologyandclinicalresearchstudies:
PI06-0366,PI04-2342,PI04-1822,PI04-1821,PI04-2188,and astatementfromtheAHACouncilonEpidemiologyandPrevention;AHAStatistics
Committee;WorldHeartFederationCouncilonEpidemiologyandPrevention;theEuropean
PI08-0166);RETIC(RD06/0020)oftheInstitutodeSaludCarlosIII;
SocietyofCardiologyWorkingGrouponEpidemiologyandPrevention;CentersforDisease
andfundsfromtheSpanishregionalgovernmentsofAndalusia,Asturias, ControlandPrevention;andtheNationalHeart,Lung,andBloodInstitute.Circulation
2003;108:2543-9.
BasqueCountry,Murcia,andNavarra,andtheCatalanInstituteof
24 VonElmE,AltmanDG,EggerM,PocockSJ,GotzschePC,VandenbrouckeJP.
Oncology.EL-GhasaRamónyCajalcontractfromtheMinistryof StrengtheningtheReportingofObservationalStudiesinEpidemiology(STROBE)
Education.Authorsofthisreport,andnotthefundingagencies,are statement:guidelinesforreportingobservationalstudies.BMJ2007;335:806-8.
25 HeK,LiuK,DaviglusML,Mayer-DavisE,JennyNS,JiangR,etal.Intakesoflong-chain
responsibleforitscontent.Thefunderdidnothaveanyroleinthestudy n-3polyunsaturatedfattyacidsandfishinrelationtomeasurementsofsubclinical
design;collection,analysis,andinterpretationofthedata;thewriting atherosclerosis.AmJClinNutr2008;88:1111-8.
26 MozaffarianD,LemaitreRN,KullerLH,BurkeGL,TracyRP,SiscovickDS.Cardiac
ofthereport;andthedecisiontosubmitthearticleforpublication.
benefitsoffishconsumptionmaydependonthetypeoffishmealconsumed:the
Competinginterests:AllauthorshavecompletedtheICMJEuniform CardiovascularHealthStudy.Circulation2003;107:1372-7.
27 LitinL,SacksF.Trans-fatty-acidcontentofcommonfoods.NEnglJMed
disclosureformatwww.icmje.org/coi_disclosure.pdf(availableon 1993;329:1969-70.
requestfromthecorrespondingauthor)anddeclare:nosupportfrom 28 BoskouG,SaltaFN,ChiouA,TroullidouE,AndrikopoulosNK.Contentof
trans,trans-2,4-decadienalindeep-friedandpan-friedpotatoes.EurJLipidSciTechnol
anyorganisationforthesubmittedwork;nofinancialrelationshipswith
2006;108:109-15.
anyorganisationsthatmighthaveaninterestinthesubmittedworkin 29 AnsorenaD,GuembeA,MendizabalT,AstiasaranI.Effectoffishandoilnatureonfrying
processandnutritionalproductquality.JFoodSci2010;75:H62-7.
thepreviousthreeyears;andnootherrelationshipsoractivitiesthat
30 HeK,LiuK,DaviglusML,JennyNS,Mayer-DavisE,JiangR,etal.Associationsofdietary
couldappeartohaveinfluencedthesubmittedwork. long-chainn-3polyunsaturatedfattyacidsandfishwithbiomarkersofinflammationand
endothelialactivation(fromtheMulti-EthnicStudyofAtherosclerosis[MESA]).AmJ
Ethicalapproval:Thisstudywasapprovedbytheethicscommitteesof Cardiol2009;103:1238-43.
theInternationalAgencyforResearchonCancer(Lyon,France)and 31 WilliamsMJ,SutherlandWH,McCormickMP,deJongSA,WalkerRJ,WilkinsGT.
Impairedendothelialfunctionfollowingamealrichinusedcookingfat.JAmCollCardiol
BellvitgeHospital(Barcelona,Spain).
1999;33:1050-5.
Datasharing:Noadditionaldataavailable. 32 WilliamsMJ,SutherlandWH,McCormickMP,YeomanD,deJongSA,WalkerRJ.Normal
endothelialfunctionaftermealsrichinoliveorsaffloweroilpreviouslyusedfordeepfrying.
NutrMetabCardiovascDis2001;11:147-52.
1 FillionL,HenryCJ.Nutrientlossesandgainsduringfrying:areview.IntJFoodSciNutr 33 MajumderK,WuJ.AngiotensinIconvertingenzymeinhibitorypeptidesfromsimulated
1998;49:157-68. invitrogastrointestinaldigestionofcookedeggs.JAgricFoodChem2009;57:471-7.
2 PokornJ,PanekJ,TrojakovaL.Effectoffoodcomponentchangesduringfryingonthe 34 EcharteM,AnsorenaD,AstiasaranI.Fattyacidmodificationsandcholesteroloxidation
nutritionvalueoffriedfood.ForumNutr2003;56:348-50. inporkloinduringfryingatdifferenttemperatures.JFoodProt2001;64:1062-6.
3 Sanchez-MunizFJ,CuestaC,Garrido-PolonioMC.Evaluationofasunfloweroilusedfor 35 SutherlandWH,WalkerRJ,deJongSA,vanRijAM,PhillipsV,WalkerHL.Reduced
fryingbydifferentanalyticalindexesandcolumnandgaschromatography.Z postprandialserumparaoxonaseactivityafteramealrichinusedcookingfat.Arterioscler
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4 SamraRA.Fatsandsatiety.In:MontmayeurJP,leCoutreJ,eds.Fatdetection:taste, 36 HuertaJM,TormoMJ,Egea-CaparrosJM,Ortola-DevesaJB,NavarroC.Accuracyof
texture,andpostingestiveeffects.CRCPress,2010. self-reporteddiabetes,hypertensionandhyperlipidemiaintheadultSpanishpopulation.
5 DrewnowskiA,Almiron-RoigE.Humanperceptionandpreferencesforfat-richfoods.In: DINOstudyfindings.RevEspCardiol2009;62:143-52.
MontmayeurJP,leCoutreJ,eds.Fatdetection:taste,texture,andpostingestiveeffects. 37 TormoMJ,NavarroC,ChirlaqueMD,BarberX.Validationofselfdiagnosisofhighblood
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6 SoriguerF,Rojo-MartinezG,DobarganesMC,GarciaAlmeidaJM,EstevaI,BeltranM, EPICGroupofSpain.JEpidemiolCommunityHealth2000;54:221-6.
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8 Sayon-OreaC,Bes-RastrolloM,Basterra-GortariFJ,BeunzaJJ,Guallar-CastillonP,de 40 Gallina-ToschiT,CerreteniL,BendiniA,Bonoli-CarbogninM,LerckerG.Oxidativestability
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9 DonfrancescoC,LoNC,BrignoliO,RiccardiG,CiccarelliP,DimaF,etal.Italiannetwork 41 CasalS,MalheiroR,SendasA,OliveiraBPP,PereiraJA.Oliveoilstabilityunder
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2008;9:53. 42 NielsenSJ,Siega-RizAM,PopkinBM.TrendsinenergyintakeinUSbetween1977and
10 KabagambeEK,BaylinA,SilesX,CamposH.Individualsaturatedfattyacidsandnonfatal 1996:similarshiftsseenacrossagegroups.ObesRes2002;10:370-8.
acutemyocardialinfarctioninCostaRica.EurJClinNutr2003;57:1447-57.
Accepted:14November2011
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RESEARCH
Whatisalreadyknownonthistopic
Theconsumptionoffriedfoodhasbeenassociatedwithsomecardiovascularriskfactors,suchashypertension,obesity,andlowlevels
ofhighdensitylipoproteincholesterol
Theassociationbetweenfriedfoodconsumptionandcoronaryheartdiseasehasbeenevaluatedinsomecase-controlstudies,with
heterogeneousresults
Whatthisstudyadds
InSpain,aMediterraneancountrythatusesoliveorsunfloweroilforfrying,theconsumptionoffriedfoodswasnotassociatedwithrisk
ofcoronaryheartdiseaseorallcausemortality
Fryingwithothertypesoffats,reusingoilsseveraltimes,orconsumingfriedsnackshighinsaltmaystillbeharmful
Citethisas:BMJ2012;344:e363 anymedium,providedtheoriginalworkisproperlycited,theuseisnoncommercialand
isotherwiseincompliancewiththelicense.See:http://creativecommons.org/licenses/by-
Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommons
nc/2.0/andhttp://creativecommons.org/licenses/by-nc/2.0/legalcode.
AttributionNon-commercialLicense,whichpermitsuse,distribution,andreproductionin
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RESEARCH
Tables
Table1|Consumptionoffriedfoods,sociodemographicvariables,andlifestylesofstudyparticipantsatbaseline,byquartersoffriedfood
consumption.Valuesaremeansunlessstatedotherwise
Quartersoffriedfoodconsumption
Characteristics 1(lowest) 2 3 4(highest)
Consumptionoffriedfoods
Totalamountoffriedfoodconsumed(g/day) 47.0 105.7 158.4 249.6
Friedfish(g/day) 12.6 28.8 40.6 53.6
Friedmeat(g/day) 8.3 21.7 36.2 59.9
Friedpotatoes(g/day) 9.3 21.6 33.3 57.7
Friedeggs(g/day) 4.0 10.7 17.1 28.0
Sociodemographicvariables
Age(years) 50.4 49.5 48.9 48.3
Educationallevel(%):
Noformaleducation 41.9 36.4 31.7 27.6
Primaryeducation 31.6 35.9 40.8 46.6
Secondaryeducation 12.6 14.2 16.0 16.0
Universityeducation 13.3 12.8 10.8 9.0
Lifestyle
Smoking(%):
Neversmoker 58.3 59.3 59.5 59.7
Currentsmoker 22.5 22.5 23.7 24.2
Formersmoker 19.2 18.2 16.8 16.1
Physicalactivityatwork(%):
Sedentary 22.8 22.1 20.4 18.8
Standing 62.1 64.2 63.7 63.4
Manuallabour 6.2 8.5 10.3 12.3
Heavymanuallabour 2.2 1.9 2.1 2.5
Doesnotwork 3.8 3.3 3.6 3.1
Physicalactivityathome(METsh/week) 68.6 69.8 70.0 68.1
Physicalactivityinleisuretime(METsh/week) 28.7 28.2 28.6 28.4
MET=metabolicequivalents.Rangeofquartersoffriedfoodconsumptioning/dayformen:firstquarter(0-112),secondquarter(113-176),thirdquarter(177-246),
andfourthquarter(247-817),andforwomen:firstquarter(0-59),secondquarter(60-103),thirdquarter(104-154),andfourthquarter(155-657).
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RESEARCH
Table2|Morbidity,menopausalstatus,useofhormonetreatment,consumptionofnon-friedfood,andpotentialmediatorsofstudy
associationamongstudyparticipantsatbaseline,byquartersoffriedfoodconsumption.Valuesaremeansunlessstatedotherwise
Quartersoffriedfoodconsumption
Characteristics 1(lowest) 2 3 4(highest)
Diseasesdiagnosed:
Diabetesmellitus(%) 7.5 5.1 3.9 3.2
Hyperlipidaemia(%) 24.8 20.5 18.5 16.7
Cancer(%) 1.0 0.9 0.8 0.8
Menopause(%)* 42.2 36.9 33.0 29.3
Hormonetreatment(%)*:
Oralcontraceptives 24.7 26.4 26.6 27.4
Hormonesubstitutiontherapy 6.4 6.2 5.5 5.6
Othernutrientsandfoodsconsumed:
Totalenergy(kcal/day) 1920.1 2133.0 2294.8 2566.6
Ethanol(g/day) 11.5 14.5 17.0 20.4
Non-friedvegetables(g/day) 255.0 241.1 232.3 237.4
Fruit(g/day) 336.6 322.0 315.3 311.2
Driedfruitandnuts(g/day) 5.0 4.6 4.2 3.9
Milkproducts(g/day) 304.7 298.1 296.9 292.0
Non-friedmeat(g/day) 93.9 98.0 97.9 96.2
Non-friedfish(g/day) 37.2 29.6 26.0 23.8
Mediatorsofstudyassociation:
Bodymassindex(kg/m2) 28.5 28.3 28.1 28.1
Waistcircumference(cm) 92.8 92.0 91.4 91.4
Hypertension(%) 23.7 20.9 18.4 17.4
Seetable1forrange(g/day)ofquartersoffriedfoodconsumptionformenandforwomen.
*Calculatedforwomen.
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RESEARCH
Table3|Associationbetweenfriedfoodconsumptionandincidenceofdefinitecoronaryheartdiseaseandallcausemortalityduring11
yearsoffollow-upinSpanishcohortofEuropeanProspectiveInvestigationintoCancerandNutrition
Quartersoffriedfoodconsumption
For100gincrease
Variables 1(lowest) 2 3 4(highest) Pfortrend offriedfood
Coronaryheartdisease:
TotalNo 10188 10190 10190 10189
Personyears 109578 110394 110943 111762
Noofevents 154 163 150 139
Model1*:hazardratios 1 1.05(0.84to1.33) 0.97(0.76to1.24) 0.94(0.72to1.23) 0.52 0.95(0.86to1.06)
(95%CI)
Model2†:hazardratios 1 1.15(0.91to1.46) 1.08(0.84to1.39) 1.11(0.84to1.46) 0.60 1.01(0.91to1.12)
(95%CI)
Model3‡:hazardratios 1 1.15(0.91to1.45) 1.07(0.83to1.38) 1.08(0.82to1.43) 0.74 1.00(0.90to1.11)
(95%CI)
Allcausemortality:
TotalNo 10188 10190 10190 10189
Personyears 110135 111019 111560 112342
Noofdeaths 328 276 273 258
Model1*:hazardratios 1 0.90(0.76to1.07) 0.91(0.77to1.09) 0.89(0.73to1.08) 0.26 0.98(0.91to1.06)
(95%CI)
Model2†:hazardratios 1 0.94(0.79to1.11) 0.95(0.80to1.14) 0.94(0.77to1.15) 0.60 1.00(0.92to1.08)
(95%CI)
Model3‡:hazardratios 1 0.94(0.79to1.11) 0.95(0.79to1.13) 0.93(0.77to1.14) 0.98 1.00(0.92to1.08)
(95%CI)
Quartersaresexspecific.Seetable1forrange(g/day)ofquartersoffriedfoodconsumptionformenandforwomen.
*Adjustedforage,sex,centre(Asturias,Gipuzkoa,Granada,Murcia,orNavarra),andenergyintake(quarters).
†Adjustedforvariablesinmodel1andforethanolconsumption(quartersamongconsumers),educationallevel(noformaleducation,primary,vocational,secondary,
universityeducation),smoking(never,current,former),physicalactivityatwork(sedentary,standing,manuallabour,heavymanuallabour,nowork),physical
activityathome(metabolicequivalentsh/weekinquarters),physicalactivityinleisuretime(metabolicequivalentsh/weekinquarters),diabetesmellitus,
hyperlipidaemia,cancer,oralcontraceptives,menopause,hormonereplacementtherapy,andconsumptionoffruit(quarters),nuts(quarters),anddairyproducts
(quarters),andnon-friedfoods(quarters):vegetables,meat,andfish.
‡Adjustedforvariablesinmodel2andforbodymassindex(<25and≥25,<30and≥30,<35and≥35),waistcircumference(quarters),andhypertension.
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RESEARCH
Table4|Associationbetweenconsumptionofmaintypesoffriedfoodandincidenceofdefinitecoronaryheartdiseaseandallcause
mortalityduring11yearsoffollow-upinSpanishcohortofEuropeanProspectiveInvestigationintoCancerandNutrition
Quartersoffriedfoodconsumption
For100gincrease
Variables 1(lowest) 2 3 4(highest) Pfortrend offriedfood
Coronaryheartdisease
Friedfish:
Noofevents 144 136 149 177 — —
Hazardratio(95%CI)* 1 0.99(0.78to1.26) 1.06(0.83to1.35) 1.13(0.89to1.44) 0.26 1.03(0.82to1.29)
Friedmeat:
Noofevents 137 158 174 137 — —
Hazardratio(95%CI)* 1 1.17(0.93to1.49) 1.40(1.09to1.79) 1.09(0.82to1.43) 0.32 1.05(0.82to1.35)
Friedpotatoes:
Noofevents 188 151 138 129 — —
Hazardratio(95%CI)* 1 0.92(0.74to1.15) 0.95(0.75to1.19) 0.90(0.70to1.15) 0.45 0.91(0.71to1.17)
Friedeggs:
Noofevents 184 151 145 126 — —
Hazardratio(95%CI)* 1 0.99(0.80to1.24) 0.95(0.76to1.20) 0.87(0.68to1.13) 0.30 0.84(0.51to1.40)
Allcausemortality
Friedfish:
Noofevents 297 276 271 291 — —
Hazardratio(95%CI)* 1 0.99(0.84to1.17) 0.97(0.81to1.15) 0.92(0.77to1.10) 0.34 0.84(0.69to1.01)
Friedmeat:
Noofevents 346 246 264 279 — —
Hazardratio(95%CI)* 1 0.80(0.67to0.95) 0.90(0.75to1.08) 0.94(0.78to1.14) 0.72 0.96(0.79to1.16)
Friedpotatoes:
Noofevents 353 273 249 260 — —
Hazardratio(95%CI)* 1 0.90(0.77to1.06) 0.92(0.78to1.09) 0.99(0.83to1.18) 0.87 1.10(0.91to1.32)
Friedeggs:
Noofevents 350 265 245 275 — —
Hazardratio(95%CI)* 1 0.96(0.81to1.13) 0.90(0.75to1.06) 1.05(0.87to1.25) 0.90 1.11(0.76to1.64)
*Adjustedthesameasmodel3intable3.
Rangeofquartersoffriedfoodconsumptioning/day:fishconsumptionformen:firstquarter(0-15),secondquarter(16-35),thirdquarter(36-61),andfourthquarter
(62-439),andforwomen:firstquarter(0-8),secondquarter(9-23),thirdquarter(24-40),andfourthquarter(41-346);meatconsumptionformen:firstquarter
(0-12),secondquarter(13-34),thirdquarter(35-65),andfourthquarter(66-384),andforwomen:firstquarter(0-2),secondquarter(3-15),thirdquarter(16-36),
andfourthquarter(37-347);potatoconsumptionformen:firstquarter(0-12),secondquarter(13-33),thirdquarter(34-59),fourthquarter(60-560),andforwomen:
firstquarter(0-3),secondquarter(4-17),thirdquarter(18-34),andfourthquarter(35-282);eggconsumptionformen:firstquarter(0-6),secondquarter(7-15),
thirdquarter(16-30),fourthquarter(31-176),andforwomen:firstquarter(0-0),secondquarter(1-8),thirdquarter(9-17),andfourthquarter(18-123).
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