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RESEARCHARTICLE Dietary habits in adolescence and midlife and risk of breast cancer in older women AlfheidurHaraldsdottir1,2*,JohannaE.Torfadottir2,UnnurA.Valdimarsdottir2,3,4,Hans- OlovAdami3,4,ThorAspelund2,LaufeyTryggvadottir5,6,MariannaThordardottir6,Bryndis E.Birgisdottir1,7,TamaraB.Harris8,LenoreJ.Launer8,VilmundurGudnason6,9, LaufeySteingrimsdottir1,7 1 FacultyofFoodScienceandHumanNutrition,UniversityofIceland,Reykjavik,Iceland,2 CentreofPublic HealthSciences,FacultyofMedicine,UniversityofIceland,Reykjavik,Iceland,3 Departmentof Epidemiology,HarvardT.HChanSchoolofPublicHealth,Boston,Massachusetts,UnitedStatesofAmerica, a1111111111 4 DepartmentofMedicalEpidemiologyandBiostatistics,KarolinskaInstitutet,Stockholm,Sweden,5 The a1111111111 IcelandicCancerRegistry,Reykjavik,Iceland,6 FacultyofMedicine,UniversityofIceland,Reykjavik, Iceland,7 UnitforNutritionResearch,UniversityofIcelandandLandspitaliNationalUniversityHospital, a1111111111 Reykjavik,Iceland,8 LaboratoryofEpidemiologyandPopulationSciences,IntramuralResearchProgram, a1111111111 NationalInstituteonAging,Bethesda,Maryland,UnitedStatesofAmerica,9 TheIcelandicHeart a1111111111 Association,Kopavogur,Iceland *[email protected] OPENACCESS Abstract Citation:HaraldsdottirA,TorfadottirJE, Recentstudiesindicatethatlifestylefactorsinearlylifeaffectbreastcancerrisk.Wethere- ValdimarsdottirUA,AdamiH-O,AspelundT, TryggvadottirL,etal.(2018)Dietaryhabitsin foreexploredtheassociationofhighconsumptionofmeat,milk,andwholegrainproductsin adolescenceandmidlifeandriskofbreastcancer adolescenceandmidlife,onbreastcancerrisk.Weuseddatafromthepopulationbased inolderwomen.PLoSONE13(5):e0198017. AGES-Reykjavikcohort(2002–2006),where3,326womenwithameanageof77years(SD https://doi.org/10.1371/journal.pone.0198017 6.0)participated.Forfooditemsandprincipalcomponentderiveddietarypatternsweused Editor:SabineRohrmann,UniversityofZurich, Coxproportionalmodelstocalculatemultivariatehazardratios(HR)with95%confidence SWITZERLAND intervals(95%CI).Duringameanfollow-upof8.8years,97womenwerediagnosedwith Received:December1,2017 breastcancer.Forbothadolescenceandmidlife,dailyconsumptionofryebreadwasposi- Accepted:May11,2018 tivelyassociatedwithbreastcancer(HR1.7,95%CI1.1–2.6andHR1.8,95%CI1.1–2.9, Published:May30,2018 respectively).Incontrast,persistenthighconsumptionofoatmealwasnegativelyassociated withbreastcancer(0.4,95%CI0.2–0.9).Noassociationwasfoundforotherfooditemsor Copyright:©2018Haraldsdottiretal.Thisisan openaccessarticledistributedunderthetermsof dietarypatternsthatincludedryebread.Highryebreadconsumptioninadolescenceand theCreativeCommonsAttributionLicense,which midlifemayincreaseriskoflate-lifebreastcancerwhilstpersistentconsumptionofoatmeal permitsunrestricteduse,distribution,and mayreducetherisk. reproductioninanymedium,providedtheoriginal authorandsourcearecredited. DataAvailabilityStatement:Datacannotbe madeavailableduetolegalrestrictions;partofthe datainthisstudywasobtainedfromthenational Introduction IcelandicCancerRegistry,wherenationaldata protectionlawsappliesandforbidsdatafrombeing Duringadolescencethefemalemammarytissueundergoesextensivemodelingorre-modeling. publiclyavailable.Datacanberequestedthrough Consequently,researchershavehypothesizedthatbreasttissuemaybeparticularlysusceptiblefor collaborationwiththeIcelandicHeartAssociation initiationofbreasttumorsduringthisperiod[1,2].Thereisincreasingevidenceontheimpor- (contact:[email protected])andthe tanceofadultmidlifedietandriskofbreastcancer[3]whileavailablestudiesontheimpactof IcelandicCancerRegistry(http://www. dietduringadolescenceonbreastcancerriskarescarceandsomewhatinconsistent[4].Studying krabbameinsskra.is/indexen.jsp?id=reference, contact:[email protected]). earlylifedietcanbechallengingduetopotentialmisclassificationbias,theneedforalongfollow- PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 1/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer Funding:TheAGES-ReykjavikStudywasfunded upandlimitedvariationinfoodintakebetweenparticipants.Interestingly,therewasconsiderable byNIHcontractN01-AG-12100,theIntramural variabilityindietaryhabitsbetweenresidencyareasinIcelandinearlyandmid20thcenturydue ResearchProgramoftheNationalInstituteon torelativeisolationofregionsanddifferencesinfoodaccess.Thisvariationwasobservedtobe Aging,bytheIcelandicHeartAssociationandthe strongestforthemostcommonfooditemsconsumedatthattime,ormeat,rye,milkproducts, IcelandicParliament.Thisworkwassupportedby fishandfishoil[5].Theseproductsarealsoofinterestinthiscontextbecauseoftheirdiversebio- theTheIcelandicCentreforResearch,RANNIS grantnumber:152495051,(http://en.rannis.is/)(A. activecompounds[6,7]aswellastheirwide-spreaduseinmodernWesterndiets. Haraldsdottir)andthePublicHealthFundofthe IntheNurses’HealthStudy,womeninthehighestquintileofredmeatconsumptionin IcelandicDirectorateofHealth(A.Haraldsdottir). adolescencehadsignificantlyhigherriskofbreastcancerthanwomeninthelowestquintile Thefundingagencies(NationalInstituteonAging, [8–10].Arecentmeta-analysisof14prospectivestudies[11]onadultred-andprocessedmeat IcelandicHeartAssociationandIcelandic consumptionreportedaslightlyincreasedbreastcancerriskandsimilarresultswereobserved Parlament,)fortheAGES-ReykjavikStudy, RANNIS,orDirectorateofHealthhadnoroleinthe intheNIH-AARPDietandHealthStudy[12].Incontrast,noassociationwitheitherchild- design,analysisorwritingofthisarticle. hoodoradultmilkconsumptionandriskofbreastcancerhasbeenfound[13–18].Hightotal dietaryfiberintakeinearlyadulthoodwasassociatedwithsignificantlylowerbreastcancer Competinginterests:Theauthorshavedeclared thatnocompetinginterestsexist. risk[19],aswastotalhighadolescentconsumptionoflignans[20],acommonphytoestrogen commonlyfoundinwholegrains[21].Highconsumptionwholegrainfoodintakeinadoles- cenceandearlyadulthoodwasassociatedwithlowerriskofpremenopausalbreastcancerrisk butnotwithpost-menopausalrisk[22].Availablestudiesontotaladultwholegrainconsump- tionandbreastcancerriskhaveeithersuggestedanegative[22–24]ornoassociation[25,26]. ForthisstudyweuseddatafromthepopulationbasedAGES-ReykjavikStudy,whichis derivedfromapopulationwithconsiderablevariationindietaryhabitsinadolescence.Using thesamecohort,wehavepreviouslyobservedapreventiveroleofveryhighfishintakeinado- lescenceandmidlifeforbreastcancer[27]andalsotheimportanceofearlierdietforprostate cancerrisk[28–30].Inthepresentstudyouraimwastoexploretheeffectsofhighconsump- tionofmeat,milk,andwholegrainproductsinadolescenceandmidlifeonbreastcancerrisk laterinlife,withamainemphasisontheadolescenceperiod. Materialsandmethods Studypopulation WeuseddatafromtheAgeGeneEnvironmentSusceptibility(AGES)—ReykjavikCohortStudy oftheIcelandicHeartAssociation,asub-cohortofthepopulationbasedReykjavikStudyinitiated in1967[31].TheAGES-ReykjavikStudyexaminationsbeganin2002andatthattime11,549 ReykjavikStudycohortmemberswerestillalive.Thereof,8,030individualswererandomlyinvited tothestudyandofthese,5,764individuals(thereof3,326women)participatedbetween2002– 2006(72%responserate).Extensivedatawerecollectedduringclinicalexaminations,including informationonfoodintakeinadolescence,midlifeandpresentoldage.Forouranalysisweused datafromthefirstclinicalexamination[32].Forthisstudy,weexcludedwomenwhohadbeen diagnosedwithbreastcancerpriortostudyentry(n=196),leaving3130womeninourstudy. Dietaryassessmentinearlylifeandmidlife Atstudyentry,theparticipantscompletedafoodfrequencyquestionnaire(FFQ)ondietin adolescence(betweentheagesof14to19years),inmidlife(betweentheages40to50years), andatstudyentry(latelife).Forthisanalysisweonlyusequestionsfromtheadolescentand midlifeperiod. TheFFQwasespeciallydesignedforthisprojectandprovidesinformationonfrequencyof intakeof10commonfoodsandfoodgroupsconsumedinadolescenceand11inmidlife.For bothadolescenceandmidlife,thesefoodgroupsweremeat(includingsaltedandsmoked meat),fish(includingsaltedorsmokedfish),fishliveroil,bloodorliversausage,ryebread,oat- meal,potatoes,milkandmilkproducts,fruitsandvegetables[33].Anadditionalquestionon PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 2/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer consumptionofwholewheatbreadwasincludedforthemidlifeperiod,butthistypeofbread wasuncommonintheadolescentperiod.Aspreviouslystated,forthisanalysisourmainfocus isonmeat,includingsaltedandsmokedmeat,milk,ryebread,oatmealandwholewheatbread. Wehavepreviouslypublishedanalysisonfishandcodliveroilfromthissamecohort[27]while analysisonfruitsandvegetableswerenotconductedduetoverylowconsumptiononadaily basisforbothadolescenceandmidlife.However,allfoodgroups,asdescribedabove,were includedinthedietarypatternanalysis(seesupportinginformation). Twoseparatequestionswereaskedregardingmeatconsumption.Oneincludedtotalcon- sumptionofmeatandgroundmeatasameal(hereafterreferredtoasmeat).Theotherques- tion(includedintotalmeatconsumption)concernedintakeofcornedmeat,cornedmeat sausage,oranykindofsalted/smokedmeat(hereafterreferredtoassaltedorsmokedmeat). Informationonmilkconsumptionincludedfrequencyofintakeofmilkandmilkproducts (hereafterreferredtoasmilk).Ryebreadconsumptionwasassessedbyonequestiononintake ofryebreadandflatbreadmadeofrye(hereafterreferredtoasryebread).Formidlife,the questiononoatmealalsoincludedmuesli,butwillbereferredtoasoatmealinbothperiods. Formeat,milk,ryebread,oatmeal,andwholewheatbread,thefrequencyofconsumption wasclassifiedinto;1)never,2)lessthanonceaweek,3)1–2timesaweek,4)3–4timesaweek, 5)5–6timesaweek,6)daily,and7)morethanonceaday.Forsaltedorsmokedmeat,thefol- lowingresponsecategorieswere:1)never,2)lessthanonceamonth,3)1–3timesamonth,4) 1–2timesaweek5)3–6timesaweek6)dailyormoreoften. Forbothadolescenceandmidlife,meatconsumptionwasdividedintotwocategories.low(2 timesorlessperweek)andhigh(3timesormoreperweek).Consumptionofsaltedorsmoked meatwasalsodividedintotwocategories,withlowintakedefinedas3timespermonthorless andhighasonceperweekormore.Consumptionofmilk,ryebreadandwholewheatbread (midlifeonly)wasdividedintotwocategories(lessthandailyanddailyormore).Consumption ofoatmealwasdividedintolow(4timesaweekorless)andhigh(5timesaweekormore). TheFFQhasbeenvalidatedformidlifeandlatelife[33,34].Inshort,midlifedietaryhabits werevalidatedbycomparingtheresultsintheAGES-FFQ(n=107)withdetaileddietarydata gatheredfromthesameindividuals18–19yearspreviouslyinaNationalnutritionsurveycon- ductedin1990.Themainresultswerethatthecorrelationcoefficientsformostofthefood itemswerewithinanacceptablerange[33]. Covariateassessment Informationonpotentialconfounderswasmainlyretrievedfromalifestylequestionnaire, completedatentrytotheAGES-ReykjavikStudy.Wecollectedinformationonageatentryto thestudy(continuous),ageatmenarche(continuous),familyhistoryofbreastcancer(mother, sisterand/ordaughtereverdiagnosedwithbreastcancer),education(primary,secondary,col- lege/university),useofhormonalreplacementtherapy(never,ever),oralcontraceptive(never, ever),useofalcoholinmidlife(yes,no),andphysicalactivityinadolescenceandmidlife (never/rarely,occasionally,moderately/often).Wealsoretrievedinformationoneverbeing pregnant(y/n)andageatfirstbirth(continuous),andcombinedthisinformationintoone variable(nobirths,age24andyounger,25andolder).FromtheReykjavikStudyweretrieved valuesonbodymassindex(BMI)andheightfromthemidlifeperiod(bothcontinuous).Infor- mationondietarycovariateswasretrievedfromtheAGES-FFQ(Fig1). Selecteddietarycovariatesonconcurrentconsumptionincluded,milk,meat,saltedand smokedmeat,oatmeal,andryebread,dependingontheexposure(seecutoffsabove).Wealso usedinformationonfishconsumption,((cid:20)2portionsp/wvs.>2–4portionsp/wvs.>4por- tionsp/w)andonsaltedandsmokedfish(3timesamonthorlessvs.onceaweekormore). PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 3/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer Fig1.Timelineofexaminationpointsinthestudy. https://doi.org/10.1371/journal.pone.0198017.g001 Asresidencedependentvarianceinfoodconsumptionexistedduringtheadolescence period[5]wealsoaddedinformationonplaceofresidencewhengrowingupinourmodels (capital,coastalvillage,ruralarea,andcombinationofcoastalvillageandruralarea)collected intheReykjavikStudy. Ascertainmentofoutcome WeascertainedbreastcancerdiagnosisthroughthenationwideIcelandicCancerRegistry [35].InformationoncauseofdeathwasobtainedfromDirectorateofHealth.Duetothecom- puterizednationalrosteranduniquepersonalidentificationnumbersforeachperson,follow- upwasvirtuallycomplete(99%)[35].Participantswerefollowedfromthestudyentry (between2002and2006)todiagnosisofbreastcancer,death,oruntiltheendoftheobserva- tionperiod(December31,2014),whicheveroccurredfirst. Statisticalanalysis Forbothadolescenceandmidlife,Coxproportionalhazardregressionmodelswereusedto calculatehazardratio(HR)and95%confidenceinterval(95%CI)forincidentbreastcancer. Forallexposuresintheadolescentperiodthefirstmodelwasadjustedforage(asacontinuous variable)atentry.Dependingonexposure,allotherfooditemsunderstudy(meat,saltedand smokedmeat,milk,ryebread,oatmeal)plusinformationonfishandsaltedandsmokedfish werethenaddedsimultaneouslytothesecondmodel(seecutoffsaboveincovariatesassess- ment).Furtheradjustmentswerethenmadeforeducation(3categories),BMI(continuous)in midlife,ageatfirstchildbirth(3categories)andageatmenarche(continuous). Aftercombininginformationoneverbeingpregnantandageatfirstbirthintoonevariable wehadmissingvaluesfor211women.Themissingvalueswereincludedinthemultivariable PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 4/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer analysisasaspecialcategory.Wealsoreplacedthe21missingvaluesforBMIwiththemean BMIvalueoftheparticipantsofthestudy,or25.The177missingvaluesforageatmenarche werereplacedwiththemeanageofmenarcheinthecohort,or14years.Wedidnotreplace missingvaluesforfooditems,neitherforexposuresorcovariatevariables. Formidlife,thesametypesofmodelswerepresented,exceptheremidlifemeasuresforall foodconsumptionwereused.Also,informationonconsumptionofalcoholandwholewheat breadwasaddedtothemultivariatemidlifemodel. Forbothperiods,furtheradjustmentforfamilyhistoryofbreastcancer,height,andphysical activity,familyhistoryofbreastcancer,hormonalreplacementtherapyororalcontraceptive didnotchangeourriskestimates(datanotshown)andwerethereforenotincludedinour finalstatisticalmodels. Toassessthepotentialeffectsoflongitudinaldietaryhabitsonbreastcancerriskwepooled consumptionofeachfooditeminadolescenceandmidlifeintoonevariablewithfourcatego- ries;1)lowinbothadolescenceandmidlife;2)lowinadolescenceandhighinmidlife;3)high inadolescenceandlowinmidlife;and4)highinbothadolescenceandmidlife.Forthisanalysis, thefirstcategory(lowconsumptioninbothperiods)wasusedasareference.Adjustmentswere madeforsamefactorsasdescribedfortheadolescentperiod.WealsoperformedSpearman´s correlationtestbetweenconsumptiononfooditemsunderstudyinadolescenceandmidlife. Tofurtherexaminewhethertheassociationobservedforryebreadandoatmealpersisted whenotherfooditemscommonlyconsumedwereincludedwealsousedprincipalcomponent analysistoidentifydietarypatternsfromtheAGES-FFQ,includingalldietarydataavailable. Thismethodisdatadrivenandformsnewlinearfactors(dietarypatterns)byreducingdata dimensionandgroupingcorrelatedvariables(foodintake).Foreachpattern,anewvariableis created,rankingparticipantsontheiradherencetothatparticularpattern[36].Eachvariable/ patternwasfurtherdividedintotertiles,orlow,medium,andhighadherencetoeachpattern. WeusedCoxproportionalhazardregressiontotestassociationbetweenadherencetoadoles- cenceandmidlifepatternsandbreastcancerrisk,usingthelowesttertileasareference.For bothadolescenceandmidlife,adjustmentsweremadeforageatentry,BMI,education,ageat menarche,andageatfirstchild,usingthesamecutoffsaspreviouslydescribedforindividual exposuresinadolescenceandmidlife.Wealsotestedfortrendinthehazardratiosforthefirst category,usingpolynomialcontrasts(datashowninS1andS2Tables). ForallstatisticalanalysisweusedSPSSsoftware,version24.0(SPSSInc.,Chicago,Illinois; www.spss.com)andRCoreTeam(2014).R:Alanguageandenvironmentforstatisticalcom- puting.RFoundationforStatisticalComputing,Vienna,Austria;(http://www.R-project.org/). ThestudyprotocolwasapprovedbytheIcelandicEthicalReviewBoardandtheIcelandic DataProtectionAuthority(VSNb2007120014/03-7). Results Themeanageatstudyentrywas77.0yearsandstandarddeviation(SD)6.0.Themeanfollow- uptimewas8.8years(SD=3.1).Duringthattime,97womenwerediagnosedwithbreastcan- cer,withmeanageatdiagnosis81.4years(SD=6.5).Thedietaryanalyseswerebasedonpar- ticipantswhoprovidedinformationondietinmidlifeandadolescencewhenenteringthe AGES-Reykjavikcohortandwerefreeofbreastcancer. Dietinadolescence Table1showscharacteristicsofthepopulationthatprovideddataonmeat(n=2,866),milk (n=2,871),andryebread(n=2,858)consumptioninadolescence.Whencomparedwith womenwithlowconsumptionofmeatinadolescence,womenwithhighconsumptionofmeat PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 5/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer Table1. CharacteristicsoffemaleparticipantsintheAGES–ReykjavikStudy(2002–2006)accordingtoconsumptionofryebread,meatandmilkinadolescence. Ryebread Meat Milk N=2858 N=2866 N=2871 Low High Low High Low High Lessthan Dailyor 2timesor 3timesor Lessthan Dailyor daily more lessperweek moreper daily more week n=1452 n=1406 Pvalue n=958 n=1908 Pvalue n=695 n=2176 Pvalue Ageatstudyentry Mean(SD) 75.2 (5.3) 77.8 (5.7) 0.001 76.1 (5.8) 76.6 (5.5) 0.001 76.3 (5.7) 76.5 (5.6) 0.549 Median 74 78 75 76 75 76 Height(cm)(cid:3) Mean(SD) 164.4 (5.2) 163.9 (5.5) 0.012 164.3 (5.4) 164.1 (5.4) 0.001 163.9 (5.1) 164.2 (5.5) 0.202 Median 164.5 164 164 164 164 164 BMI(kg/m2)(cid:3) Mean(SD) 24.9 (3.7) 25.0 (3.8) 0.520 24.8 (3.8) 25.0 (3.8) 0.001 25.3 (3.9) 24.8 (3.7) 0.010 Median 24 24.5 24 24 24.5 24 Education,n(%) Primary 560 (39) 667 (47) 0.001 358 (37) 874 (46) 0.001 316 (46) 915 (42) 0.232 Secondary 665 (46) 572 (41) 446 (47) 792 (42) 292 (42) 951 (44) University/College 227 (15) 167 (12) 154 (16) 242 (12) 87 (13) 310 (14) Birthcohort,n(%) 1908–1919 85 (6) 236 (17) 0.001 104 (11) 216 (11) 0.016 73 (11) 247 (11) 0.386 1920–1924 285 (20) 373 (26) 205 (21) 456 (24) 157 (23) 505 (23) 1925–1929 470 (32) 435 (31) 283 (30) 621 (33) 209 (30) 699 (32) 1930–1935 612 (42) 362 (26) 366 (38) 615 (32) 256 (37) 725 (33) Locationoffirstresidence,n(%) Reykjavik 603 (42) 458 (33) 0.001 351 (37) 712 (38) 0.001 283 (41) 783 (37) 0.001 Coastalvillage 515 (36) 417 (30) 267 (28) 666 (36) 270 (39) 664 (31) Ruralarea 259 (18) 450 (33) 277 (30) 437 (23) 113 (17) 601 (28) Combinationofcoastalvillageandruralarea 53 (4) 50 (4) 45 (5) 58 (3) 18 (3) 86 (4) Ageatmenarche,n(%) (cid:20)13y 669 (46) 609 (43) 0.147 447 (47) 836 (44) 0.147 309 (45) 978 (45) 0.824 (cid:21)14y 782 (54) 794 (57) 510 (53) 1069 (56) 385 (55) 1195 (55) Ageatfirstbirth,n(%) Nochildren 101 (7) 111 (8) 0.003 81 (8) 132 (7) 0.017 40 (6) 173 (8) 0.172 (cid:20)24y 927 (64) 804 (57) 544 (57) 1197 (63) 441 (63) 1300 (60) (cid:21)25y 404 (28) 472 (34) 317 (33) 557 (29) 205 (30) 673 (31) Physicalactivity Never 600 (44) 685 (52) 0.001 405 (46) 881 (49) 0.179 310 (47) 977 (48) 0.499 Rarely/occasionally 335 (25) 242 (19) 202 (23) 376 (21) 153 (23) 426 (21) Moderate/high 426 (31) 377 (29) 281 (32) 526 (30) 194 (30) 615 (31) Familyhistoryofbreastcancer Yes 235 (16) 238 (17) 0.593 147 (15) 330 (17) 0.186 121 (17) 355 (16) 0.499 Highintakeofotherfoodgroups Fish(>4portionsp/w) 532 (37) 606 (43) 0.001 186 (19) 956 (50) 0.001 256 (37) 887 (41) 0.045 Saltedfish(oncep/wormore) 600 (42) 861 (62) 0.001 450 (47) 1008 (53) 0.002 255 (37) 1210 (56) 0.001 Oatmeal((cid:21)5timesp/w) 377 (26) 686 (49) 0.001 353 (37) 710 (38) 0.840 132 (19) 932 (43) 0.001 Saltedorsmokedmeat(oncep/wormore) 356 (25) 575 (41) 0.001 334 (35) 595 (31) 0.053 146 (21) 783 (36) 0.001 Milk(dailyormore) 974 (67) 1185 (84) 0.001 733 (77) 1432 (75) 0.328 (Continued) PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 6/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer Table1. (Continued) Ryebread Meat Milk N=2858 N=2866 N=2871 Low High Low High Low High Lessthan Dailyor 2timesor 3timesor Lessthan Dailyor daily more lessperweek moreper daily more week n=1452 n=1406 Pvalue n=958 n=1908 Pvalue n=695 n=2176 Pvalue Meat(cid:21)3timesp/w) 944 (65) 953 (68) 0.122 473 (68) 1432 (66) 0.328 Abbreviations:SD,standarddeviation. (cid:3)Measuredinmidlife—atentrytotheReykjavikStudy PvaluesarebasedonChi-squaretests,exceptforageatentry,heightandBMI,whereOne-WayANOVAtestwasused https://doi.org/10.1371/journal.pone.0198017.t001 (3timesormorep/w)wereolderatstudyentry,lesseducated,andolderwhenhavingtheir firstchild.Theyalsoconsumedmoresaltedorsmokedmeatandmoresaltedandregularfish. Womenwithhighmilkconsumption(dailyormoreoften)hadlowerBMIinmidlife,were moreoftenraisedinruralareas,andhadmorefrequentconsumptionofcodliveroil,saltedor smokedfish,totalfish,meat,andoatmeal.Whencomparedwithlessthandailyryebreadcon- sumption,womenwhoconsumedryebreaddailyormoreoftenwereolderwhenenteringthe study,hadlowereducationlevel,weremorecommonlyraisedinruralareas,wereolderupon firstbirth,andlessphysicallyactive.Theyalsoconsumedfishmorefrequently,particularly saltedorsmokedfishaswellasmilk,oatmeal,andmeat,includingsaltedorsmokedmeat. Table2presentshazardratios,with95%CI,forbreastcanceranddietinadolescence.No statisticallysignificantassociationwasfoundformeat,saltedandsmokedmeatandmilkcon- sumption.Forwholegrainproducts,wefoundapositiveassociationbetweenhighconsump- tionofryebread(dailyormoreoften)inadolescenceandbreastcancerrisk(HR1.7,95%CI Table2. Multivariateanalysisofbreastcancerriskbymeat,milkandwholegrainintakeinadolescence. Meat Saltedor Milk Ryebread Oatmeal smokedmeat N=2866 N=2862 N=2871 N=2858 N=2856 Low High Low High Low High Low High Low High 2timesorless 3timesor 3timesamonth Oncep/wor Lessthan Daily Lessthan Dailyor 4timesorless 5timesor p/w morep/w orless more daily ormore daily more p/w morep/w n=958 n=1908 n=1930 n=932 n=695 n=2176 n=1452 n=1406 n=1791 n=1065 Breastcancer 28 68 61 36 29 68 41 55 68 29 (%) (2.9) (3.6) (3.2) (3.9) (4.2) (3.1) (2.8) (3.9) (3.8) (2.7) Ageadjusted 1.0 1.2 1.0 1.3 1.0 0.8 1.0 1.5 1.0 0.7 HR (95%CI) (ref.) (0.8–1.9) (ref.) (0.8–1.9) (ref.) (0.50– (ref.) (1.0–2.2) (ref.) (0.5–1.2) 1.2) Multivariate 1.0 1.3 1.0 1.4 1.0 0.7 1.0 1.7 1.0 0.7 HR(cid:3) (95%CI) (ref.) (0.8–2.0) (ref.) (0.9–2.2) (ref.) (0.4–1.1) (ref.) (1.1–2.6) (ref.) (0.5–1.2) Abbreviations:CI,confidenceinterval;HR,hazardratio:p/w,perweek (cid:3)MultivariateHR;adjustedforageatentry,education,bodymassindexinmidlife,ageatfirstchildandageatmenarche.Allfooditemsunderstudy(meat,saltedand smokedmeat,milk,ryebread,oatmeal)plusinformationonfishandsaltedandsmokedfishwerethenaddedsimultaneouslytothemultivariatemodel.The multivariateanalysisincluded2810women,thereof95withbreastcancer. https://doi.org/10.1371/journal.pone.0198017.t002 PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 7/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer 1.1–2.6),whencomparedwithlowerconsumption(lessthandaily).Nosignificantassociation wasobservedforoatmealconsumption.Whenaddingearlyliferesidencetothemultivariate modeltheriskestimatesforhighryebreadconsumptionincreased(HR1.8,95%CI1.2–2.9). Nodifferencewasobservedforotherestimates. Wefurtherdividedryebreadconsumptionintothreegroups(twotimesorlessperweek, 3–6timesperweek,anddailyormore)andexploredtheassociationwithbreastcancerrisk, wherewefoundasignificanttrendacrossthegroups,HR1.0(95%CI0.5–2.0)andHR1.7 (95%CI0.9–3.2),respectively(P =0.043). trend Midlifediet Formidlife(Table3),nosignificantassociationwasobservedformeatandmilkconsumption, althoughamarginallypositiveassociationwasobservedforhighconsumption(onceperweek ormore)ofsaltedorsmokedmeat(HR1.6,95%CI1.0–2.6)comparedwithwomenwithlow consumption(3timesamonthorless).Forwholegrainproducts,noassociationwasobserved forwholewheatbreadwhileastatisticallysignificantpositiveassociationwasobservedfor highconsumption(dailyormore)ofryebread(HR1.8,95%CI1.1–2.9)whencomparedwith lowerconsumption(lessthandaily).Nosignificantassociationwasobservedforoatmeal.No differencewasobservedforanyoftheriskestimateswhenearlyliferesidencewasaddedtothe model. Ryebreadconsumptioninmidlifewasfurtherdividedintothreegroups(twotimesorless perweek,3–6timesperweek,anddailyormore).Comparedwiththegroupwiththelowest consumption,theriskestimatesfor3–6timesperweekanddailyormorewere1.4(95%CI 0.8–2.4)and2.3(95%CI1.3–4.1),respectively(P <0.01). trend Longtermconsumption Table4presentsSpearman’scorrelationbetweendietaryhabitsinadolescenceandmidlife. Thestrongestcorrelationwasfoundforryebreadconsumption(ρ=0.50,P=0.001)andthe lowestformeatconsumption(ρ=-0.19,P=0.001). Table5presentslongtermconsumptionformeat,saltedorsmokedmeat,milk,ryebread, andoatmealwithlowconsumptioninadolescenceandmidlifeasareferencecategory.Aposi- tiveassociationwasobservedforhighryebreadconsumptioninadolescenceandmidlife(HR 2.1,95%CI1.2–3.5).Aninverseassociationwasobservedbetweenbreastcancerriskandhigh consumptionofoatmealinbothadolescenceandmidlife(HR0.4,95%CI0.2–0.9)(P = trend 0.07).Noassociationwasobservedbetweenbreastcancerandmeat,saltedorsmokedmeat andmilk. Supplementarymaterial—dietarypattern Fourdietarypatternswereextractedfortheadolescentperiod.Factorloadingcoefficientsfor thosepatternsarepresentedinS1Table.Onepatterncontainingryebreadinadditionto bloodliversausage,saltedmeat,saltedfish,andoatmealrepresentstraditionalIcelandicdietin theearlierhalfofthe20thcentury.Highadherencetothispatternwasnotsignificantlyassoci- atedwithbreastcancerrisk(HR1.395%CI0.7–2.1).Borderlineinverseassociationwas observedforthehighestadherencetoapatternhighinconsumptionoffish,blood/liversau- sage,oatmeal,fishoil,andmilkinadolescence(HR0.6,95%CI0.4–1.0)(P =0.049)(S2 trend Table). Fourdietarypatternswerealsoextractedforthemidlifeperiod.Noassociationwas observedforanyofthosepatterns,includingthedietarypatternincludingryebreadconsump- tion(datanotshown). PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 8/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer Discussion Inthispopulationbasedcohort,dailyconsumptionofryebreadduringbothadolescenceand midlifewaspositivelyassociatedwithbreastcancer.Conversely,wefoundreducedriskfor breastcanceramongwomenwhoconsumedoatmealpersistentlybothinadolescenceand midlife.However,nodietarypatternineitheradolescenceormidlifethatincludedryebread wassignificantlyassociatedwithbreastcancerwhileapatterninadolescencethatrepresented fish,blood/liversausage,oatmeal,fishoil,andmilkseemedtobeprotectiveforbreastcancer. Wealsoobservedborderlineriskofbreastcancerwithhighmidlifeconsumptionofsaltedor smokedmeat.Noassociationwasfoundbetweenhighmilkintakeandbreastcancerriskin eitherperiod. Tothebestofourknowledge,nostudyhasspecificallyaddressedadolescentconsumptionof ryebread,acommonwholegrainproductintheNordiccountries,inrelationtolate-lifebreast cancer.Afewstudieshaveanalyzedtotaladolescentconsumptionoflignans,acommonphyto- estrogeninwholegraincereals—suchasrye,wheat,oats,andbarley—butalsoinlegumes,oil- seeds,andvariousfruitsandvegetables[37].ACanadiancasecontrolstudyfoundthathigh adolescentintakeoflignansreducedtheriskofbreastcancer.However,althoughryebreadwas includedinthedietassessmentofthestudy,itwasnotcommonlyconsumedandtheseresults canalsobeconfoundedbyotherhealthyeatinghabits[20].ResultsfromtheNurses’Health Studysuggestthathighconsumptionofwholegrainsinadolescencecanreducetheriskofpre- menopausalbreastcancer[22].However,themaindifferencebetweenthisstudyandourswas ryebreaddoesnotseemtobeincludedintotalwholegrainconsumptionintheNurse´sHealth Studyquestionnaire.Also,thewomeninourcohortwereallpost-menopausalwithahigh meanageatdiagnosis,andthereforepossiblydifferentcarcinogenicprocess[38]. Thefewstudiesontotalwholegrainconsumptioninadultsandbreastcancerhaveeither suggestedaprotective[23,24]ornoassociation[25,26].Themajordifferencebetweenmost Table3. Multivariateanalysisofbreastcancerriskbymeat,milkandwholegrainintakeinmidlife. Meat Saltedor Milk Ryebread Oatmeal Wholewheatbread smokedmeat N=2871 N=2864 N=2864 N=2875 N=2768 N=2865 Low High Low High Low High Low High Low High Low High 2timesor 3timesor 3timesa Oncep/w Lessthan Dailyor Lessthan Dailyor 4timesor 5timesor Lessthan Dailyor lessp/w morep/w monthor ormore daily more daily more lessp/w morep/w daily more less n=1203 n=1668 n=2210 n=654 n=1247 n=1617 n=1918 n=957 n=2094 n=674 n=1238 n=1627 Breast 41 56 71 26 41 56 57 40 81 16 44 53 cancer (3.4) (3.4) (3.2) (4.0) (3.2) (3.5) (3.0) (4.2) (3.7) (2.3) (3.6) (3.3) (%) Age 1.0 1.0 1.0 1.3 1.0 1.1 1.0 1.5 1.0 0.6 1.0 0.9 adjusted HR (95%CI) (ref.) (0.6–1.5) (ref.) (0.8–2.1) (ref.) (0.7–1.6) (ref.) (1.0–2.3) (ref.) (0.4–1.1) (ref.) (0.6–1.4) Multivariate 1.00 1.0 1.0 1.6 1.0 1.1 1.0 1.8 1.0 0.6 1.0 0.8 HR(cid:3) (95%CI) (ref.) (0.6–1.4) (ref.) (1.0–2.6) (ref.) (0.7–1.7) (ref.) (1.1–2.9) (ref.) (0.4–1.1) (ref.) (0.5–1.3) Abbreviations:CI,confidenceinterval;HR,hazardratio. (cid:3)MultivariateHR;adjustedforageatentry,education,bodymassindexinmidlife,alcoholconsumptioninmidlife,ageatfirstchildandageatmenarche.Allfooditems understudy(meat,saltedandsmokedmeat,milk,ryebread,oatmealandwholewheatbread)plusinformationonfishandsaltedandsmokedfishwerethenadded simultaneouslytothemultivariatemodel.Themultivariateanalysisincluded2813women,thereof97withbreastcancer. https://doi.org/10.1371/journal.pone.0198017.t003 PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 9/16 Ryebreadintakeinadolescenceandmidlifeandriskofbreastcancer Table4. Dietaryhabitsamongparticipantsthroughdifferenttimeperiods. Adolescence Midlife Spearmans´sρ P n(%) n(%) Ryebread 0.50 0.001 Lessthandaily 1452(51) 1918(67) Dailyormore 1406(49) 957(31) Milkandmilkproducts 0.44 0.001 Lessthandaily 695(24) 1247(44) Dailyormore 2176(76) 1617(56) Meat -0.19 0.001 2timesorlessp/w 958(33) 1203(42) 3timesormorep/w 1908(67) 1668(58) Saltedorsmokedmeat 0.36 0.001 3timesamonthorless 1930(67) 2210(77) Onceormorep/w 932(33) 654(23) Oatmeal 0.38 0.001 4timesorlessp/w 1791(63) 2715(76) 5timesormorep/w 1065(37) 690(24) Vegetables 0.38 0.001 Never 585(20) 163(6) 6timesp/worless 2175(76) 2845(87) Daily 105(4) 213(7) Fruit 0.24 0.001 Never 1013(36) 114(4) 6timesp/worless 1784(62) 2501(87) Daily 68(2) 256(9) https://doi.org/10.1371/journal.pone.0198017.t004 oftheseandthepresentstudyisthatwedisentangledwholegrainconsumptionintorye, wholewheatbreadandoatmeal.Differenttypesofwholegrainscontaindissimilarbioactive compounds[7]whichmayactdifferentlyonbreastcancergenesis. ADanishstudy[25]reportednoassociationbetweenneithertotaladultconsumptionof wholegrainsnorwhenanalyzedseparately(ryebread,wholegrainbread,andoatmeal)with breastcancer.However,thewomenintheDanishcohortwereyoungeratstudyentryandat diagnosis(averageage56years)thanparticipantsintheAGES-ReykjavikStudy(averageage 77years).Thismightreflectapreviouslyreporteddifferenceincharacteristicsofdiagnosed breasttumorsinolderwomen(over70)comparedwiththoseinyoungerwomen[38].Indeed, wefoundnoassociationforryebreadwhenaseparateanalysiswasmadeforwomenwho werealreadydiagnosedwithbreastcanceratstudyentry(meanageatdiagnosis64years,data notshown). Prolongedexposuretoryebreadmightthereforepossiblyexplaintheobservedriskfound inourcohort.Ryebreadisrichinlignans,whichcanbeconvertedintoenterolignansbythe gutmicrobiome.Enterolignanshavebeensuggestedtoenhancebreastcancerriskreduction [7,39,40].However,theycanalsoexpressweakestrogenicaffinityandcanactbothasagonists orantagonistsinbreasttumors.althoughthismechanismisconsideredcomplex[7,41–43]. Nevertheless,longitudinalexposuretoestrogens,exemplifiedbyearlymenarche,latemeno- pause,anduseofhormonalreplacementtherapy,areconsideredasamajorriskfactorsfor breastcancer[44].Therefore,itmaybehypothesizedthatlongtermexposuretophytoestro- gensviaryebreadconsumptionmayhaveasimilareffect.Indeed,ouranalysisondietary PLOSONE|https://doi.org/10.1371/journal.pone.0198017 May30,2018 10/16

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risk [19], as was total high adolescent consumption of lignans [20], a common phytoestrogen commonly found in whole grains [21]. High consumption
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