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PLOSONE:AlcoholConsumption,TypesofAlcohol,andParkinsonsDisease

Alcohol Consumption, Types of Alcohol, and Parkinsons Disease


RuiLiu

, XuguangGuo, YikyungPark, JianWang, XuemeiHuang, AlbertHollenbeck, AaronBlair, HongleiChen

Published:June19,2013

http://dx.doi.org/10.1371/journal.pone.0066452

Abstract
Background

TheepidemiologicevidenceonalcoholconsumptionandParkinsonsdisease(PD)isequivocal.Weprospectivelyexaminedtotal
alcoholconsumptionandconsumptionofspecifictypesofalcoholicbeverageinrelationtofutureriskofPD.
Methods

Thestudycomprised306,895participants(180,235maleand126,660female)ages5071yearsin19951996fromtheNIH
AARPDietandHealthStudy.Consumptionofalcoholicbeveragesinthepast12monthswasassessedin19951996.Multivariate
oddsratios(OR)and95%confidenceintervals(CI)wereobtainedfromlogisticregressionmodels.
Results

Atotalof1,113PDcasesdiagnosedbetween2000and2006wereincludedintheanalysis.Totalalcoholconsumptionwasnot
associatedwithPD.However,theassociationdifferedbytypesofalcoholicbeverages.Comparedwithnonbeerdrinkers,the
multivariateORsforbeerdrinkerswere0.79(95%CI:0.68,0.92)for<1drink/day,0.73(95%CI:0.50,1.07)for11.99drinks/day,
and0.86(95%CI:0.60,1.21)for2drinks/day.Forliquorconsumption,amonotonicincreaseinPDriskwassuggested:ORs(95%
CI)were1.06(0.91,1.23),1.22(0.94,1.58),and1.35(1.02,1.80)for<1,11.99,and2drinks/day,respectively(Pfortrend
<0.03).Additionalanalysesamongexclusivedrinkersofonespecifictypeofalcoholicbeveragesupportedtherobustnessofthese
findings.Theresultsforwineconsumptionwerelessclear,althoughaborderlinelowerPDriskwasobservedwhencomparingwine
drinkersof11.99drinks/daywithnonedrinkers(OR=0.74,95%CI:0.53,1.02).
Conclusions

OurresultssuggestthatbeerandliquorconsumptionmayhaveoppositeassociationswithPD:lowtomoderatebeerconsumption
withlowerPDriskandgreaterliquorconsumptionwithhigherrisk.Thesefindingsandpotentialunderlyingmechanismswarrant
furtherinvestigations.
Citation:LiuR,GuoX,ParkY,WangJ,HuangX,HollenbeckA,etal.(2013)AlcoholConsumption,TypesofAlcohol,and
ParkinsonsDisease.PLoSONE8(6):e66452.doi:10.1371/journal.pone.0066452
Editor:YiqingSong,Brigham&Women'sHospital,andHarvardMedicalSchool,UnitedStatesofAmerica
Received:December20,2012Accepted:May4,2013Published:June19,2013
Thisisanopenaccessarticle,freeofallcopyright,andmaybefreelyreproduced,distributed,transmitted,modified,built
upon,orotherwiseusedbyanyoneforanylawfulpurpose.TheworkismadeavailableundertheCreativeCommonsCC0
publicdomaindedication.
Funding:ThisstudywassupportedbytheintramuralresearchprogramoftheNationalInstituteofHealth,theNational
InstituteofEnvironmentalHealthSciences(Z01ES101986)andtheNationalCancerInstitute(Z01CP01019602).The
fundershadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,orpreparationofthemanuscript.
Competinginterests:XG,isemployedbyWestatInc.,whichisagovernmentcontractingcompanythathelpswithourdata
analysis.However,thisdoesnotaltertheauthors'adherencetoallthePLOSONEpoliciesonsharingdataandmaterials.

Introduction
Alcoholdrinkingisacommonlifestylechoicethatcanhavesignificantandcomplexbehavioral,medicalandpublichealth
consequences[1],[2].Whileheavyalcoholuseisundoubtedlydetrimentaltohealth,lighttomoderatealcoholconsumptionhas
beenlinkedtolowerriskofcardiovasculardisease[1]andmorerecentlytolowerriskofcognitivedeclineanddementia[3],[4].
Little,however,isknownaboutalcoholdrinkingandParkinsonsdisease(PD).Likesmokingandcoffeeconsumption,excessive
alcoholdrinkingmaybeafeatureofarisktakingpersonalitythathasbeenhypothesizedtobeassociatedwithlowerPDrisk[5].
Moreover,consumptionofalcoholicbeverages,particularlybeer,elevatesplasmaurate[6]urateisapotentfreeradicalscavenger
thathasbeenlinkedtolowerPDrisk[7][10]andslowerPDprogression[11],[12].Giventhepaucityofexistingepidemiologic
evidence,weexaminedtheconsumptionoftotalandspecifictypesofalcoholicbeveragesandPDriskinalargeUScohortofolder
adults.

Methods
StudyPopulationandPDCaseIdentification

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TheNIHAARPDietandHealthStudyconductedacomprehensivebaselinesurveyondietandlifestylein19951996andrecruited
566,398AARPmembers(ages50to71)fromsixUSstates(California,Florida,NorthCarolina,Pennsylvania,NewJersey,and
Louisiana)andtwometropolitanareas(AtlantaandDetroit)[13].AARP,formerlyknownastheAmericanAssociationofRetired
Persons,isanonprofitorganizationwithmembersof50yearsorolderacrosstheUS.Between2004and2006,afollowupsurvey
wasmailedtosurvivingparticipantstoupdatelifestyleexposuresandtoascertaintheoccurrenceofmajorchronicdiseases,
includingPD.ParticipantsreportedlifetimediagnosisofPDandtheyearofdiagnosisinthefollowingcategories:before1985,
19851994,19951999,or2000topresent.Atotalof318,257participants(187,496menand130,761women)participatedinthe
followupsurveyandwerethereforeincludedinthecurrentanalysis.Oftheseparticipants,2,432reportedaPDdiagnosisand
315,825didnot.WewereconcernedthatsomePDpatientsmighthavealteredtheirdietarybehaviorsandlifestyleevenbefore
diagnosisduetononmotororsubtlemotorsymptoms(i.e.reversecausality),andthereforeexcludedallcaseswhoreportedaPD
diagnosisbeforetheyear2000(n=1,094)fromtheanalyses.Wefurtherexcluded214selfidentifiedPDpatientswhosediagnosis
waslatercontradictedbythemselvesorbytheirtreatingphysiciansinthevalidationstudydescribedbelow.Inaddition,wealso
excluded9caseswithextremeenergyintakes(definedasvaluesmorethan2interquartilerangesabovethe75thorbelowthe25th
percentileonthelogtransformedenergyintakedistribution),and2missingonalcoholconsumption.Amongparticipantswhodid
notreportaPDdiagnosis,weexcluded8,050participantswithmissingPDstatus,1,682withextremeenergyintake,and311with
missinginformationonalcoholconsumption.Thefinalanalyticdatasetincluded1,113selfreportedPDcaseswhosefirstdiagnoses
wereafter2000,and305,782participantswithoutPD.
WevalidatedtheaccuracyofselfreportedPDdiagnosesinconjunctionwithDNAcollectionforPDgeneticresearch.Thedetailsof
thisvalidationhavebeendescribedpreviously[14].Briefly,wefirstaskedpotentialPDpatientstoconfirmtheirearlierselfreports
andthenaskedtheirtreatingphysicianstocompleteadiagnosticquestionnaireandtoprovideacopyofthepatientsmedical
records.Themedicalrecordsweresubsequentlyreviewedbyamovementdisorderspecialist(X.H.).Thediagnosiswasconsidered
validif:1)thetreatingneurologistconfirmedthediagnosisor2)ifthemedicalrecordincludedafinalPDdiagnosisorevidenceof
twoormorecardinalsignsofPD(withonebeingresttremororbradykinesia),aprogressivecourse,responsivenessto
dopaminergictreatments,andabsenceoffeaturesthatsuggestedanalternativediagnosis.Ofthe1,069physicianresponses
received,940(87.9%)PDdiagnoseswereconfirmed.Theconfirmationratewassimilaracrossyearsofdiagnosis:83.3%forcases
diagnosedbefore1985,92.8%forcasesdiagnosedin19851994,87.9%forcasesdiagnosedin19951999,and87.2%forcases
diagnosedafter2000.
ExposureAssessment

Aspartofthecohortsbaselinesurveyin19951996,consumptionofalcoholicbeverageswasassessedusingavalidatedself
administered124itemfoodfrequencyquestionnaire(FFQ)[15].TheFFQqueriedconsumptionofbeerduringthesummer,beer
duringtherestoftheyear,liquorormixeddrinks,orwineorwinecoolersduringtheprevious12months.Foreachdrink,
informationwassoughtonfrequencyofconsumption(tencategoriesrangingfromneverto6times/day)andthreeportionsizes
(<1,12,>2drinks).Drinksofalcoholperdaywerecomputedfortotalalcoholandforeachtypeofalcoholicbeverage,withone
drinkofalcoholicbeveragedefinedasone12fluidouncebeer,one5fluidounceglassofwine,orone1.5ounceshotofliquor,
basedontheUSDepartmentofAgriculturesFoodGuidePyramid[16].Eachdrinkcontainsapproximately13gramsofalcohol.
Dataoncoffeeandothercaffeinecontainingdrinksorfoodswerealsocollectedaspartofthedietarysurvey.Inadditiontodiet,the
baselinesurveyalsocollecteddataonbasicdemographicsandlifestylefactorssuchassmokinghabit,physicalactivity,andself
evaluatedhealthstatus.
StatisticalAnalysis

Intheprimaryanalyses,wecategorizedtheconsumptionfrequenciesintodrinksperday:none,<1,11.99,22.99,33.99,44.99
and5fortotalalcohol,andnone,<1,11.99,and2forindividualalcoholicbeverages(beer,wine,liquor).Multivariateoddsratios
(OR)and95%confidenceintervals(CI)werederivedfromlogisticregressionmodels,firstadjustingforageatbaseline(in5year
groups),andthenadditionallyadjustingforsex,race(whitesvs.nonwhites),educationlevel(lessthan12years,12yearsor
completedhighschool,posthighschoolorsomecollege,collegeandpostgraduate),maritalstatus(marriedorlivingasmarried,
widowed,divorced,separatedornevermarried),smokingstatus(neversmokers,pastsmokers[yearssincequitting:35,3034,
2029,1019,19],andcurrentsmokers[cigarettesperday:110,1120,>20]),caffeineintake(quintiles),generalhealthstatus
(excellent/verygood,good,fairorpoor),andphysicalactivity(never/rarely,13times/month,12times/week,34times/week,and
5times/week).Specifictypesofalcoholicbeverageconsumptionwerefirstanalyzedindividuallyandthenmutuallyadjustedfor
eachother.Wheneveramonotonictrendwassuggested,weexaminedthestatisticalsignificanceforalineartrendbyincludingthe
midpointofeachexposurecategoryasacontinuousvariableintheregressionmodel.Finally,weconductedseveralsensitivityand
stratifiedanalysestoexaminethenatureandrobustnessofourkeyfindings.First,weexaminedriskassociatedwithspecifictypes
ofalcoholicbeverageinrelationtoPDamongnondrinkersofothertypesofalcoholicbeverages.Second,westratifiedthe
analysesaccordingtoknownPDriskfactors:age(medianinyears),gender(menandwomen),smokingstatus(neverandever
[currentandpastsmokers]),andcaffeineintake(median).Statisticaltestingformultiplicativeinteractionswasexaminedbyadding
aproducttermbetweenalcoholintakeandpotentialmodifierintotheregressionmodel.Allstatisticalanalyseswereperformed
usingSAS,version9.1(SASInstituteInc.,Cary,NC).Significancetestsweretwotailedwith=0.05.
StandardProtocolApprovals,Registrations,andPatientConsents

Participantsconsentedtothestudybyreturningsurveyquestionnaires.ThestudyprotocolwasapprovedbytheInstitutional
ReviewBoardoftheNationalInstituteofEnvironmentalHealthSciencesandtheSpecialStudiesInstitutionalReviewBoardofthe
NationalCancerInstitute.

Results
PopulationcharacteristicsaccordingtototalalcoholconsumptionareshowninTable1.Comparedwithnondrinkers,alcohol
drinkersweremorelikelytobemen,nonHispanicWhites,haveacollegeeducationorabove,marriedorlivingasmarried,and
pastorcurrentsmokers.Theywerealsomorelikelytoreporthighercaffeineintake,slightlyhigherphysicalactivity,andexcellentor
verygoodhealthstatus.

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Table1.BaselinePopulationCharacteristicsAccordingtoTotalAlcoholConsumptionCategories,NIHAARPDietandHealthStudy,19952006.

http://dx.doi.org/10.1371/journal.pone.0066452.t001
TotalalcoholconsumptionatbaselinewasnotrelatedtofuturePDrisk(Table2).Whenspecifictypesofalcoholicbeverageswere
examinedindividually,theeffectsappearedtodifferbybeveragetype.Comparedwithnonbeerdrinkers,themultivariateORsfor
beerdrinkerswere0.79(95%CI:0.68,0.92)for<1drink/day,0.73(95%CI:0.50,1.07)for11.99drinks/day,and0.86(95%CI:
0.60,1.21)for2drinks/day.Incontrast,amonotonicincreaseinPDriskwasobservedwithgreaterconsumptionofliquor(Pfor
trend=0.03).ThemultivariateadjustedORswere1.06(95%CI:0.91,1.23)forlessthan1drinksofliquorperday,1.22(95%CI:
0.94,1.58)for11.99drinksperday,and1.35(95%CI:1.02,1.80)for2ormoredrinksperday.Resultsforwineconsumption
werelessclear,althoughanonsignificantloweredPDriskwasobservedwhencomparingdrinkersof11.99drinksofwine/day
withnonwinedrinkers(OR=0.74,95%CI:0.53,1.02).

Table2.OddsRatiosofParkinsonsDiseaseAccordingtoConsumptionofTotalAlcoholandSpecificTypesofAlcoholicBeverages,NIHAARP
DietandHealthStudy,19952006.

http://dx.doi.org/10.1371/journal.pone.0066452.t002
Whenrestrictedtheanalysestoexclusivedrinkersofaspecifictypeofalcoholicbeverage(Table3),significantmonotonictrends
wereobservedforbothbeerdrinkers(Pfortrend=0.05)andliquordrinkers(Pfortrend=0.02).Comparedwithnonalcohol
drinkers,thosewhoconsumedoneormoredrinksofbeerperdayhad59%loweredriskofPD(OR=0.4195%CI:0.17,1.00).In
contrast,liquordrinkersconsumingoneormoredrinksperdayhadmorethan2foldhigherriskofPDthannonalcoholdrinkers.
NoassociationwasobservedbetweenexclusivedrinkersofwineandriskofPD.

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Table3.OddsRatiosofParkinsonsDiseaseAccordingtoExclusiveDrinkersofaSpecificTypeofAlcoholicBeverage,NIHAARPDietand
HealthStudy,19952006.

http://dx.doi.org/10.1371/journal.pone.0066452.t003
Finally,weconductedanexploratoryanalysistoexaminewhethertheassociationbetweenbeerorliquorconsumptionandriskof
PDwasmodifiedbyage,sex,smokingstatus,andcaffeineintake(Figure1).Generally,theanalysesrevealednocleareffect
modifications.Althoughastatisticallysignificantinteractionwasfoundbetweenbeerconsumptionandsmoking,nocleartrends
wereobserved.Forliquor,ahigherPDriskwasobservedwithincreasingliquorconsumptionforthoseaged62.4yearandolder
thanyoungerindividuals(Pfortrend=0.003).Amarginalsignificantinteraction(P=0.055)wasobservedbetweengenderandliquor
consumptionwithapositiveassociationinmen(Pfortrend=0.005)butnotinwomen(Pfortrend=0.1).Finally,visualinspectionsof
thefiguresuggestthatwhenstratifiedbycaffeineintake,theassociationofbeerorliquorwithPDonlyexistsamongindividualswith
highercaffeineintake.However,thePforinteractionwasnotstatisticallysignificant.

Figure1.Oddsratiosand95%confidenceintervalsofParkinsonsdiseaseaccordingtobeerandliquorconsumptionwithinsubgroups,NIH
AARPDietandHealthStudy,19952006.

indicatespforinteraction.
http://dx.doi.org/10.1371/journal.pone.0066452.g001

Discussion
Inthislargeprospectivecohortstudyofolderadults,wedidnotfindevidenceforanassociationbetweentotalalcoholconsumption
andriskofPD.However,adifferentialeffectwasobservedfordifferenttypesofalcoholicbeverages.Whilelowtomoderatebeer
consumptionmaybeassociatedwithlowerPDrisk,greaterliquorconsumptionwasassociatedwithhigherPDrisk.Wine
consumptiondidnotappeartobeassociatedwithriskofPD.
TheroleofalcoholdrinkinginPDetiologyhasnotbeenextensivelyevaluated.Mostofthepreviousepidemiologicstudieswere
casecontrolstudiesanddidnotdifferentiatethespecifictypesofalcoholicbeverage,andmostdidnotfindanassociationbetween
alcoholconsumptionandPDrisk.Thefewexistingprospectivestudiesalsoshowedinconsistentresults.Detailedstudydesignand
resultsofpreviouspublicationsaresummarizedinTableS1.OurfindingthatlowtomoderatebeerconsumptionandlowerPDrisk
isconsistentwiththatfromtheHealthProfessionalsFollowupStudyandtheNursesHealthStudy[17],whileresultonliquor
consumptionwasdifferent.ResultsfromtherecentCancerPreventionStudyIINutritionCohort,however,foundnoassociationwith
anytypesofalcoholbeverages[18].IntheSwedishtwinsstudy,alcoholintakeingeneralwasnotassociatedwithPDrisk
however,stratifiedanalysesamongneversmokersshowedalowerPDriskforeverdrinkersascomparedwithabstainers[19].The
discrepantresultswithalcoholicbeveragesobservedacrossstudiesmaybeduetodifferencesinstudydesign,dietary
assessment,andadjustmentforpotentialconfounders(e.g.smokingandcoffeeconsumption).Forexample,themajorityofthe
studiesarecasecontrolstudieswithprevalentcaseswhichmightbemorepronetorecallbiasesandreversecausation.
BiologicalmechanismsthatlinkalcoholandPDareunclearandspeculative.Ourfindingofdifferentialassociationswithspecific
typesofalcoholicbeveragessuggestsmechanismsinvolvingfactorsotherthanorinadditiontoethanolitself.Beer,butnotwineor
liquor,containsalargeamountofpurine,whichmayworksynergisticallywithethanoltoaugmentplasmaurate[6].Urateisa
potentfreeradicalscavenger[20],andhasbeenlinkedtolowerPDrisk[7][10]andslowerclinicalprogressionamongPDpatients
[11],[12].Relativetowineorliquor,beeralsocontainshighlevelsofniacin[21],whichhasbeenreportedtoreducetheriskofPD
[22].OurfindingofhigherPDriskamongheavyliquordrinkersismoredifficulttoexplain.Wespeculatethismayberelatedtothe

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relativelyhighproportionofpureethanolfoundinliquorcomparedtobothwineandbeer[23].Pureethanolhasbeenshownto
induceoxidativestressbyactingasaprooxidantandmaybeproinflammatory[24].Moreover,liquorandotherdistilledbeverages
containnovitaminsorantioxidants[21].Polyphenoliccomponents(e.g.,resveratrol)foundinredwinehasbeenshowntoattenuate
neurotoxin6hydroxydopamine(6OHDA)inducedtoxicityinanimalmodelsofPD[25],[26]viaitsantioxidantandanti
inflammatorypotentials.However,existingepidemiologicstudiesincludingourshavelargelyfailedtofindaneuroprotectiveeffectof
wineonriskofPD.
Majorstrengthsofthecurrentstudyincludetheprospectivedatacollection,largesamplesize,examinationoftotalandspecific
typesofalcoholicbeverages,andstratifiedanalysesbyPDriskfactors.Ourstudyalsohasseverallimitations.Weonlyassessed
thefrequencyandportionsizeofalcoholconsumptioninthepast12monthspriortobaseline,thereforewewereunabletoexamine
lifetimealcoholconsumptionordrinkingpatternsinrelationtoPDrisk.Further,exposuremisclassificationwaslikelyifthis
misclassificationwasrandom,itwouldattenuatethetruerelationship.Inaddition,duetotheobservationalnatureofthisanalysis,
wecouldnotexcludethepossibilityofresidualorunmeasuredconfounding.Nevertheless,wetriedtocontrolforavarietyofsocio
economicvariablesandconductedstratifiedanalysesbyknownPDriskfactors.IntermsofPDassessment,wehadtorelyonself
reporteddiagnosestoidentifypotentialPDpatientsinthislargeUScohort,andthisinevitablyintroducedreportinganddiagnostic
errors.However,ourvalidationstudyvalidated88%oftheselfreporteddiagnosesamongwhommedicalinformationwasavailable.
Wefurtherremovedfromtheanalysispersonswithidentifiederroneousreportsormisdiagnoses.Finally,ouranalysiswas
conductedonlyamongparticipantsinthefollowupsurveyandthereforewecouldnotexcludethepossibilityofselectionbiasdue
tolosstofollowup.
Inconclusion,ourfindingssuggestthattotalalcoholconsumptionisnotrelatedtotheriskofPD,butspecifictypesofalcoholic
beveragesmayhavedifferenteffectsonPDrisk.OurobservationoflowerPDriskamonglowtomoderatebeerdrinkersbuthigher
PDriskamongheavyliquordrinkerswarrantfurtherinvestigations.

SupportingInformation
TableS1.

CharacteristicsofStudiesontheAssociationbetweenAlcoholConsumptionandParkinsonsDisease.
doi:10.1371/journal.pone.0066452.s001
(DOC)

Acknowledgments
TheauthorsaregratefultothecontinuouscontributionoftheNIHAARPDietandHealthStudyparticipants.

AuthorContributions
Conceivedanddesignedtheexperiments:RLHC.Performedtheexperiments:RLXGHC.Analyzedthedata:RLXGHC.
Contributedreagents/materials/analysistools:XGHC.Wrotethepaper:RLHC.Substantialcontributionsanalysisand
interpretationofdatarevisingitcriticallyforimportantintellectualcontentandfinalapprovaloftheversiontobepublished:RLXG
YPJWXHAHABHC.

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