Gender differences in the transmission of risk for antisocial behavior problems across generations

16 Pages·2017·1.56 MB·English

RESEARCHARTICLE
Gender differences in the transmission of risk
for antisocial behavior problems across
generations
PinLi1,JillB.Becker2,3*,MaryM.Heitzeg3,MicheleL.McClellan4,BethGloverReed5,
RobertA.Zucker3
1 SchoolofPublicHealth,UniversityofMichigan,AnnArbor,Michigan,UnitedStatesofAmerica,
2 DepartmentofPsychologyandtheMolecular&BehavioralNeuroscienceInstitute,UniversityofMichigan,
AnnArbor,Michigan,UnitedStatesofAmerica,3 DepartmentofPsychiatry,UniversityofMichigan,Ann
a1111111111
Arbor,Michigan,UnitedStatesofAmerica,4 DepartmentofHistoryandtheResidentialCollege,Universityof
a1111111111
Michigan,AnnArbor,Michigan,UnitedStatesofAmerica,5 SchoolofSocialWorkandtheDepartmentof
a1111111111 Women’sStudies,UniversityofMichigan,AnnArbor,Michigan,UnitedStatesofAmerica
a1111111111
a1111111111 *[email protected]
Abstract
OPENACCESS Previousstudieshaveshownthatchildrenofalcoholusedisorder(AUD)parentsaremore
Citation:LiP,BeckerJB,HeitzegMM,McClellan likelytodevelopalcoholproblemsaswellasantisocialandotherbehaviorproblems.Thepur-
ML,ReedBG,ZuckerRA(2017)Gender poseofthisstudywastoexaminegenderdiscordanceintheeffectofearlymaternaland
differencesinthetransmissionofriskforantisocial
paternalinfluencesonantisocialbehaviorsofboysandgirls,aswellastheenvironmental
behaviorproblemsacrossgenerations.PLoSONE
factorsthatmoderatetheparentaleffects.Specifically,weexaminedtheeffectsofchildhood
12(5):e0177288.https://doi.org/10.1371/journal.
pone.0177288 andadulthoodantisocialbehavioroftheparentsonoffspringantisocialbehaviorasyoung
adults.Wealsoexaminedwhethermothers’andfathers’drinkingproblemswhenoffspring
Editor:ZhichengCarlLin,HarvardMedicalSchool,
UNITEDSTATES wereyoungchildren(6–8years)affectedoffspringantisocialbehaviorasyoungadults
(18–21years).Weevaluated655childrenfrom339familiesintheMichiganLongitudinal
Received:July14,2016
Study(MLS),aprospectivestudyofAUDandnon-AUDfamilies.Pathmodelswerecon-
Accepted:April25,2017
structedinordertotestfortheparentalcontributionstooffspringoutcomes.Wefoundthat
Published:May15,2017
bothmothers’andfathers’antisocialbehaviorcontributedtothechildren’syoungadultantiso-
Copyright:©2017Lietal.Thisisanopenaccess cialbehavior.Onlymothers’drinkingproblemswhiletheirchildrenwerelittlehadasignificant
articledistributedunderthetermsoftheCreative
effectontheirsons’laterdrinking,butnotontheirdaughters’.Thesedifferentparentaleffects
CommonsAttributionLicense,whichpermits
suggestthatmaternalandpaternalinfluencesmaybemediatedbydifferentmechanisms.
unrestricteduse,distribution,andreproductionin
anymedium,providedtheoriginalauthorand
sourcearecredited.
DataAvailabilityStatement:Theanonymousdata
usedinthisstudyareavailableattheopenICPSR
website(http://doi.org/10.3886/E100484V1).
Introduction
Funding:Thisworkwassupportedinpartby
grantsfromtheNationalInstituteonAlcoholAbuse Asthemostcommonsubstanceofabuseintheworld,alcoholcontributesnotonlytoalcohol
andAlcoholism(R37AA07065toRAZ,R01AA usedisorder(AUD)butalsotoahostofrelatedproblemssuchasviolence,physicalabuse,traf-
07065toRAZandMMH,andbyanMCubedgrant
ficaccidents,fetalalcoholsyndromeandothernegativeoutcomesaswellasmedicalcondi-
toJBB,MLM,BGR,MMH,andRAZfundedbya
tionsandprematuremortality.Problemdrinkingisalsorecognizedasonetypeofimpulsive
parentgrantfromtheSloanFoundationtoCarl
behavior.AccordingtotheNationalLongitudinalAlcoholEpidemiologicSurveyin2014,
Lagoze.JBBissupportedinpartbyagrantfrom
theNationalInstituteonDrugAbuse approximately16.3million(6.8%)ofU.S.adultswereclassifiedwithalifetimediagnosisof
PLOSONE|https://doi.org/10.1371/journal.pone.0177288 May15,2017 1/16
Genderdifferencesintransmissionofantisocialbehaviorproblems
R01DA039952.Thefundershadnoroleinstudy DSM-IValcoholabuseordependence,including10.6millionmenand5.7millionwomen[1].
design,datacollectionandanalysis,decisionto Inaddition,nearly43%ofUSchildrenweremembersofhouseholdswithatleastoneadult
publish,orpreparationofthemanuscript.
whohadabusedorwasdependentonalcohol.Amongthesechildren,51.1%weremale.
Competinginterests:Theauthorshavedeclared Childrenofalcoholics(COA)havebeenfoundtohaveheightenedriskforantisocial,aggres-
thatnocompetinginterestsexist. sive,andimpulsivebehavior[2].Anumberofstudieshaveinvestigatedthecausesofantisocial
behavior(ASB)inbothmalesandfemales,andbothgeneticandenvironmentalinfluenceshave
beendescribed[3,4].Priortwinstudieshavesuggestedthatgeneticandenvironmentalfactors
thatcontributetotheASBofadultsarethesameformalesandfemales[5,6].Ontheother
hand,geneticinfluencesmaycausegreatergenderdifferencesinASBduringadolescencewhen
girlsgothroughpubertyearlierthanboys[7].Hicksetalfoundthattherewasanincreasing
geneticvariationandheritabilityofASBformenastheygrowolder,butadecreasingheritabil-
ityforwomenwiththeincreaseofage[8].Similarly,alcoholconsumptionfromearlyadoles-
cencetoyoungadulthoodappearstobeinfluencedbygeneticfactorsandshared
environmentalfactors,andtheenvironmentaleffectisgender-specific[3,9].Priorstudieshave
notevaluatedtheroleofthegenderofparentaswellasthechildinshapingtheseeffects.
Thegenderofachildplaysaroleintheriskfordevelopingalcoholusedisorder(AUD)and
othernegativeconsequencesfacedbyCOAs.Weshouldnotethatweusetheterm‘gender’
throughoutthisarticletorefertothecombinedeffectofbiologicalandsocioculturalfactors
thatcontributetodifferencesbetweenmalesandfemales.WhilebothmaleandfemaleCOAs
aremorelikelytodevelopAUDthanchildrenwithnon-AUDparents,theriskisevenhigher
formaleCOAs[10].Inaddition,maleCOAswithantisocialparentsaremoresusceptibleto
intellectual,cognitive,andacademicdeficitsthannon-COApeers[11].Atyoungages,COAs
alsohavemoreexternalizingbehaviorssuchasaggressionandviolence,aswellasinternalizing
behaviorsuchasdepressionandanxiety,asreportedbytheirparents[12].Boysshowmore
behaviorproblemsthangirlsinbothdomains,andolderchildrenhavemoreinternalizing
problemsthanyoungerchildren[10].However,thereishugevariabilityinthedevelopmentof
problemsinCOAs,whichindicatestherearemultipleriskfactorsinvolved.
Asshownbystudyofmonozygotic(MZ)anddizygotic(DZ)twins,addictionsaremoder-
atelytohighlyheritable,withaheritabilityof50%forAUDand60–70%incocaineandopiate
addiction[13].Thefamilialtransmissionofalcoholanddrugdependenceimpliesthatgenetic
factorscouldaffectindividualriskforalcoholism[14].Forexample,theGABAreceptorgene
GABRA2hasbeenassociatedwithadultalcoholdependenceaswellaswithexternalizing
behaviorssuchasimpulsiveness[15],likelyduetoaninfluenceonincentivemotivationneuro-
circuitryinadolescence[16].
Inadditiontogeneticfactors,environmentalinfluencesonCOAdevelopmentarealso
importantandcomplex.TheadultproblemsofCOAscan,atleastinpart,betracedbackto
theirexperiencesininfancyandearlychildhood.Afamily’slowsocioeconomicstatus(SES),
andhighfamilypsychopathology(e.g.,lowcohesion,highconflict,andpoorproblem-solving
skills)canincreasetheCOA’sriskofbehaviordisordersaswellasofAUD[17].Neighborhood
residentialinstabilityinchildhoodandotherenvironmentalchangesfromearlychildhoodto
adolescencealsocontributetothedevelopmentoflateadolescentAUD[18].Ontheother
hand,COAswithmoresourcesofsupportintheirchildhoodandyouthcopemoreeffectively
withthetraumaofgrowingupinanAUDfamily,whichindicatestheprotectiveeffectofcare-
givingfromrelativesandcommunity[19,20].Identifyingenvironmentalfactorsthatmoderate
thegeneticeffectsonthedevelopmentofCOAsisthereforeofgreatimportance.
Importantly,ithasbeendemonstratedthatethanolcancauseepigeneticeffects(thatis,
changesinhowgenesareexpressedwithoutchangingtheunderlyingDNA).Specifically,site
selectiveacetylation,methylation,andphosphorylationofhistonesduetoalcoholconsump-
tionaffecttheexpressionofgenesandcanbetransmittedacrossgenerations[21].Arecent
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Genderdifferencesintransmissionofantisocialbehaviorproblems
animalstudyshowedthatthePomcgene,whichcontrolsneuroendocrine-immunefunctions,
canbeimprintedbyfetalalcoholexposureandhypermethylatedthroughthreegenerations.
Additionally,thealcoholepigeneticmarksonthePomcgenearemaintainedonlyinthe
males,whichindicatesagenderdifferenceinepigenetictransmission[22].
Parents’AUDmaycontributesubstantiallytothebehavioroftheirchildrenthroughaseries
ofcomplexbiological,psychological,andsocialmechanisms,andeachofthesemechanismsis
likelytohaveaneffectongenderdifferences,althoughsuchdifferenceshavenotbeenwell
studied.TheeffectsofparentalAUDonchildrenmaybedirect,asconveyedbygeneticorepi-
geneticinfluence,andalsoindirect,bywayofthenegativebehaviorstheyshowtowardstheir
children,includinglessattentionyetmorephysicalpunishmentandabuse.Anassociationhas
beenreportedamongCOAsbetweenexperiencingmaltreatmentandcumulativestressful
eventsinearlylife,andtheearlyonsetofbothproblemdrinkinginadolescenceaswellasalco-
holanddrugdependenceinearlyadulthood.Theseoutcomescouldbetheresultofgene
expressionchangesinthemesolimbicdopaminerewardpathway,andthuswouldbeepige-
netic[23].TheAUDofoneparentmayalsoaffecthis/herrelationshipwiththespouse,whose
behavioralsoinfluencesthechildren.Forexample,thedrinkingproblemsofthefathermay
contributetotheexternalizing/internalizingbehaviorsofthewife[24],whichisamediation
effectonthebehaviorofchildren.Oneparent’sAUDmayalsomoderatetheinfluenceofthe
spouseonthechildren.Thecohesionandconflictinafamilythusmayinfluencethestrength
oftherelationshipbetweenparentsandchildrenandrelatetotheirantisocialanddelinquent
behaviors[25];infact,COAswerefoundtobemoreemotionallyreactivetomaritalconflict
thannon-COAs[26].However,theroleofgenderislessclearontheseadditiveeffects.
CurrentresearchtendstomainlyfocusonthebehaviorofboysinfamilieswithAUD,espe-
ciallyfatherswithAUD,sinceAUDinmalesismoreprevalent.However,theproblemof
addictionanddruguseinwomenisincreasingandmaternalinfluencesonchildrenarealso
important[27].Comparedwithpaternalvariables,maternalvariableswereevenstrongerpre-
dictorsofthree-year-oldsons’problembehaviors[27].Thedevelopmentofgirlsisofequal
importancetoboys;however,theirdifferentperformanceinresponsetopaternalandmaternal
influencehasbeenlessfrequentlystudied.
IntheanalysespresentedhereweexaminedthepredictionthattheASBofparents,during
theirchildhoodandastheparentsofyoungchildrenwouldhavelong-termeffectsontheASB
oftheirchildrenasyoungadults.Weincludedinourmodelproblemdrinkingbehaviorfor
thefatherandthemotherthatwaspresentwhenthechildrenwere6–8yearsold.Weinvesti-
gatedgenderdifferencesinhowboysandgirlsrespondedtoparentalbehavior.Wehypothe-
sizedthatthefathers’problemdrinkingbehaviorwouldhavegreatereffectonthechildren’s
ASBasyoungadultsthantheproblemdrinkingbehaviorofmothers.Wealsopredictedthat
theASBofthefatherwouldhaveagreatereffectonboysthanongirls.Finally,sincefamily
cohesioncandifferentiallymediatetheeffectsofparentaldrinkingandASBonboysandgirls,
weincludedparentalperceptionoffamilycohesiononboys’andgirls’ASBinthismodel.
Wereportherethatbothmothers’andfathers’ASBhadeffectonchildren’sASBasyoung
adults.Comparedtofathers,themothers’drinkingbehaviorearlyduringachild’slifewasa
strongerpredictorofboys’ASBbutnotofgirls.
Methods
Sampleandprocedures
ThisstudyispartoftheongoingMichiganLongitudinalStudy(MLS)offamilieswithorwith-
outAUD,whichstartedinthe1980’s[28,29].AUDfamilieswerecategorizedassuchviathe
drinkingbehavioroftheadultmeninthefamily;allmenwithdrunk-drivingconvictionsina
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Genderdifferencesintransmissionofantisocialbehaviorproblems
four-countyareawithabloodalcoholconcentrationofatleast.15%(iffirstconviction)orat
least.12%(ifapreviousdrinking-relatedlegalproblemhadoccurred)werepotentialcandi-
datesforstudyenrollment.Theyalsoneededtomeetdiagnosisforprobable/definiteAUD.
TheoriginalrecruitmentoffathersusedFeighnercriteria[30]todiagnoseAUD,andpartici-
pantswerelaterrediagnosedusingDSM-IValcohol-usedisordercriteriaasthestudypro-
gressed,datawerecollectedpriortoDSM-Vcriteriaavailability[29,31].Subjectswere
requiredtohaveatleastone3-to5-year-oldbiologicalsonandtobelivingwiththechildand
hisbiologicalmotheratthetimeofrecruitment.TheAUDstatusofthemotherswasfreeto
vary.Femalesiblingsjoinedtheprojectseveralyearslater(whenthetargetedboyswereatages
6–11yearsold)whenfundingbecameavailabletoincludegirls.Acontrast/controlgroupof
non-AUDfamilies(neitherparentwithahistoryofsubstanceuse)wasrecruitedthrough
door-to-doorcanvassinginthesameneighborhoodsastheAUDfamilies.Duringthecanvass-
ing,anintermediate-riskgroup(AUDfathersbutwithoutahistoryofalcohol-relatedlegalor
drunk-drivingproblemsoccurringduringthelifeoftheirchild)wasnoticedandrecruitedat
thesametime.Ofallthe471recruitedfamilies,45%areAUDfamilieswithdrunk-driving
fathers(courtAUDfamilies),21%areAUDfamiliesfromthesameneighborhoods(commu-
nityAUDfamilies),and34%arenon-AUDfamilies(controlfamilies).Thisresearchwas
approvedbytheUniversityofMichiganMedicalSchoolInstitutionalReviewBoard(IRB).
Childrenunder9yearsoldprovidedverbalconsent(andwrittenconsentlaterastheygrew
older),andtheirparentsprovidedwrittenconsentwithassignedconsentforms.Thedatafor
thisstudywereanalyzedanonymously.
Familiesreceivedextensiveassessmentsatbaseline(Time1withmaletargetchildatage3
to5)andevery3yearsthereafter(e.g.,Time2withmaletargetchildatage6to8).Ateach
wave,datawerecollectedfromallfamilymembersbyinterviews,self-reportquestionnaires,
reportsbycollateralInformantssuchasspouses,parents,andteachers,aswellaschildren’s
reportsoftheirexperienceswiththeirparents[31].
InthepresentstudyweincludedallchildrenwhohadcompletedTime6(whentheywere
earlyemergingadultsat18-to20-yearsofage);thispoolincluded655childrenfrom339fami-
lies.AmongthechildrenwhowereoldenoughforTime6assessmentwhenthepresentstudy
wasconducted(about80%ofthetotalchildrenintheMLS),theretentionrateofchildren
fromTime1wasapproximately95%.Thesampleconsistedof47%courtAUDfamilies,21%
communityAUDfamiliesand32%non-AUDfamilies.Thepercentageoffamiliesineachof
thecategorieswasconsistentovertheyearsindicatingnobiasinattrition.AtTime6,themean
ageoffatherswas48yearsoldandmotherswas46yearsold.Ouranalyticalmodelexamines
therelationshipofparents’ASBatT1withtheadulthoodASBoftheiroffspring.Italsoexam-
inestheeffectsofotherfactors,suchasparents’drinkingproblems,parents’socialsupport,
andfamilycohesionandconflictatT1andT2ontheASBofoffspringasyoungadults.The
purposeofthisapproachwastodeterminewhethertherearepotentiallongtermeffectsof
parentalbehaviorontheadultbehavioroftheiroffspring.
Measures
Antisocialbehavior. TheAntisocialBehaviorChecklisthas45itemsthataskaboutfre-
quencyofaggressiveandantisocialactivitiesinchildhoodandadulthood[32,33].Thescores
foreachitemrangefrom0to3(0=never,1=rarely,2=sometimes,3=often),withhigher
scoresindicatingahigherfrequencyofthebehavior.ThisinstrumentalsodifferentiatesAUD
fromnon-AUDadults,withhigherASBscoresamongtheAUDcomparedtothenon-AUD
males[34].Inthisstudy,theantisocialindicesinchildhoodandadulthoodofparentsatTime
1wereusedtopredictthetotalantisocialscoresofchildrenatTime6.
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Genderdifferencesintransmissionofantisocialbehaviorproblems
Socialsupport. TheNorbeckSocialSupportQuestionnaire,usinganinterviewformat,
evaluatestheaffect,affirmationandaidcomponentsofsupportivetransactions[35].Themea-
suredescribestheindividual’sstructuralsupportnetworkwithsignificantpeopleinhisorher
lifefromseveralperspectives.SocialsupportisevaluatedbyLengthofTimeKnown,Feeling
Alikewiththeother,Acceptance,Trust,MonetarySupport,EmotionalSupport,SicknessSup-
port,CrisisSupport,Love,andDesiretoImitate,withascaleof1to5(“notatall”to“agreat
deal”).Thetotalsocialsupportscoreforparents(calculatedastheproductoftotalnumberof
personsinone’ssupportnetworkandaveragelevelfromallsources)atTime1wasusedfor
analysis.
Drinkinganddrughistory[36]. Thisquestionnaireincorporatesitemsfromthe1978
NationalInstituteonDrugAbuseSurvey[37],fromtheAmericanDrinkingPracticesSurvey
[38]andfromtheV.A.MedicalCenter(UniversityofCalifornia,SanDiego)ResearchQues-
tionnaireforAlcoholics[39].Alloftheitemshavebeenextensivelyusedinavarietyofsurvey
andclinicalsettings.Theyprovidedataonquantity,frequencyandvariabilityofalcoholand
druguse,andtroublesrelatedtotheuseofthesesubstances.Thetotalnumberofdrinking
problemsforparentsatTime2wasusedtodescribetheiralcoholabuse.
Familyconflictandcohesion. TheFamilyEnvironmentScaledescribesdimensionsof
thefamilyclimatewithwhicheachfamilymembermustcope[40].Theinstrumentprovides
scoresinareasthathavepreviouslybeensignificantlyimplicatedinAUDanddrugabusing
families:e.g.,Cohesion,Conflict,Moral-ReligiousEmphasis,andAchievementOrientation.
TheFamilyEnvironmentScaleprovidesinsightsintotheperceptionsofdifferentfamilymem-
bers.TheCohesionsubscaleassessestheextentofcommitment,concern,andsupportpro-
videdbyfamilymemberstooneanother.TheConflictsubscaleassessestheextentofopen
aggression,anger,andconflictedinteractionsamongfamilymembers.Thesetwoscales
reportedbyparentsatTime1wereusedtoevaluatethefamilyclimate.
Analyticapproach
The655childrenwerematchedwiththeirparents’variableswhentheywereatTime1(3–5
yearsold)andTime2(6–8yearsold).Theoutcome,theASBofthechildrenatTime6,isa
completevariable,buttherearesomemissingdataineachofthe12parentvariablesforthe
339parentalpairs.Overall,therewere6.9%missingdataamongallvariablevalues.We
assumedthedataaremissingatrandom(MAR),whichisappropriatebecausethevariablesfor
parentstendtobeassociatedandothervariablesinthedatasetcanbeusedtopredictmissing-
nessforagivenvariable.Weadoptedamultipleimputationapproachtoimpute10setsof
completedatabyMarkovChainMonteCarlowithmultiplechainsusingSASPROCMI.This
procedureisdesignedforcontinuousvariableswithcontinuouscovariatesforarbitrarymiss-
ingdata[41].ThenSASPROCMIANALYZEwasusedtoaggregatethe10setsofmediation
andmoderationmodelstogetestimatedparametersandtheirvariances.
Tostudythedifferenteffectsoffathersandmothersonboysandgirls,weusedamedia-
tion-moderationmodeltoexaminetheeffectofparents’adulthoodASBontheirchildren’s
adultASB,withthemediationeffectinvolvingparents’drinkingproblems.ALinearMixed
Modelwasusedtoadjustthecorrelationbetweensiblings.Wealsotestedthemoderation
effectoffamilycohesionandconflictonparents’adulthoodASBandthemoderationeffectof
totalsocialsupportonparents’drinkingproblems.Tocomparethedifferencebetweenrisk
groups,wealsobuiltmodelsfornon-AUD(control)familiesandAUD(courtAUDandcom-
munityAUD)familiesseparately.Wetestedtheeffectofparents’childhoodASBontheirown
adulthoodASB,andontheiroffsprings’adultASB,whichinvolvesalongitudinalinfluenceof
approximatelythreedecades.
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Genderdifferencesintransmissionofantisocialbehaviorproblems
Table1. Pairedcomparisonofparentsvariables:Mean,standarddeviations(SDs),differences,andcorrelation.
Variable Parent Mean(SD) Min. Max. Differences Correlation
ChildhoodAntisocialBehavior Mother 6.43(4.78) 0 28 -3.28** 0.299**
Father 9.71(7.34) 0 42
AdulthoodAntisocialBehavioratTime1 Mother 4.58(3.43) 0 22 -3.77** 0.307**
Father 8.35(6.86) 0 56
NumberofdrinkingproblemsatTime2 Mother 0.98(2.15) 0 14.39 -2.04** 0.225**
Father 3.02(4.93) 0 24.36
TotalsocialsupportatTime1 Mother 28.17(13.09) 3.91 77.91 4.19** 0.360**
Father 23.98(12.23) 3.36 69.25
FamilycohesionatTime1 Mother 7.30(1.89) 0 9 0.07 0.361**
Father 7.37(1.62) 0 9
FamilyconflictatTime2 Mother 3.69(2.16) 0 9 0.29** 0.478**
Father 3.40(2.24) 0 9
**:Significantatthe0.01level(2-tailed)
https://doi.org/10.1371/journal.pone.0177288.t001
Results
Descriptivestatistics
Table1listsdescriptivestatisticsforthe339pairsofparents.Allofthevariablesweresignifi-
cantlypositivelycorrelatedbetweenfatherandmother(p<0.01),andthecorrelationcoeffi-
cientsrangedfrom0.225to0.478.Bypairedcomparison,fathershadsignificantlyhigher
childhoodASB,adultASB,andnumberofdrinkingproblemsthanmothers,whilemothers
hadsignificantlymoresocialsupportthanfathers(p<0.01).Regardingtheevaluationoffamily
climate,fathersandmothershadsimilaropinionsaboutfamilycohesion,butmothers
reportedsignificantlymorefamilyconflictthanfathers(p<0.01).S1andS2Tablesliststhe
descriptivestatisticsforAUDfamiliesandnon-AUDfamiliesrespectively.ThechildhoodASB
andadultASBaswellasnumberofdrinkingproblemsforbothparentswerehigherinAUD
familiescomparedwithnon-AUDfamilies(S3Table).Thedifferencesbetweenfathersand
motherswerealsolargerinAUDfamilies.ThecorrelationsweresimilarinAUDandnon-
AUDfamilies.
Ofthe655childrenfrom339families,199weregirlsand456wereboys.AtTime6,they
wereataverageage19.6±2.0yearsold;themeanASBforgirlswas4.04,whichwassignifi-
cantlylowerthanboys(7.15),asshowninTable2.Inbothnon-AUDandAUDfamilies,on
averageboyshadsignificanthigherASBthangirls(2.42higherinnon-AUDfamiliesand3.52
higherinAUDfamilies).ThemeanASBforgirlsinAUDfamilieswas2.27higherthangirlsin
Table2. Descriptivestatisticsofchildren’santisocialbehavioratTime6.
FamilyType Children N Mean(SD) Min. Max. Differences
AUDfamilies Girls 136 4.76(4.85) 0 25 -3.52**
Boys 303 8.28(8.60) 0 77
Non-AUDfamilies Girls 63 2.49(2.58) 0 11 -2.42**
Boys 153 4.91(4.55) 0 27
Combined Girls 199 4.04(4.39) 0 25 -3.11**
Boys 456 7.15(7.65) 0 77
**:Significantatthe0.01level(2-tailed)
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Table3. Correlationbetweenmothers’variables.
Correlations: 1 2 3 4 5 6
1.ChildhoodAntisocialBehavior 1.00
2.AdulthoodAntisocialBehavioratTime1 0.55** 1.00
3.NumberofdrinkingproblemsatTime2 0.34** 0.31** 1.00
4.TotalsocialsupportatTime1 -0.07 -0.09 -0.04 1.00
5.FamilycohesionatTime1 -0.23** -0.26** -0.17** 0.17** 1.00
6.FamilyconflictatTime2 0.17** 0.24** 0.19** -0.03 -0.47** 1.00
**:Significantatthe0.01level(2-tailed)
https://doi.org/10.1371/journal.pone.0177288.t003
non-AUDfamilies(p<0.001),andthemeanASBforboysinAUDfamilieswas3.37higher
thanboysinnon-AUDfamilies(p<0.001).
Tables3and4displaythepotentialcorrelationsbetweenallvariablesformotherandfather
separately.Allmothers’variablesweresignificantlycorrelatedwitheachotherexceptfortotal
socialsupport,whichwasonlysignificantlypositivelycorrelatedwithfamilycohesion.The
majorityofthefathers’variablesweresignificantlycorrelatedwitheachotherexceptfortotal
socialsupport,whichwasnotsignificantlycorrelatedwithadulthoodASB,numberofdrinking
problemsorfamilyconflict.Ingeneral,themajorityofthevariableswerepositivelycorrelated
witheachother,whiletotalsocialsupportandfamilycohesionwerenegativelycorrelatedwith
othervariables.Wealsoexaminedthecorrelationsbetweenchildren’sASBandparents’child-
hoodASBandadulthoodASB,andfoundsignificantpositivecorrelationsamongthesevari-
ablesbetweenfathersandbothboysandgirls,andalsobetweenmothersandbothboysand
girls(p<0.05,showninS3Table).
Mediation&moderationanalysis
AsshowninFig1,amodelofthemediation-moderationeffectofparents’ASBanddrinking
problemsonchildren’sASBwasbuiltformothers’andfathers’effectonboysandgirls.The
standardizedparameterestimateisshownoneachpath,whichreflectsthemagnitudeofthe
effect.Thesignificanteffectsareshowninsolidlines.Mothers’adultASBhadsignificanteffect
onthechildren’sASB(0.146forboys,0.156forgirls),whiletheeffectofmothers’drinking
problemswassignificantonlyonboys(0.155).Theeffectoffathers’adultASBwassignificant
onbothboys’andgirls’ASB(0.134forboysand0.164forgirls),withnodirectsignificant
effectofthefathers’drinkingproblems.Fortheeffectoffamilycohesionandconflicton
Table4. Correlationbetweenfathers’variables.
Correlations: 1 2 3 4 5 6
1.ChildhoodAntisocialBehavior 1.00
2.AdulthoodAntisocialBehavioratTime1 0.72** 1.00
3.NumberofdrinkingproblemsatTime2 0.25** 0.42** 1.00
4.TotalsocialsupportatTime1 -0.14* -0.11 -0.05 1.00
5.FamilycohesionatTime1 -0.18** -0.25** -0.20** 0.13* 1.00
6.FamilyconflictatTime2 0.24** 0.27** 0.15* -0.04 -0.43** 1.00
*:Significantatthe0.05level(2-tailed);
**:Significantatthe0.01level(2-tailed)
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Fig1.Modeldisplayingmediation-moderationeffectofparents’antisocialbehaviorsanddrinkingproblemson
children’santisocialbehaviors,theeffectdiffersbyfatherandmotheronboysandgirls.Thepathswhere
standardizedparameterestimatesaresignificantatthe0.05levelareinsolidlines.
https://doi.org/10.1371/journal.pone.0177288.g001
children,onlyfathers’reportoffamilycohesionhadsignificantnegativeeffectontheoffspring,
anditwasonlyonboys(-0.095).
Forbothmotherandfather,theeffectofchildhoodASBonadultASBatTime1wassignifi-
cant,butfathers’childhoodASBhadastrongerinfluenceonadultASBcomparedwithmoth-
ers’(p<0.05)(Fig1).Themoderationeffectoffamilycohesionandconflictontheeffectof
childhoodASBonadultASBwasnotsignificantandthusnotincludedinthemodel.Mothers’
childhoodASBandadulthoodASBatT1aswellasfathers’drinkingproblemsatT2hadan
effectonmothers’drinkingproblemsatT2.Butfathers’childhoodASBhadnodirecteffecton
fathers’drinkingproblemsatT2.Wecanalsoseethatfathers’ASBatT1hadadominanteffect
onfathers’drinkingproblemsatT2(comparedwiththeeffectofmothers’drinkingproblems,
p<0.05).ThemoderationeffectoftotalsocialsupportontheeffectofadultASBondrinking
problemswasnotsignificantandthusexcludedfromthemodel.
Theseresultsprovidedmixedsupportforourhypotheses.Wefoundfathers’andmothers’
ASBbothhadaneffectonboysandgirls.Contrarytoourhypothesis,onlythemothers’drink-
ingproblemshadsignificanteffectonboys,butfathers’didnot,andneitherparents’drinking
hadaneffectongirls.Thefathers’perceptionoffamilycohesionmediatedtheeffectonboys’
ASB.
Fig2showsthemodelsofmediation-moderationeffectofparents’ASBanddrinkingprob-
lemsonchildren’sASBfordifferentsubjectgroups.Forthe216childrenfromcontrolfamilies,
mothers’adultASBanddrinkingproblemsaswellasfathers’adultASBhadsignificanteffect
onboys,andonlyfathers’adultASBwassignificantongirls.Forthe428childrenfromcourt
AUDandcommunityAUDfamilies,mothers’adultASBanddrinkingproblemsaswellas
fathers’reportoffamilycohesionhadsignificanteffectonboys,whileongirls,nothingwassig-
nificant.Incontrolfamilies,theeffectofmothers’adultASBonboyswasnegative(-0.125)and
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Genderdifferencesintransmissionofantisocialbehaviorproblems
Fig2.Modeldisplayingmediation-moderationeffectofparents’antisocialbehaviorsanddrinkingproblemsonchildren’s
antisocialbehaviorsforeachriskgroup:(a)controlgroup,(b)courtAUDandcommunityAUDgroup.Thepathswhere
standardizedparameterestimatesaresignificantatthe0.1levelareinsolidlines.
https://doi.org/10.1371/journal.pone.0177288.g002
theeffectofmothers’drinkingproblemswasdominant.IncourtAUDandcommunityAUD
families,theeffectofmothers’adultASBwaspositiveanddominantcomparedwithmothers’
drinkingproblems.Thusthemechanismsofhowparents’ASBanddrinkingproblemsaffected
childrenweredifferentinAUDandnon-AUDfamilies.
Discussion
OurfindingsdemonstrateadifferencebetweenmaternalandpaternalinfluencesontheASB
problemsoftheiroffspringduringthelifestageknownas“earlyadulthood.”Mothers’ASB
hadaneffectonboys’ASBandthiseffectwasmediatedbymothers’drinkingproblems.For
girls,theinfluencewasfrommothers’adultASBonly.Fathers’ASBhadaneffectonboth
boys’andgirls’ASB,buttherewasnosignificanteffectoffathers’drinkingproblemsonboys
orgirls.
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Genderdifferencesintransmissionofantisocialbehaviorproblems
Comparingtheeffectsofparents’behaviorsraisesimportantquestionsaboutthesocial
rolesofmothersandfathers,aswellassexandgenderdifferencesinthedevelopmentand
manifestationofAUDandASB.Ourfindingsareconsistentwithpreviousresearchdemon-
stratingtheimportanceofpaternalinfluenceonchildren’sdevelopment[42],evenwhen
fathers’ASBtendednottohappenathomeandovertviolencetowardchildrenwaslow.A
studyof5year-oldtwinsshowedthatforchildrenwithfatherswhohaveahighlevelofAUD,
themoretimetheylivedwiththeirfather,themoreconductproblemstheyhad,suggesting
thatchildrenwhoresidedwithantisocialfathersreceiveda“doublewhammy”ofgeneticand
environmentalriskforbehaviorproblems[43].Duetothehighcorrelationbetweenfathers’
ASBduringtheirchildhoodandadulthood,wecan’tdistinguishtheirinfluenceindividually,
buttogethertheireffectcan’tbeignored.
Althoughitwasthefathers’drinkingbehavioratT1thatwasthereasonforrecruitment,we
didobservemotherswithproblemdrinkingbehavior.Inourstudy,41%ofthecourtAUD
fathersand46%ofthecommunityAUDfathersweremarriedwithAUDmothers,andthere
wasamoderatecorrelation(0.2–0.3;valuesseeTable1)betweenmaternalandpaternaldrink-
ingproblemsandASB,whichweinterpretasaformofassortativemating.Empiricalstudies
haverevealedthatAUDmalestendedtofindspouseswhowerethedaughtersofAUDfathers
whileAUDfemalesmayhavebothAUDfathersandhusbands,andbothmenandwomen
withASBwerelikelytojoinanASBmate[44].Thesepairingscanleadtodomesticviolencein
thehome,asconfirmedbytheextremelyhighdivorcerateoftheAUDandASBfamiliesinthe
MLS[31],andrepresentriskforthenextgeneration[45].
WhilemenandwomenmightbothdemonstrateASBanddrinkingproblemsinthesefami-
lies,ourstudyshowsthatmothers’drinkingbehaviorcanbringdifferentconsequencesfor
childrenespeciallyforboys,ascomparedtofathers’drinking.Eventhoughpaternaldrinking
problemsweremoreseriousinthemajorityoffamilies,maternaldrinkingproblemswere
moreinfluentialontheirchildren’sdevelopment,possiblybecausemothersareusuallythepri-
marycaregivers.IntheMLS,itwasrevealedthatmaternaldrinkingduringboys’middle
childhoodpredictedthenumberoftheirdrinkingdaysinmiddleadolescence[46].Another
studyonyoungadultoffspringofAUDparentsrevealedthatCOAswithmotherswithdrink-
ingproblemsreportedmorenegativechildhoodexperiences,whichcouldberelatedtothefact
thatmotherswithdrinkingproblemsweremorelikelytodrinkregularlyathome[47].
ResearchhasalsofoundthatchildrenofAUDmothershavemoresocialrelationshipprob-
lemssuchasdistantrelationshipswithsiblingsandfriends,negativeinteractionwithclass-
mates,andisolationwithintheirneighborhood,allofwhichcouldbesecondarystressorsand
furtherdamagechildren’smentalhealth[48].Inotherstudies,ithasbeenshownthatteenagers
whoreportlessconformityandbenevolence,butmoreindependence,aremorelikelyto
developASBinbothmalesandfemales[49].Furthermore,interpersonalrelationshipscan
positivelyornegativelyaffectASBduringadolescence[49].Thesefindingshighlightthateven
thoughthepresentstudyfocusesonthelongtermeffectsofparentalbehaviorpriortoand
duringearlychildhoodonASBinyoungadults,thesocialstructuresinwhichachildlivesand
personalityfactorsalsoaffectASB.
Theanalysisofthegenderoftheoffspringindicatesimportantdifferencesinthetransmis-
sionandmodelingofASBforboysandgirls.InAUDfamilies,theeffectofparentalinfluence
wasmuchstrongeronmaleoffspringthanonfemaleoffspring.Thesefindingssuggestthat
withrespecttopaternalandmaternalASB,boyshaveahigherheritabilitythangirls,which
couldresultinmoreASBinboysthangirls,asweobserved.Whilethisgenderdifferenceissig-
nificant,itisimportanttonotethatwefoundinapreviousstudythatevenatveryearlyages,
maleandfemaleCOAswereheterogeneouspopulationsthatweredistinguishablebyfamilial
subtypes,inparticular,betweenantisocialAUDandnon-antisocialAUDindividuals[10].
PLOSONE|https://doi.org/10.1371/journal.pone.0177288 May15,2017 10/16