Autistic features in school age children: IQ and gender effects in a population-based cohort

Autistic features in school age children: IQ and gender effects in a population-based cohort

Hilde K. Ryland

^a,b,

*, Mari Hysing

^b

, Maj-Britt Posserud

^b,c

, Christopher Gillberg

^e

, Astri J. Lundervold

^a,b,d

aDepartmentofBiologicalandMedicalPsychology,UniversityofBergen,Postbox7807,N-5020Bergen,Norway

bRegionalCentreforChildandYouthMentalHealthandChildWelfare,UniHealth,UniResearch,Postbox7800,N-5020Bergen,Norway

cDepartmentofChildandAdolescentPsychiatry,HaukelandUniversityHospital,N-5021Bergen,Norway

dK.G.JebsenCentreforResearchonNeuropsychiatricDisorders,UniversityofBergen,JonasLiesVei91,N-5009Bergen,Norway

eGillbergNeuropsychiatryCentre,DepartmentofNeuroscienceandPhysiology,UniversityofGothenburg,Kungsgatan12,SE-41119 Gothenburg,Sweden

1. Introduction

Intelligenceandmentalhealtharecloselyinterrelated.Atestedintelligencequotient(IQ)below85isknowntoincrease theriskofmentalhealthproblems(Dekker&Koot,2003;Dekker,Koot,vanderEnde,&Verhulst,2002),whereashigherIQ mayservetoprotectagainstthedevelopmentofmentalhealthproblemsinchildren(Ryland,Lundervold,Elgen,&Hysing, 2010). Autism spectrum disorder (ASD) is a neurodevelopmental disorder that may occur at all IQ-levels (American PsychiatricAssociation,2013).WithinthediagnosticcategoryofASD,thereisahighmale:femaleratio(Fombonne,1999, 2003).Interestingly,genderhasbeenrelatedtoIQinindividualswithASD,inthatthemale:femaleratiohasbeenreportedto belargestinindividualswithanIQ-levelwithinthenormal range(Gillberg, Cederlund,Lamberg,&Zeijlon,2006)and approaching1:1inseverelyintellectuallydisabledsubgroups(Wing,1981).Thisillustratesthecomplexityofassociations betweenIQ,genderandsymptomloadinneurodevelopmentaldisorders.

ARTICLE INFO

Articlehistory:

Received9August2013

Receivedinrevisedform30November2013 Accepted5December2013

Keywords:

Autisticfeatures IQ

ASSQ Children Gender

ABSTRACT

Levelandcharacteristicsofintellectualfunction(IQ)havebeenassociatedwithsymptom presentationinchildrenwithautismspectrumdisorder.Thepresentstudyexamined associationsbetweenIQandautisticfeaturesinasampleofschoolagedboysandgirls selectedfromapopulation-basedcohort.Thestudyincludeddetailedexaminationsof325 childrenaged8–12years,selectedfromthesampleoftheBergenChildStudy.IQwas assessedusingthethirdversionoftheWechslerIntelligenceScaleforChildren(WISC-III) andautisticfeaturesbyparentreportsontheAutismSpectrumScreeningQuestionnaire (ASSQ).BoysobtainedhigherASSQscoresthangirls.GenderandFSIQhadmaineffectson ASSQscores,withtheASSQscoresshowingagradualdeclinewithhigherFSIQforboth genders.DiscrepanciesbetweenverbalandperformanceIQwererelativelyunrelatedto ASSQscores.Thefindingsemphasizetheimportanceofconductingcarefulassessmentsof childrenbeforereachingconclusionsaboutcognitivefunctionandautisticfeatures.

ß2013TheAuthors.PublishedbyElsevierLtd.

*Correspondingauthorat:DepartmentofBiologicalandMedicalPsychology,UniversityofBergen,Postbox7807,N-5020Bergen,Norway.

Tel.:+4799792312.

E-mailaddresses:hilde.ryland@uni.no(H.K.Ryland),mari.hysing@psybp.uib.no(M.Hysing),maj-britt.posserud@uni.no(M.-B.Posserud), christopher.gillberg@gnc.gu.se(C.Gillberg),astri.lundervold@psybp.uib.no(A.J.Lundervold).

ContentslistsavailableatScienceDirect

Research in Autism Spectrum Disorders

J our na l ho me pa ge : ht t p: / / e e s. e l s e v i e r. c om/ R A S D / de f a ul t . a sp

1750-9467ß2013TheAuthors.PublishedbyElsevierLtd.

http://dx.doi.org/10.1016/j.rasd.2013.12.001

Open access under CC BY license.

Open access under CC BY license.

DiscrepanciesbetweenverbalandnonverbalIQarefrequentlyfoundinchildren(Kaufman&Lichtenberger,2000)and havebeenrelatedtoautisticfeatures.InastudyofchildrenandadultswithKlinefeltersyndrome(vanRijn&Swaab,2011), thosewithdiscrepantlyhigherperformanceIQ(PIQ)(asmeasuredbytheWISC-III(Wechsler,1991)orWAIS-III(Wechsler, 1997)) had higher levels of autistic traits – as measured with the Autism Spectrum Quotient (AQ) (Baron-Cohen, Wheelwright,Skinner,Martin,&Clubley,2001)–thanindividualswithdiscrepantlyhigherverbalIQ(VIQ).Discrepantly higher non-verbal abilities (as measured by the Differential Ability Scale) (Elliott, 1990) was also associated with significantlygreatersocialimpairmentasassessedbytheAutismDiagnosticObservationSchedule(ADOS)(Lord,Rutter, DiLavore,&Risi,1999)inagroupof47high-functioningchildrenwithautismaged7–14years(Joseph,Tager-Flusberg,&

Lord,2002).Theseresultsare,however,inconflictwithresultsfromastudybyBlackandcolleagues(2009),showingthat bothdiscrepantlyhigherPIQandVIQ(asmeasuredbytheWISC-III,WISC-IV(Wechsler,2003),orWASI(Wechsler,1999)) were associatedwithhigher (i.e. more abnormal)social symptomsscores as assessedby the ADOSandthe Autism DiagnosticInterview(ADI)(LeCouteuretal.,1989)inasampleof78high-functioningchildrenwithautismaged6–17years (Black,Wallace,Sokoloff,&Kenworthy,2009).Finally,astudybyCharmanandcollaborators(2011),including156children aged10–14yearswithASD,couldnotsupportanyrelationbetweensuchadiscrepancyscoreandsymptompresentationof ASD.

Population-basedstudiesshowthatautisticfeaturesaredimensionallydistributedinthegeneralpopulationofchildren, andthatboysshowmoreautisticfeaturesthangirls(Constantino&Todd,2003;Kamioetal.,2012;Posserud,Lundervold,&

Gillberg,2006).Still,wedonotknowhowIQandgenderarerelatedtothisbroaderdistributionofautisticfeatures.Thislack ofknowledgemotivatedthepresentstudytoexamineassociationsbetweenIQandautisticfeaturesinasampleofchildren selectedfromthepopulation-basedBergenChildStudycohort(BCS,www.uib.no/bib).Autisticfeatureswereassessedby parentreportsontheNorwegiantranslationoftheAutismSpectrumScreeningQuestionnaire(ASSQ)(Ehlers&Gillberg,1993), whichhasbeenvalidated(Posserud,Lundervold,&Gillberg,2009)andfactor-analysed(Posserudetal.,2008)aspartofthe BCS.IQwasmeasuredusingtheWISC-III(Wechsler,1991).WeexaminedhowlevelandcharacteristicsofIQperformance andgenderwererelatedtoautisticfeaturesinthissampleofchildren.WehypothesizedthatfullscaleIQperformancewould benegativelyassociatedwithASSQscores,andthatgenderwouldinfluencetheassociationbetweenthetwovariables.The IQperformancewasbothanalysedatascalelevelandwhencategorizedintothreedifferentlevelsthatcommonlyareused clinically to describe the intellectual functioning of a child. Finally, we examined associations between a VIQ-PIQ discrepancyandtheASSQscores.

2. Methods 2.1. Participants

Data from the first wave of the BCS, a longitudinal population-based studyof mental health and development (www.uib.no/bib)wereused.ThefirstwaveoftheBCShadathree-phasedesign(fordetails,seeHeiervangetal.,2007), anddata includedinthe presentstudywerecollected aspartof thethirdphase (seeLundervold,Posserud, Ullebo, Sorensen,&Gillberg,2011;Posserudetal.,2013).Inthefirstscreeningphase,aquestionnaire,includingtheASSQ,the StrengthsandDifficultiesQuestionnaire(SDQ)plusanumberofotherscales/items,wassenttoparentsandteachersofall childrenattendingthesecondtofourthprimaryschoolgradesinallschools(publicandprivate)inthemunicipalitiesof Bergen(N=9430)andSund(N=222)intheautumnof2002.Parentsof7007children(74%ofallthechildreninthe populationcohort)gavetheirinformedconsenttoparticipate.Achildwasdefinedasscreenpositiveif:(1)theSDQtotal difficulties score exceeded the 90th percentile cut-off according to parents or teachers, (2) there was a severe impairment accordingtoparentsorteachersontheSDQimpactsection,or (3)the scoreononeof theotherscales includedinthequestionnaire,suchastheASSQ,exceededthe98thpercentilecut-off.Thefamiliesofchildrendefinedas screenpositivesinthefirstphaseandarandomsampleofscreennegativechildrenwereinvitedtoparticipateinthe secondphaseoftheBCS,withaparticipationrateof44%.Inthissecondphase,theparentswereinterviewedwiththe DevelopmentandWell-BeingAssessment(DAWBA)(Goodman,Ford,Richards,Gatward,&Meltzer,2000).TheDAWBA isastructuredinterviewwithopen-endedquestionsdesignedforintervieworonlineself-completion,generatingICD- 10andDSM-IVpsychiatricdiagnosesin5–17yearolds(www.dawba.com).IntheBCS,theDAWBAwasadministeredby trained interviewers and scored by two experienced and trained clinicians. When in doubt, cases were discussed betweenraters,andalldiagnoseswerefinallyreviewedanddiscussedwithProfessorR.Goodman,whohasdeveloped theinterview.AllchildrenwhoobtainedadiagnosisaccordingtotheDAWBAinthesecondphase,anequalnumberof screen positive andscreen negative children randomly sampled from the second phase, and 25children included directlyfromthefirst screeningphase,wereinvitedtoparticipatein theextensiveclinicalexamination ofthethird phase(n=421).Thefinalsampleclinicallyexamined included329children (78%ofthoseinvited).Parentshadbeen interviewed(DAWBA)regarding304childrenintheprevious(second)phase.The25childreninviteddirectlyfromthe firstscreeningphasehadachronicphysicalillnessandwereinviteddirectlyinordertoincreasethenumberofchildren with chronicillness in the sample. Table1 provides a clinical descriptionof the third phasesample. The BCS was approvedbytheRegionalCommitteeforMedicalandHealthResearchEthicsWesternNorway,andbytheNorwegian DataInspectorate.

2.2. Instruments

2.2.1. TheAutismSpectrumScreeningQuestionnaire(ASSQ)

TheASSQincludesawiderangeofsymptomspredictiveofASD,andisdesignedtobecompletedbyteachersorparents.It consistsof27itemsscoredonathree-pointscale:‘‘nottrue’’(0),‘‘somewhattrue’’(1),or‘‘certainlytrue’’(2).Possiblescores rangefrom0to54,withhigherscoresindicatinggreatersymptomload.TheASSQhasbeenshowntohavegoodscreening propertiesboth inclinical(Ehlers,Gillberg,&Wing,1999;Guoetal.,2011;Mattilaetal.,2012)and population-based samples(Mattilaetal.,2012;Posserudetal.,2009).TheBCSvalidationstudyshowedthatmorethan90%ofchildrenwho receivedanASDdiagnosisaccordingtotheDiagnosticInterviewforSocialandCommunicationDisorders(DISCO),werealso ratedabovethe98thpercentile on theASSQ byparents and/orteachers,correspondingtoa sensitivity of0.91and a specificityof0.86(Posserudet al.,2009).Previousstudies fromtheBCS haveshown thattheASSQhasgoodinternal consistency(Cronbach’salpha=0.86)(Posserudetal.,2006)andastablethree-factorstructurewithfactorslabelledSocial difficulties(11items),Motor/tics/OCD(7items),andAutisticstyle(9items)(Posserudetal.,2008).AsdescribedbyPosserud etal.(2008),theautisticstylefactorincludesitemsthatcharacterizeaverballanguageandsocial-cognitivestyleoftenseen inhigh-functioningindividualswithASD.TheEnglishversionoftheASSQisavailableinthepublicationsbyEhlersand Gillberg(1993)andEhlersetal.(1999).Inthepresentstudy,thesumscoresofparentreportsontheASSQwereusedas measuresofautisticfeatures.

2.2.2. WechslerIntelligenceScaleforChildren,3rded.(WISC-III)

TheWISC-IIIis designedtoassessintellectualabilities inchildren andadolescentsaged 6–16years.Itcontains 13 subtests,ofwhichfiveareincludedintheverbalIQ(VIQ)scoreandanotherfiveintheperformanceIQ(PIQ)score.Thefull scaleIQ(FSIQ)isacompositescorebasedontheVIQandPIQscores.TheWISC-IIIwasadministeredaccordingtothetest manualandscoredaccordingtoSwedishnorms(Sonnander,Ramund,&Smedler,1998)bywell-trainedandexperienced test-techniciansemployedataNeuropsychologicalOutpatientClinic.ThestandardscoreofFISQ(Wechsler,1991)wasused asthemeasureofintellectualfunctioninginthepresentstudy.

TheFSIQscorewasanalysedatacontinuousaswellasacategoricallevel,forwhichitwasdividedintothreelevels:FSIQ

<70,FSIQ70–84,andFSIQ85(including21childrenwithFSIQ115).AsignificantIQdiscrepancywasdefinedasa

differencebetweenVIQandPIQofatleast14IQpoints,basedontheIQdiscrepancythatreachesstatisticalsignificance (p<0.05)accordingtotheSwedishWISC-IIImanual(Sonnanderetal.,1998).

Table1

Clinicalcharacteristicsofthethirdphasesample(N=329).

n

Screenpositivephase1 194

DAWBAdiagnosisphase2 97

K-SADS-PLdiagnosisphase3 142^a

Majordepressivedisorder 2

Psychotictraits 1

Dysthymia 4

DepressivedisorderINA 2

Adjustmentdisorderwithdepressivemood 1

Mania 1

Panicdisorder 1

Separationdisorder 4

Specificphobia 47

Socialphobia 12

Generalanxietydisorder 5

Adjustmentdisorderwithanxiety 3

Obsessive–compulsivedisorder 6

Acutestressdisorder 1

Enuresis 31

Encopresis 8

AttentionDeficitHyperactivityDisorder 52

OppositionalDefiantDisorder 24

ConductDisorder 5

Tourettesyndrome 10

Chronictics 11

Transienttics 17

Alcoholabuse 1

Otherpsychiatricdisorder 10

DISCOautismspectrumdisorderphase3 14

Neurologicaldisorder 30

Note:DAWBA=DevelopmentandWell-BeingAssessment.K-SADS-PL=ScheduleforAffectiveDisordersandSchizophreniaforSchool-AgeChildren– PresentandLifetimeVersion.DISCO=DiagnosticInterviewforSocialandCommunicationDisorders.

aNotethatchildrenmayhavemorethanonediagnosis.

2.3. Missingdata

WhencalculatingtheASSQtotalscore,themeanscoreofthetotalsamplewasinsertedformissingitemswhen4/27(15%) orfeweritemsweremissing.ASSQformswithmorethanfouritemsmissingwerediscardedfromthepresentanalyses.

Formsfrom325(98.8%)parentswerecompletedwithfourorfeweritemsmissingandincludedinthepresentstudy.

2.4. Statisticalanalyses

IBMSPSSStatistics20wasusedfordataanalyses.Independent-samplest-testsandchi-squaretestswereusedtoanalyse gender-differences. Effect sizes (Cohen’s d and

h

p²) of significant mean differences werecalculated and interpreted accordingtoCohen(1988),inwhichadvalueof0.20=small,0.50=medium,and0.80=large,anda

h

p²of0.01=small, 0.06=medium,0.13=large.Bivariatecorrelationanalyses(Pearson’sr)wereusedtoanalyserelationsbetweenIQandASSQ scoresandinterpretedaccordingtoCohen(1988),inwhichanrvalueof0.10–0.29islow,0.30–0.49ismoderate,and0.50–

1.0ishigh.SignificantresultswerefollowedbyunivariateANOVAsusingtheGLMpackage,includingtheASSQscoresas dependentvariablesinseparateanalysesandgenderandtheFSIQscoreasfixedfactorsinafullfactorialmodel.Theanalyses wererepeatedbyincludingthethreeFSIQlevelsasafixedfactortogetherwithgender.SignificanteffectsofthethreeFSIQ levelswerefollowedbyposthoctestsusingTukeyHSDcorrectionformultiplecomparisons.

3. Results

3.1. Genderandage

Themeanageofthesamplewas10years,withafouryearsrange.Thereweresignificantlymoreboys(64.3%)thangirlsin thesample(x²=26.61,p<0.001),withanon-significantgender-differenceinage(Table2).

3.2. Intellectualfunction

Overall, the meanWISC-III scoreswere below thestandardized mean of 100, with a wide distribution. Boyshad significantlylowerPIQscoresthangirls(t(323)= 3.05,p=0.002),whilethemeandifferencefortheotherIQscoreswere non-significant(Table2).

Ofthetotalsample,42children(15.8%oftheboysand7.8%ofthegirls)hadFSIQ<70,66children(22.0%oftheboysand 17.2%ofthegirls)between70and84,and217children(62.2%oftheboysand75.0%ofthegirls)hadFSIQ85.Therewere 123children(37.8%)showingasignificantVIQ–PIQdiscrepancy(68boysand55girls),ofwhich39childrenhaddiscrepantly higherVIQ(VIQ>PIQ)(13.9%oftheboysand7.8%ofthegirls)and85childrendiscrepantlyhigherPIQ(PIV>VIQ)(18.7%of theboysand39.7%ofthegirls).Theremaining202childrenhadnosignificantVIQ–PIQdiscrepancy(VIQPIQ).

3.3. Autisticfeatures

ThetotalASSQscoreinthesamplerangedfrom0to42,withameanscoreof6.4.Boysobtainedsignificantlyhigherscores thangirlsonallASSQvariablesexcepttheAutisticstylefactorscore.Theeffectsizesofthesignificantmeandifferences betweenboysandgirlsrangedfromsmalltomediumsize(Table2).ThemeanASSQscoreswithinthedifferentFSIQlevels anddiscrepancygroupsareshownforgirlsandboysinTable3.ThegenderdifferencesinASSQscoreswithinthethreeFSIQ levelswereallnon-significant.

Table2

Age,IQandASSQscores(mean,SDandrange)inthetotalsampleandinboysandgirls.

Total(N=325) Boys(n=209) Girls(n=116) d

Age^a 9.96(0.97,7.77–11.98) 10.02(1.00,7.77–11.98) 9.86(0.92,7.81–11.57)

WISC-IIIIQ^a

FSIQ 89.12(17.89,37–133) 87.78(18.20,37–133) 91.54(17.14,37–126) 0.21

VIQ 88.58(16.29,42–136) 88.39(17.24,42–136) 88.91(14.48,42–116) 0.03

PIQ 92.30(19.10,32–136) 89.92(18.42,32–129) 96.59(19.64,35–136)^** 0.35

ASSQscores^a

Totalscore 6.42(7.00,0–42) 7.42(7.46,0–42) 4.61(5.73,0–31)^*** 0.42

Socialdifficulties 3.18(4.05,0–17) 3.79(4.37,0–17) 2.09(3.14,0–13)^*** 0.45

Motor/tics/OCD 0.76(1.58,0–12) 0.96(1.72,0–12) 0.41(1.24,0–10)^*** 0.37

Autisticstyle 2.13(2.23,1–13) 2.30(2.37,0–13) 1.84(1.92,0–7) 0.21

Note:FSIQ=fullscaleIQ.VIQ=verbalIQ.PIQ=performanceIQ.ASSQ=AutismSpectrumScreeningQuestionnaire.d=Cohen’sd(effectsize).

a Datageneratedfromindependentsamplest-testandpresentedasmean(SD,range).

*** p<0.001.

** p<0.01.

3.4. Associationsbetweenintellectualfunctionandautisticfeatures

Table4showsthecorrelationsbetweentheFSIQandASSQscoresinthetotalsampleandwithinthetwogendergroups.

Allcorrelations,exceptfortheAutisticstylefactorscoreinboys,werestatisticallysignificantandinthelowtomediumrange (Cohen,1988).

UnivariateANOVAanalysesshowedastatisticallysignificantmaineffectofgenderandFSIQscorewhenthetotalASSQ score,theSocialdifficultiesandMotor/tics/OCDfactorscoreswereincludedasdependentvariables(Table5).Theeffects wereaboutmediumsizeforgenderandFSIQonthefullASSQscoreandtheSocialdifficultiesfactorscore,butthesizewas muchsmallerforgenderontheMotor/tics/OCDfactorscore.Theinteractioneffectwasstatisticallysignificant(p=0.003)for theSocialdifficultiesfactorscore,meaningthatthisscorewashigherinboysthaningirls(indicatingmoredifficulties)inthe lowerendoftheFSIQscale,withasteeperslopeinboys,makingtheSocialdifficultiesfactorscoreinthetwogendergroups

Table5

SummaryofresultsfromANOVA,showingtheeffectsofgenderandFSIQonASSQscores,withseparateanalysesfortheFSIQatascalelevelandcategorized intothreelevels(N=325).

FSIQatascalelevel FSIQcategorizedintothreelevels

F p-Value d F p-Value hp²

ASSQtotalscore

Gender 9.6 0.002 0.45 2.8 ns 0.01

FSIQ 2.6 <0.001 0.49 23.4 <0.001 0.13

Gender:FSIQ 1.4 0.059 0.23 0.3 ns 0.00

ASSQSocialdifficulties

Gender 12.5 <0.001 0.58 4.6 0.033 0.014

FSIQ 2.8 <0.001 0.52 22.5 <0.001 0.12

Gender:FSIQ 1.8 0.3 0.28 0.41 ns 0.00

ASSQMotor/tics/OCD

Gender 5.5 0.020 0.03 1.7 ns 0.01

FSIQ 2.4 <0.001 0.47 25.7 <0.001 0.14

Gender:FSIQ 0.72 ns 0.13 0.2 ns 0.00

ASSQAutisticstyle

Gender 1.4 ns 0.01 0.1 ns 0.00

FSIQ 1.1 ns 0.29 4.3 0.001 0.026

Gender:FSIQ 0.9 ns 0.17 0.5 ns 0.00

Note:FSIQ=fullscaleIQ.ASSQ=AutismSpectrumScreeningQuestionnaire.d=Cohen’sd(effectsize).hp²=h²(effectsize).ns=non-significant.

Table3

ASSQscoresinboysandgirlsaccordingtoFSIQlevelanddiscrepancyscore(N=325).

ASSQtotalscore^a Socialdifficultiesfactorscore^a Motor/tics/OCDfactorscore^a Autisticstylefactorscore^a

Boys Girls Boys Girls Boys Girls Boys Girls

FSIQlevel

<70 13.85(9.16) 11.89(8.13) 7.47(5.28) 5.56(3.97) 2.52(2.27) 2.44(1.59) 3.00(2.80) 3.11(2.37)

70–84 7.67(5.46) 6.90(4.99) 4.33(3.76) 3.80(3.85) 0.74(1.20) 0.35(0.75) 2.33(2.14) 2.35(1.90)

>85 5.69(6.68) 3.33(4.88) 2.69(3.78) 1.34(2.43) 0.64(1.49) 0.21(1.11) 2.11(2.32) 1.59(1.81)

Discrepancyscore

VIQ>PIQ 7.34(6.44) 9.11(12.38) 3.76(4.05) 4.11(5.64) 1.07(1.67) 2.00(3.46) 2.38(2.13) 2.56(3.00) PIQ>VIQ 8.38(8.74) 3.59(4.17)^** 4.33(4.89) 1.63(2.59)^** 1.15(1.76) 0.20(0.54)^** 2.23(2.72) 1.41(1.60) VIQPIQ 7.16(7.28) 4.72(5.06)^** 3.65(4.30) 2.15(2.97)^** 0.88(1.72) 0.33(0.85)^** 2.30(2.33) 2.05(1.91) Note:FSIQ=fullscaleIQ.VIQ=verbalIQ.PIQ=performanceIQ.ASSQ=AutismSpectrumScreeningQuestionnaire.

aDatageneratedfromindependentsamplest-testandpresentedasmean(SD,range).

** p<0.01.

Table4

CorrelationsbetweenIQandASSQscoresinthetotalsample(N=325).

ASSQtotalscore Socialdifficulties Motor/tics/OCD Autisticstyle

FSIQtotalsample 0.37^** 0.39^** 0.34^** 0.15^**

FSIQboys(n=209) 0.35^** 0.38^** 0.30^** 0.10

FSIQgirls(n=116) 0.40^** 0.37^** 0.43^** 0.23^*

Note:FSIQ=fullscaleIQ.ASSQ=AutismSpectrumScreeningQuestionnaire.

** p<0.01(2-tailed).

* p<0.05(2-tailed).

similaratthehighestendoftheFSIQscale.Amoreparallelslope,withboysobtainingthehighestASSQscores,wasfoundon theothertwoscales.TheeffectsofgenderandFSIQwerenon-significantfortheAutisticstylefactorscore.

TheANOVAanalyseswererepeatedbysubstitutingthecontinuousFSIQscorewiththreelevelsofFSIQthatcommonly areusedclinicallytoevaluateachild’sintellectualfunction.TheeffectofFSIQ-levelwasstatisticallysignificantfortheASSQ totalscoreandallthethreefactorscores,withlarge

h

p²forallbuttheAutisticstylefactorscore(Table5).Aposthocanalysis withTukeycorrectionformultiplecomparisonsshowedthattheASSQtotalandallthefactorscoresintheIQ<70subgroup weresignificantlyhigherthanintheothertwogroups(p<0.001).Furthermore,theintermediategroupwashigherthanthe IQ85groupontheASSQtotal(p=0.008)andtheSocialdifficultiesfactorscore(p<0.001).Theeffectofgenderwasonly statisticallysignificantfortheSocialdifficultiesfactorscore,reflectingthatboysobtainedasomewhathigherscorethangirls acrossthethreeFSIQlevels(Table3).NoneoftheinteractionsbetweenFSIQandgenderwerestatisticallysignificant.

3.5. IQdiscrepancyscoreandautisticfeatures

TheeffectofdiscrepancygroupontheASSQscoreswasinvestigatedbyANOVAanalysesincludingdiscrepancyscore (VIQ>PIQ,PIV>VIQ,VIQPIQ)asafactorinseparateanalysestogetherwithgenderandaninteractionterm.Astatistically significanteffectofdiscrepancygroupwasonlyfoundontheMotor/tics/OCDfactor,F=4.3,p=0.14,

h

p²=0.026.Onthis variable,therewasalsoasignificantinteractioneffectbetweendiscrepancygroupandgender,F=3.9,p=0.22,

h

p²=0.024, reflecting thatgirlshad a higherscorethanboysin thesubgroupwithVIQ>PIQ.Boys,on theotherhand,showeda significantlyhigherscorewhenthePIQ>VIQ(Table3).Theeffectswerenon-significantforallASSQscoreswhenFSIQlevel orthecontinuousFSIQscorewereincludedascovariates,andwhensplittingthediscrepancygroupintothosewithand withoutadiscrepancy.

4. Discussion

4.1. Summaryoffindings

ThepresentstudyexaminedassociationsbetweenIQ,genderandautisticfeaturesinasampleofchildrenselectedfroma population-basedcohort.Firstofall,wedidnotfindtheexpectedimpactofhavingalargediscrepancybetweenverbaland performanceIQonthefrequencyofautisticfeatures.TheonlyeffectfoundwasontheMotor/tics/OCDfactorscore.The relationshipbetweenIQandautisticfeatureswasnegativeandmoderateforallASSQvariablesexcepttheAutisticstyle factorscore,withtheASSQscoreshowingagradualdeclinewithhigherFSIQforbothgenders.ThecontinuousFSIQscore interactedwithgenderontheSocialdifficultiesfactorscore.

4.2. Generaldiscussion

Inline withfindingsfrompopulationstudies(Constantino&Todd,2003;Kamioetal.,2012;Posserudetal.,2006), parentsratedtheASSQscoressignificantlyhigherinboysthaningirls.Surprisingly,thiswasnotfoundfortheAutisticstyle factorscore.AccordingtoPosserudetal.(2008,p.109),‘‘thisfactorcouldrepresentasetofitemsthataremorespecificfor childrenwithASDasopposedtochildrenwithsocialdifficultiesforotherreasons’’.Also,inclinicalsamplesofchildrenwith ASD,thefrequencyofboysandgirlspresentingwiththesefeatureshavenotbeenshowntodiffersignificantly,whereasthey discriminatedwellbetweenASDandnon-ASDcasesandbetweenASDandADHDcases(Kopp&Gillberg,2011).Inasample selectedfromapopulation,then,oneshouldperhapsnotexpectthesemore‘‘ASDspecific’’featurestooccurmoreorless frequentlyinanyofthetwogenders.Thisassumptionwasconfirmedbyafollow-upanalysiswheretheASSQscoreswerez- transformed,showingthattheAutisticstylefactorscorewastheleastwidespreadforbothgenders.

Overall,discrepantverbalversusnon-verbalskillswerenotassociatedwithaspecificpatternofASDsymptomsinthe presentstudy.Inthisrespect,ourresultssupportedtheconclusionbyCharmanetal.(2011).Conflictingresultswithother studies mayberelated todifferences in assessment methods(ASSQversus AQ/ADOS/ADI)and sample characteristics (children selected froma population-basedsample versus clinical samples). Also, one longitudinal study of ASDhas demonstratedthatnegativeeffectsof‘‘non-verballearningproblems’’(VIQ>PIQ)onsocialandexecutiveoutcomewere demonstratedonlyforthesubgroupwithpersistent(morethannineyearsafterstudyinschoolage)non-verballearning problems(Hagberg,Nyden,Cederlund,&Gillberg,2013).However,theeffectsshowninthepresentstudyofdiscrepancy groupanditsinteractionwithgenderontheMotor/tics/OCDfactorareworthacomment.Onthisfactorscore,theimpactofa discrepantlyhigherVIQorPIQwasspecifictogirlsandboys,respectively.ThefindingofahigherASSQscoreinboyswith PIQ>VIQaccordswithassociationsfoundbetweendiscrepantlyhighernonverbalabilitiesandautisticfeaturesinsamples ofpredominantlyboyswithASD(Blacketal.,2009;Josephetal.,2002)andKlinefeltersyndrome(vanRijn&Swaab,2011).

ThefindingofahigherMotor/tics/OCDfactorscoreingirlswithVIQ>PIQisnotaseasilyunderstood,asgirlsarescarceinthe studiesexaminingtheseassociations(Blacketal.,2009;Charmanetal.,2011;Josephetal.,2002;vanRijn&Swaab,2011).

BetterverbalversusperformancescoresinchildrenwithASDhasbeenlinkedtopoorcoordination,butnotspecificallyin girls(Wing,1981).FuturestudiesshouldfurtherinvestigatethisgenderdifferenceinIQdiscrepancyandautisticfeatures.

Thepresentstudyincludedinformationaboutintellectualfunctioningasmeasuredbythefull-scalescoreonanIQtest andbycategorizingthescoresaccordingtoatraditioncommonlyusedintheclinictodescribeintellectualfunctionofachild.

Basedontheanalysesofthefullscale,thedifferencebetweengirlsandboyswasclearlylargerwhentheFSIQscorewaslow, withsimilarresultsbetweenthetwogendergroupswhentheyobtainedahighFSIQscoretogetherwithascoreoforabout zeroontheASSQ.ThemaincontributionofincludinglevelswastoshowthatalthoughASDmayoccuratalllevelsof intellectualfunctioning(AmericanPsychiatricAssociation,2013),anIQlevel<70isnotonlyassociatedwithahighrateof ASD(DiGuiseppietal.,2010;Gillberg&Soderstrom,2003;Kent,Evans,Paul,&Sharp,1999),butalsowithautisticfeatures inasamplewherethesefeaturesarewidelydistributedalongthewholescale.Ourfindingsareinaccordancewithstudies showinghighratesofsocialproblemsinchildrenwithintellectualdisability(Dekkeretal.,2002),aswellaswithresults fromalarge-scaleJapanesepopulationsurvey(Kamioetal.,2012),inwhichtheauthorsreportedthatscoresontheSocial ResponsivenessScale(SRS),aquestionnaireofautistictraits(Constantino&Gruber,2005),showedlowcorrelationwithan IQscoreinthenormalrange,whilechildrenwithintellectualdisabilitytendedtohavehigherSRSscores.IQwasalsofound tobeamoderatorofASDsymptomsinastudyofadultswithintellectualdisabilitywhensplitinto‘‘lowIQ’’versus‘‘high IQ’’,showinga decreaseinASDsymptomswithhigherIQ(Matson,Dempsey,Lovullo,&Wilkins,2008).Incontrast, intellectualdevelopmentwasnotfoundtobeamoderatorofASDsymptomsinarecentstudyofinfantsandtoddlerswith autism,PDD-NOS,andatypicaldevelopmentwhensplitintoa‘‘lowdevelopmentallevel’’anda‘‘highdevelopmental level’’. However, developmental level was found to be higher in individuals who displayed less ASD symptoms (Matsonetal.,2013).

ThehighASSQscoresatthelowerendoftheIQscalemayberelatedtothefactthatthechildrenwithaFSIQ<70were characterizedbyaratherhighrateofneurologicaldisorders(26.2%,comparedto9.1%inchildrenwithFSIQ70–84,and3.2%

inchildrenwitha>85)inadditiontotheirintellectualdisability.Neurologicaldisordershavecommonlybeenassociated withsymptomsofASD(Gillberg,2010;Ryland,Hysing,Posserud,Gillberg,&Lundervold,2012),andithasbeenproposed thatcognitiveimpairments,suchasintellectualdisability,inchildrenwithneurologicaldisordersmayinhibittheirsocial informationprocessingskills,which,inturn,mayhaveanegativeimpactonthechildren’ssocialfunctioning(Boni,Brown, Davis,Hsu,&Hopkins,2001;Bottcher,2010);e.g.,reflectedinmoreautisticfeatures.

4.3. Strengthsandlimitations

Themainstrengthofthestudywastheuseofastandardizedtestofintellectualfunction(WISC-III)andavalidated instrumentforautisticfeatures(ASSQ).Otherstrengthsarerelatedtocharacteristicsofthesample.Although‘‘enriched’’by bothdevelopmentallyandphysicallydisabledchildren,thechildrenwereselectedfromapopulation-basedstudy.Because ofthis,thesampleincludedbothchildrenwithandwithoutproblemsaccordingtoascreeninginstrumentassessingmental health,andthechildren showeda widedistributionofboth intellectualfunctionandautistic features.Thestudyalso includedasubstantialnumberofgirls,makingitpossibletoexaminegender-differencesinWISC-IIIandASSQscoresand relationsbetweenthetwo.

Thepresentstudyhasseverallimitations.Firstofall,autisticfeatureswerenotassessedbyincludingdirectobservation andstandardizedclinicalevaluationofthechildren,buttheinformationwassolelybasedonparentreports.Secondly,the distributionofFSIQscoreswasskewedtowardsthelowerendoftheFSIQ-scale,probablyduetohowthesamplewas recruited.Ontheotherhand,coveringthefullrangeofFSIQscoresmayalsobeconsideredtobeastrength.Thirdly,sincethe ASSQfactorshavenotbeenvalidated,theresultsregardingfactorscoresshouldbeinterpretedwithcaution.Furthermore, methodologicaldifferencesregardingsampleandassessmentmadeitdifficulttocomparethepresentfindingswithresults ofearlierstudies,whichhavemainlyfocusedonchildrenwithASD.However,littlewasknownabouthowintellectual functionandgenderisrelatedtothebroaderdistributionofautisticfeaturesinchildren.Assuch,webelievethepresent studyhasadded newknowledge,althoughfirm conclusionsregardingthegeneralizabilityoftheresultsawaitfurther studiesincludinglargersamplesandsubgroupsofchildrenrepresentingthedifferentFSIQlevelsandFSIQdiscrepancies.

Finally,cognitiveabilitieshaverecentlybeenassociatedwithadaptivefunctioninginpreschoolchildren(Hedvalletal., 2013)andyoungadults(Hagbergetal.,2013)withASD.Futurestudiesshouldincludemeasuresofadaptivefunctioningto furtherassesstheimpactofcognitivefunctiononoutcomeinchildrenwithautisticfeatures.

4.4. Clinicalimplications

In thepresent sampleselected froma population-basedcohort, therelationshipbetween measures ofintellectual functioningandautisticfeatureswasfarfromstraightforward.Thishighlightstheimportanceofnotinferringintellectual functionfromautisticfeaturesandviceversawheninvestigatingchildrenfromageneralpopulation,andtheimportanceof conductingacarefulassessmentbeforereachingclinicalconclusionsinagivenchild.

5. Conclusion

ThepresentstudyshowedthattherelationshipbetweenautisticfeaturesasassessedbytheASSQandresultson a commonlyusedIQ-testwasmainlyexplainedbychildrenwithFSIQscoresatthelowerendofthedistribution.Discrepancies betweenverbalandperformanceIQwerefoundtoberelativelyunrelatedtoASSQscores.Thepresentfindingscallforfuture studiesincludingabroaderrangeofcognitivetasksandmeasuresofadaptivefunctioning,andemphasizetheimportanceof broadandcarefulassessmentsofchildrenbeforereachingconclusionsaboutcognitivefunctionandautisticfeatures.

Acknowledgements

ThepresentstudywassupportedbytheCentreforChildandAdolescentMentalHealthandWelfare,UniHealth,Uni Research,Bergen,Norway,andwasalsofundedbytheUniversityofBergen,theNorwegianDirectorateforHealthandSocial Affairs, and the WesternNorway Regional Health Authority. We are grateful to the children, parents, and teachers participatingintheBergenChildStudy(BCS),andtotheBCSprojectgroupformakingthestudypossible.

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