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ORIGINAL ARTICLE Symptoms of autism spectrum disorder in subtypes of attention- decit/hyperactivity disorder AYS ̧ E BURCU AYAZ 1 , SEBLA GÖKÇE 2 , FUNDA GÜMÜS ̧ TAS ̧ 3 & MUHAMMED AYAZ 1 1 Child and Adolescent Psychiatry Outpatient Clinic, Sakarya University Training and Research Hospital, Sakarya, Turkey, 2 Child and Adolescent Psychiatry Outpatient Clinic, Erenköy Psychiatric and Neurologic Research and Training Hospital, Istanbul, Turkey, and 3 Child and Adolescent Psychiatry Outpatient Clinic, Adıyaman University Training and Research Hospital, Adıyaman, Turkey Abstract Background This study aimed to compare symptoms of autism spectrum disorder (ASD) in children according to attention- decit/hyperactivity disorder (ADHD) subtypes and children without ADHD. Method The Schedule for Affective Disorders and Schizophrenia for School-Age Children Present and Lifetime Version (K-SADS-PL), the Social Responsiveness Scale (SRS), the Childhood Behavior Checklist (CBCL), and the ADHD Rating Scale (ADHD-RS) were used to evaluate the children. Results ASD symptoms were signicantly higher in all ADHD subtypes. After controlling for age, gender, and CBCL social withdrawal score, the difference in ASD symptoms between the 3 ADHD subtypes was not signicant. Conclusions Children with ADHD, regardless of subtype, had a similar risk of ASD symptoms. Keywords: children, attention-decit/hyperactivity disorder, autism spectrum disorder symptoms Introduction Attention-decit/hyperactivity disorder (ADHD) is a neurodevelopmental disorder that is common in school-age children (Polanczyk, de Lima, Horta, Bie- derman, & Rohde, 2007). There are three ADHD presentations: predominantly inattentive (I), predo- minantly hyperactive/impulsive (H/I), and combined (American Psychiatric Association [APA], 2013). It has been reported that some children diagnosed with ADHD have similar social interaction and com- munication difculties to those diagnosed with autism spectrum disorder (ASD; Pelham & Bender, 1982). Social interaction problems, which are dened as an important feature in ASD, include misinterpretation of nonverbal communication, such as gaze, gesture, and gait, difculties in developing appropriate friend- ships, and limited social responsiveness. According to the Diagnostic and Statistical Manual of Mental Disorders (5th ed., DSM-5, APA, 2013), for the diag- nosis of ADHD children must have at least six symp- toms from either (or both) the inattention group of criteria and the hyperactivity and impulsivity criteria. On the other hand, diagnostic criteria of ASD in DSM-5 include persistent decits in social communi- cation, problems with nonverbal communication, problems with social awareness, and restrictive, repetitive patterns of behaviour. Unlike in the DSM- IV (APA, 1994), ADHD can now be diagnosed in conjunction with ASD in the DSM-5. Clinical research has shown that autism spectrum symptoms (ASSs), such as impaired social inter- action and communication, are observed in 6580% of children diagnosed with ADHD and that the majority of children with ADHD exhibit stereoty- pic hand and body gestures (Clark, Feehan, Tinline, & Vostanis, 1999). In general, 32% of boys and 75% of girls diagnosed with ADHD scored within the © 2014 Australasian Society for Intellectual Disability, Inc. This manuscript was accepted under the Editorship of Ian Dempsey. Correspondence: Ayş e Burcu Ayaz, I ̇ stiklal Mah. Mehmet Altınış ık Cad. Defne Sok. Osmanbey sitesi B/2 No: 24 54100 Serdivan Sakarya, Turkey. E-mail: [email protected] Journal of Intellectual & Developmental Disability, 2014 Vol. 39, No. 3, 290297, http://dx.doi.org/10.3109/13668250.2014.916184

Symptoms of autism spectrum disorder in subtypes of attention-deficit/hyperactivity disorder

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Page 1: Symptoms of autism spectrum disorder in subtypes of attention-deficit/hyperactivity disorder

ORIGINAL ARTICLE

Symptoms of autism spectrum disorder in subtypes of attention-deficit/hyperactivity disorder†

AYSE BURCU AYAZ1, SEBLA GÖKÇE2, FUNDA GÜMÜSTAS3 & MUHAMMED AYAZ1

1Child and Adolescent Psychiatry Outpatient Clinic, Sakarya University Training and Research Hospital, Sakarya, Turkey,2Child and Adolescent Psychiatry Outpatient Clinic, Erenköy Psychiatric and Neurologic Research and Training Hospital,Istanbul, Turkey, and 3Child and Adolescent Psychiatry Outpatient Clinic, Adıyaman University Training and ResearchHospital, Adıyaman, Turkey

AbstractBackground This study aimed to compare symptoms of autism spectrum disorder (ASD) in children according to attention-deficit/hyperactivity disorder (ADHD) subtypes and children without ADHD.Method The Schedule for Affective Disorders and Schizophrenia for School-Age Children – Present and Lifetime Version(K-SADS-PL), the Social Responsiveness Scale (SRS), the Childhood Behavior Checklist (CBCL), and the ADHD RatingScale (ADHD-RS) were used to evaluate the children.Results ASD symptoms were significantly higher in all ADHD subtypes. After controlling for age, gender, and CBCL socialwithdrawal score, the difference in ASD symptoms between the 3 ADHD subtypes was not significant.Conclusions Children with ADHD, regardless of subtype, had a similar risk of ASD symptoms.

Keywords: children, attention-deficit/hyperactivity disorder, autism spectrum disorder symptoms

Introduction

Attention-deficit/hyperactivity disorder (ADHD) is aneurodevelopmental disorder that is common inschool-age children (Polanczyk, de Lima, Horta, Bie-derman, & Rohde, 2007). There are three ADHDpresentations: predominantly inattentive (I), predo-minantly hyperactive/impulsive (H/I), and combined(American Psychiatric Association [APA], 2013). Ithas been reported that some children diagnosedwith ADHD have similar social interaction and com-munication difficulties to those diagnosedwith autismspectrum disorder (ASD; Pelham & Bender, 1982).Social interaction problems, which are defined as animportant feature in ASD, include misinterpretationof nonverbal communication, such as gaze, gesture,and gait, difficulties in developing appropriate friend-ships, and limited social responsiveness. Accordingto the Diagnostic and Statistical Manual of Mental

Disorders (5th ed., DSM-5, APA, 2013), for the diag-nosis of ADHD children must have at least six symp-toms from either (or both) the inattention group ofcriteria and the hyperactivity and impulsivity criteria.On the other hand, diagnostic criteria of ASD inDSM-5 include persistent deficits in social communi-cation, problems with nonverbal communication,problems with social awareness, and restrictive,repetitive patterns of behaviour. Unlike in the DSM-IV (APA, 1994), ADHD can now be diagnosed inconjunction with ASD in the DSM-5.Clinical research has shown that autism spectrum

symptoms (ASSs), such as impaired social inter-action and communication, are observed in 65–80% of children diagnosed with ADHD and thatthe majority of children with ADHD exhibit stereoty-pic hand and body gestures (Clark, Feehan, Tinline,& Vostanis, 1999). In general, 32% of boys and 75%of girls diagnosed with ADHD scored within the

© 2014 Australasian Society for Intellectual Disability, Inc.

†This manuscript was accepted under the Editorship of Ian Dempsey.Correspondence: Ayse Burcu Ayaz, Istiklal Mah. Mehmet Altınısık Cad. Defne Sok. Osmanbey sitesi B/2 No: 24 54100 Serdivan Sakarya, Turkey. E-mail:[email protected]

Journal of Intellectual & Developmental Disability, 2014Vol. 39, No. 3, 290–297, http://dx.doi.org/10.3109/13668250.2014.916184

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clinical range for ASD, and children with severeforms of ADHD were found to have clinically signifi-cant symptoms in social interaction, communication,and repetitive behaviour symptom domains of autism(Reiersen, Constantino, Volk, & Todd, 2007). Astudy that examined social reciprocity in childrenwith ADHD reported that the attention deficit andhyperactivity/impulsivity problems have an inverserelationship with social reciprocity (Ayaz, Ayaz, &Yazgan, 2013). Furthermore, it was noted thatASSs, such as restricted capacity to recognise thefeelings of others and difficulty in establishingrelationships, might be caused by the main symptomsof ADHD (i.e., inattention and impulsivity; Clarket al., 1999). Despite findings that highlight theassociation of attention deficit issues and social reci-procity, an epidemiological study conducted in maletwins reported that genetic factors that affect socialreciprocity differ from those that affect attention(Constantino, Hudziak, & Todd, 2003).

Although ASSs, including impairment in socialreciprocity, are usually observed in individuals withADHD, there are a limited number of studies onASSs in ADHD subtypes. Additionally, the relation-ship between ASSs observed in ADHD and thesymptoms of ADHD is unclear. As such, thepresent study aimed to compare ASSs betweenADHD subtypes and children without ADHD, aswell as to investigate the relationship between thesymptoms of ADHD and ASSs in ADHD subtypes.

Materials and methods

This study was conducted in the Child and Adoles-cent Psychiatry Clinic at the Sakarya UniversityTraining and Research Hospital in Sakarya,Turkey. The study protocol was approved by theSakarya University School of Medicine Ethics Com-mittee (030.01.04/21). Permission to invite publicschool students to participate in the study’s controlgroup was obtained from the Sakarya ProvincialDirectorate for National Education.

Participants

This study included 387 children/adolescents: 238 inthe ADHD group and 149 in the control group. Thestudy group consisted of 6–17-year-old children andadolescents, who agreed to participate in the study,and who were diagnosed with ADHD for the firsttime by a child psychiatrist between 1 January 2013and 1 June 2013. Participants’ diagnoses werebased on clinical examination and DSM-IV (APA,1994) diagnostic criteria. Children considered tohave intellectual disability and/or who were

diagnosed with ASD, psychosis, or bipolar disordervia a semistructured interview were excluded fromthe study. Children who were previously diagnosedas having ADHD and received psychological orpharmacological treatment were also excluded fromthe study group. The control group includedprimary and high school students aged 6–17 yearsof age who did not have ADHD, intellectual disabil-ity, psychosis, bipolar disorder, or ASD. All of theparticipants and their families were informed aboutthe study by the researchers, and written informedconsent was obtained from the parents.

Materials

Schedule for Affective Disorders and Schizophrenia forSchool-Age Children – Present and Lifetime Version(K-SADS-PL). The K-SADS-PL is a semistructuredinterview developed by Kaufman et al. (1997) that isused to determine present and lifetime affective dis-orders in children and adolescents based on DSM-IV (APA, 1994) diagnostic criteria. The Turkishversion of the scale was reported to be valid andreliable for use in Turkey (Gökler et al., 2004). TheK-SADS-PL was used to determine the presence ofpsychiatric disorders in the participants, and at leastone parent who could provide information abouttheir child participated in the assessment process.

Childhood Behavior Checklist (CBCL; ages 4–18 years).The CBCL was developed by Achenbach and Edel-brock (1983). The 1991 version of the scale was trans-lated intoTurkish and subsequently updated to ensurethe Turkish version’s validity and reliability for use inTurkey in accordance with the scale’s 1985 version(Akçakın, 1985; Erol & Simsek, 1998). The CBCLprovides two behaviour symptom scores: internal pro-blems and external problems. The internal problemsscore is based on the CBCL social withdrawal,somatic complaints, and anxiety/depression subscalescores, and the external problems score is based onthe CBCL criminal behaviours and aggressive beha-viours subscale scores. In addition, theCBCL includessocial problems, thought problems, sexual problems,and attention problems subscales. In the presentstudy, CBCL was used to determine the severity ofsocial withdrawal in the participants.

Social Responsiveness Scale (SRS). The SRS was devel-oped by Constantino for assessing ASSs (Constantino,Davis et al., 2003; Constantino, Przybeck, Friesen, &Todd, 2000). The scale has 65 items: 39 items regard-ing observable mutual social behaviours, six regardingsocial use of language, and 20 items regarding beha-viours characteristic of ASD. Higher scores are

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indicative of more severe social impairment. The SRSwas used to assess ASSs in the study population.

The ADHD Rating Scale. The ADHD Rating Scale(ADHD-RS) is an 18-item questionnaire based onDSM-IV (APA, 1994) diagnostic criteria forADHD. The scale is completed independently by aparent and scored by a clinician. The scale consistsof two subscales: inattention (nine items) and hyper-activity/impulsivity (nine items). Each item is scored0 (not at all), 1 (a little), 2 (pretty much), or 3 (verymuch); the total scale score range is 0–54. Theparent version of the ADHD-RS has a large base ofnormative data and has been shown to be reliableand have discriminant validity in children and adoles-cents (DuPaul, Power, Anastopoulos, & Reid, 1998).The scale was used to measure the severity of ADHDsymptoms in the study participants.

Procedures

The ADHD group included children and adolescentsthat presented to the Child and Adolescent Psychia-try Clinic for the first time with a prediagnosis ofADHD. Those who agreed to participate in thestudy (238 children and adolescents) were evaluated.The control group was composed of 149 students

from a primary school and high school in the Adapa-zarı district of Sakarya who were selected via randomsampling. Students in the first grade were notincluded, as they were aged 5–6 years old. TheCBCL was sent to the parents of the selected stu-dents. Students with an attention subscale scoreindicative of the absence of clinically relevant atten-tion deficit and hyperactivity/impulsivity problemswere invited to participate in the study by setting upan appointment by phone.The researchers administered the K-SADS-PL to

all of the children/adolescents and one of theirparents, and DSM-IV (APA, 1994) Axis I diagnoseswere determined. During the interview, the diag-noses of the participants that could not be scannedthrough the K-SADS-PL, such as ASD, dyslexia,communication disorders, and attachment disorder,were evaluated with a semistructured interviewbased on the DSM-IV diagnostic criteria. Theparents of the children/adolescents in the ADHDgroup completed the ADHD-RS, CBCL, and SRS,and the parents of the students in the control groupcompleted the SRS.

Statistical analysis

SPSS Version 17.0 for Windows was used to analysethe data. Univariate analysis of variance (ANOVA)

was used to compare continuous data between thethree ADHD subtypes. SRS scores were covariedaccording to age, gender, and CBCL social withdra-wal score; they were then reevaluated using the uni-variate general linear model. Pearson’s correlationanalysis was used to determine correlations. Thelevel of statistical significance was accepted asp < .05 for all analyses.

Findings

In the ADHD group, 28.6% (n = 68) were diagnosedas ADHD I subtype, 13.0% (n = 31) as ADHD H/Isubtype, and 58.4% (n = 139) as ADHD combinedsubtype. The mean age in the ADHD group (10.99± 2.30 years) and control group (11.24 ± 2.40years) was similar (t= –1.041, p= .299). In all,64.7% (n = 154) of the ADHD group and 57% (n= 85) of the control group were male (χ² = 2.276, p= .131). Among those in the ADHD group, ≥ 1comorbid psychiatric disorders were noted in38.2% (n = 26) of the ADHD I subtype patients,58.1% (n = 18) of the H/I subtype patients, and53.2% (n = 74) of the combined subtype patients.In the control group, 6.7% (n = 10) of the studentswere diagnosed with a psychiatric disorder.The mean CBCL total score, internal problems,

external problems, and social withdrawal subscalescores differed significantly among the controlgroup and the three ADHD subtypes (Table 1).The CBCL social withdrawal scores were signifi-cantly different between the ADHD I subtype andthe control group (p< .001), between the ADHDcombined subtype and the control group (p < .001),and between the ADHD combined subtype and theH/I subtype (p= .007). The CBCL social withdrawalscore was correlated with the SRS total (r= .24, p< .001), SRS communication (r = .19, p = .003),SRS social (r = .27, p< .001), and SRS autism (r= .25, p < .001) subscale scores.Based on the ANOVA, the mean SRS total and all

subscale scores were significantly higher in all ADHDsubtypes than in the control group (p< .001). TheSRS total and the social subscale scores were higherin the ADHD combined subtype than in theADHD H/I subtype (p< .05). SRS communication,autism, and stereotypic behaviour subscale scoresdid not significantly differ between the threeADHD subtypes (p > .05). After controlling for theeffect of age, gender, and CBCL social withdrawalscore, there was a significant difference in SRS totaland all subscale scores among the control groupand the three ADHD subtypes; however, the differ-ence between the three ADHD subtypes was not sig-nificant (see Table 2).

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Assessment of the relationship between theADHD-RS subscale scores and the SRS total andsubscale scores based on Pearson’s correlation analy-sis showed that there was no significant correlationbetween ADHD-RS subscale scores and any SRSscore in any of the three ADHD subtypes (seeTable 3).

Discussion

In this study, three ADHD subtypes were comparedto each other and to a control group in terms of ASSs.

In addition, the relationship between ASSs andADHD symptom severity was investigated in allADHD subtypes. The findings show that ASSsoccurred more frequently in the ADHD group thanin the control group. Furthermore, there was no sig-nificant difference in ASSs between the three ADHDsubtypes, and there was no significant correlationbetween the symptoms of ADHD and ASSs.Previous studies mentioned that the impairment in

social reciprocity, communication deficits, andstereotypic behaviours observed in ASD might alsobe seen in children with ADHD and that children

Table 2. Comparison of SRS after age, gender, and CBCL social withdrawal were adjusted using covariates

Mean Covariated mean SE ANOVA test result

SRS total scoreControl group 45.99 ± 20.22 49.47 1.99 F= 48.77, df = 3, p< .001ADHD I subtype 84.16 ± 26.47 81.98 2.85ADHD H/I subtype 71.81 ± 27.74 72.76 4.15ADHD combined subtype 85.13 ± 25.26 82.26 2.04

SRS social subscale scoreControl group 37.83 ± 14.92 40.49 1.40 F= 39.38, df = 3, p< .001ADHD I subtype 63.00 ± 18.16 61.48 2.00ADHD H/I subtype 53.71 ± 17.27 54.38 2.91ADHD combined subtype 63.28 ± 17.97 61.02 1.43

SRS communication subscale scoreControl group 2.87 ± 2.41 3.24 0.29 F= 41.62, df = 3, p< .001ADHD I subtype 8.07 ± 3.95 7.86 0.42ADHD H/I subtype 6.19 ± 4.44 6.28 0.61ADHD combined subtype 7.83 ± 3.78 7.52 0.30

SRS stereotypic behaviour subscale scoreControl group 5.29 ± 4.93 5.75 0.54 F= 37.25, df = 3, p< .001ADHD I subtype 13.09 ± 7.56 12.65 0.77ADHD H/I subtype 11.90 ± 8.38 12.09 1.12ADHD combined subtype 14.02 ± 6.44 13.71 0.55

SRS autism subscale scoreControl group 3.87 ± 3.49 4.54 0.40 F= 39.38, df = 3, p< .001ADHD I subtype 9.81 ± 5.33 9.41 0.57ADHD H/I subtype 8.13 ± 5.91 8.31 0.82ADHD combined subtype 10.42 ± 5.23 9.86 0.41

Note. ADHD I = attention-deficit/hyperactivity disorder inattentive; ADHD H/I = attention-deficit/hyperactivity disorder hyperactivity/impulsivity; CBCL=Childhood Behavior Checklist; SRS = Social Reciprocity Scale.∗p < .001.

Table 1. Mean CBCL scores

Control groupADHD Isubtype

ADHD H/Isubtype

ADHD combinedsubtype ANOVA test result

CBCL total score 46.79 ± 10.48 60.57 ± 7.93 64.03 ± 7.11 66.81 ± 9.12 F= 118.57, df= 3,p < .001

CBCL internal problemssubscale score

51.15 ± 10.41 60.78 ± 8.48 60.74 ± 7.33 62.47 ± 10.56 F= 35.39, df= 3,p < .001

CBCL external problemssubscale score

44.70 ± 9.31 55.60 ± 9.16 61.55 ± 8.86 64.00 ± 9.82 F= 106.24, df= 3,p < .001

CBCL social withdrawalsubscale score

53.46 ± 5.96 60.04 ± 7.55 56.35 ± 7.74 61.44 ± 9.60 F= 27.35, df= 3,p < .001

Note. ADHD I = attention-deficit/hyperactivity disorder inattentive; ADHD H/I = attention-deficit/hyperactivity disorder hyperactivity/impulsivity; CBCL=Childhood Behavior Checklist.

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diagnosed with ADHD have impaired social recipro-city when compared to children not diagnosed withADHD (Clark et al., 1999; Constantino, Hudziak,et al., 2003; Santosh & Mijovic, 2004). In addition,it was reported that children with ADHD who haveimpaired social skills have a higher rate of comorbidpsychiatric diagnosis (Greene et al., 1996; Mulliganet al., 2009). A recent study reported that 54.7% ofchildren with ADHD had subclinical or clinicalASSs, and when the difference in intelligence levelbetween the ADHD group and the control groupwas controlled for, the difference in ASSs betweenthe two groups persisted (Ayaz et al., 2013). Thepresent findings support the notion that ASSs occurmore frequently in children with ADHD than inthose without ADHD.There are a limited number of studies comparing

social reciprocity and social skills according to thesubtypes of ADHD. The Missouri Twin Study,which examined characteristics of ASD in subtypesof ADHD, reported that unlike those with ADHDI or the combined subtype, children with the H/Isubtype did not have significantly higher SRSscores (Reiersen et al., 2007). Additionally, a studyby Fernández-Jaén et al. (2011) that evaluatedsocial skills in ADHD using the Behaviour Assess-ment System for Children (BASC) reported thatthe level of social skills was highest in those withthe H/I subtype, followed by those with the com-bined subtype and I subtype; the differencebetween those with the combined and I subtypeswas significant. Additionally, it was reported thatthe symptomatic intensity of attention deficit nega-tively affected social skills (Fernández-Jaén et al.,2011). Previous studies also reported that therewas a relationship between ADHD and ASSs;however, the symptoms of attention deficit or

hyperactivity/impulsivity were insufficient toexplain the relationship, and ASSs potentiallyindex a subgroup of ADHD (Mulligan et al.,2009; Nijmeijer et al., 2009). In contrast with thepredominant findings in the literature, the presentfindings indicate that there is no difference inASSs between ADHD subtypes. Furthermore, thefindings support the notion that the symptom setsof ADHD are insufficient for explaining therelationship between ADHD and ASSs.In addition to ASSs, shyness and social withdrawal

symptoms differed between ADHD subtypes andwere observed more frequently in those with theADHD I subtype than in those with the ADHD H/Isubtype and the control group (Hodgens, Cole, &Boldizar, 2000). Moreover, shyness and social with-drawal symptoms that were frequently observed inchildren with the ADHD I subtype have a negativeeffect on social function by diminishing the frequencyof interaction with others, and, as such, the ADHD Isubtype could be considered a disorder distinct fromADHD H/I and combined subtypes (Barkley, 2003;Milich, Balentine, & Lynam, 2001). It is reportedthat even though almost 50% of individuals diag-nosed with ASD exhibit symptoms of social withdra-wal at the subclinical level, social withdrawal is notspecific to ASD and might be associated with anumber of affective disorders, including anxiety,depression, psychosis, personality disorders, andsuicidal behaviour (Mazefsky, Anderson, Conner, &Minshew, 2011; Rubin, Althoff, Walkup, &Hudziak, 2013). These findings indicate a widediversity of social withdrawal symptoms in affectivedisorders that is not specific to the ADHD Isubtype but that might have a marked impact onthe comorbid symptomatology of ADHD such asASSs.

Table 3. Correlations between SRS scores and the severity of ADHD symptoms based on the ADHD Rating Scale

GroupSRS communication

subscaleSRS stereotypic

behaviour subscaleSRS socialsubscale

SRS autismsubscale SRS total

ADHD I subtype I score r= .104 r =−.085 r=−.109 r=−.005 r=−.084p= .405 p= .499 p= .384 p= .968 p= .503

H/I score r= .090 r= .223 r= .027 r= .162 r = .096p= .474 p= .071 p= .831 p= .195 p= .445

ADHD H/I subtype I score r=−.012 r= .159 r= .212 r= .083 r = .178p= .948 p= .394 p= .251 p= .657 p= .337

H/I score r=−.042 r= .022 r=−.067 r=−.177 r=−.042p= .820 p= .906 p= .721 p= .341 p= .823

ADHD combined subtype I score r= .138 r= .074 r= .064 r= .129 r = .085p= .109 p= .390 p= .458 p= .132 p= .323

H/I score r=−.009 r= .057 r= .066 r= .122 r = .063p= .919 p= .507 p= .442 p= .156 p= .464

Note. ADHD I = attention-deficit/hyperactivity disorder inattentive; ADHD H/I = attention-deficit/hyperactivity disorder hyperactivity/impulsivity; SRS = Social Reciprocity Scale.

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In the present study, in contrast with earlierstudies (Fernández-Jaén et al., 2011; Reiersenet al., 2007), even though SRS total and social sub-scale scores were higher in the ADHD combinedsubtype than in the ADHD H/I subtype, the differ-ence did not persist after the effects of age, gender,and CBCL social withdrawal scores were adjustedvia covariation. Even if intrusive behaviours fre-quently encountered in the ADHD H/I subtype,such as talking at inconvenient times and interrupt-ing the games of other children, are consideredinappropriate, they might be considered behavioursthat aim to establish social interaction. Additionally,such symptoms, which are common to the ADHDH/I subtype, might lead to low CBCL social with-drawal scores. The present findings suggest thatthe symptoms of hyperactivity/impulsivity might berelated with a higher level of social skills in associ-ation with less severe social withdrawal. In linewith this, it should be noted that symptoms ofhyperactivity/impulsivity are not associated with adecrease in the occurrence of ASSs, and thatthose with the ADHD H/I subtype have the samerisk of ASSs as those with the other ADHDsubtypes.

In the DSM-5, unlike the DSM-IV (APA, 1994),the differences between the subtypes of ADHD havebeen moderated, and a new nomenclature forADHD subtypes has been accepted as a terminologychange – “presentation” instead of “subtype” (APA,2013). It is known that ADHD may present in thesame individual by different subtypes, and the symp-toms of a subtype may be replaced by the symptomsof another subtype over time. The demonstration ofsymptom fluidity among the ADHD subtypes inDSM-5, and the alleviation of the boundariesbetween subtypes also support our notion thatthere is no significant difference in ASSs betweenthe ADHD subtypes. Social skills in those withADHD are associated with various factors.Santosh and Mijovic (2004) described two types ofsocial skill impairments and emphasised the impor-tance of distinguishing social impairment causedby disruptive behaviour disorders accompanied byADHD and social impairment caused by ASSs inchildren with ADHD. It was reported that eventhough the first type of social impairment, whichcould also be described as relationship difficulty, isassociated with environmental factors, social com-munication problems are associated with not onlylanguage and speech impairment, but also withrepetitive behaviours that are supposed to beunder the influence of innate deficits. It must beemphasised that the SRS used in the present studyevaluates social communication problems caused

by developmental problems rather than relationshipproblems caused by comorbid disruptive behaviourdisorders. Thus, the present study did not evaluatethe potential dissimilarities in CBCL aggressiveand delinquent subscale scores or disruptive behav-iour disorders in the three ADHD subtypes.However, this issue might be explored in a futurestudy.Some of the present study’s findings contradict

earlier reports, which might have been due to thefact that the sample groups were selected from differ-ent populations, such as clinic-based/population-based sample groups, there was a wide range ofADHD symptom severity (Ho, Todd, & Constan-tino, 2005; Reiersen et al., 2007), and differentassessment scales were used (Fernández-Jaén et al.,2011). A homogeneous, clinically referred samplemay limit the manifestation of correlation betweenADHD symptoms and SRS scores in the presentstudy. Moreover, it was reported that the SRS isone of the questionnaires that should be used toevaluate social reciprocity in children diagnosedwith ADHD, as it focuses on ASSs and is one ofthe instruments with acceptable levels of validity(Nijmeijer et al., 2008). Furthermore, intelligenceand neurocognitive evaluations were not performedin the present study, but two similar studies usedseveral Wechsler Intelligence Scale for Children(WISC-R) subscale scores for assessment (Nijmeijeret al., 2009; Reiersen et al., 2007) and some includedintellectual disability as the only exclusion criterion(Clark et al., 1999; Fernández-Jaén et al., 2011).Controlling the groups for intelligence might revealsignificant differences in results.Despite methodological limitations of the present

study, our results have some clinical implications.In our own clinical experience, children with a com-bination of ADHD symptoms and ASSs are gener-ally much more difficult to treat than children withADHD alone. This may be caused by the increasedrisk of developing comorbid disorders such as oppo-sitional defiant disorder and conduct disorder inchildren with ADHD and ASSs (Mulligan et al.,2009), which are considered to require a moredetailed evaluation and treatment. Furthermore,even if ADHD symptoms respond to treatment inchildren with ADHD and ASSs, the childrenrequire close monitoring for side effects (Santosh,Baird, Pityaratstian, Tavare, & Gringras, 2006).The present findings indicate the importance of eval-uating ASSs, planning, and implementing treatmentmodalities such as child-based social skills training,intensive parent training, and family-based interven-tions oriented for ASSs regardless of ADHDsubtypes.

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Conclusions

Our findings show that social withdrawal symptomsin those with ADHD might have effects on ASSs.However, no significant differences were found inASSs between the ADHD subtypes when this effectwas removed, and all ADHD subtypes had a similarrisk of ASSs. Moreover, in view of our results, itmay be hypothesised that ASSs are accompanied byADHD regardless of the symptoms of ADHD, andASSs may potentially form a subgroup of ADHD.

Author note

No research funding was involved and there were noconflicts of interest.

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