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WHATS KNOWN ON THIS SUBJECT: Studies examining the AUTHORS: Amelia Kotte, PhD,a Gagan Joshi, MD,b,c Ronna
prevalence and associated features of autistic traits (ATs) in Fried, EdD,a,b Mai Uchida, MD,a Andrea Spencer, MD,a
children with ADHD with exclusionary autism spectrum disorders K. Yvonne Woodworth, BA,a Tara Kenworthy, BA,a Stephen
suggest that children with ATs exhibit more severe social and V. Faraone, PhD,d and Joseph Biederman, MDa,b
aClinicaland Research Programs in Pediatric Psychopharmacology
interpersonal dysfunction reminiscent of the decits in children
with autism spectrum disorders. and Adult ADHD, Massachusetts General Hospital, Boston,
Massachusetts; bDepartment of Psychiatry, Harvard Medical
School and cAlan & Lorraine Bressler Center, Massachusetts
WHAT THIS STUDY ADDS: Our results suggest that ATs are General Hospital, Boston, Massachusetts; and dDepartments of
overrepresented in ADHD children when compared with control Psychiatry and of Neuroscience and Physiology, SUNY Upstate
subjects. They also suggest that the presence of ATs is associated Medical University, Syracuse, New York
with more severe psychopathology as well as more impaired KEY WORDS
interpersonal, school, family, and cognitive functioning. ADD, ADHD, attention decit disorder, attention-decit/
hyperactivity disorder, AT, autistic traits, autism traits,
comorbidity, social disability
ABBREVIATIONS
ADDattention decit disorder
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Twin, family, and linkage studies in- based on structured interview di- family, major sensorimotor handicaps,
dicate that attention-decit/hyperactivity agnoses. We did not exclude controls psychosis, autism, language barriers, or
disorder (ADHD) and autism spec- having other psychiatric disorders. an estimated IQ ,80 were exclusionary
trum disorders (ASDs) share a portion ADHD cases were identied from either for both ADHD and control participants.
of their heritable etiology.14 Genome- a major academic medical center, in Parents provided written informed con-
wide association studies found rare which we selected ADHD subjects from sent, and children and adolescents pro-
copy number variants shared between consecutive referrals to its pediatric vided written assent. The institutional
the 2 disorders,5 raising the possibility psychopharmacology clinic and from review board at MGH approved the study.
that some children with ADHD may a major health maintenance organiza-
manifest symptoms of autism even in tion, in which ADHD subjects were se- Assessment Procedures
the absence of a diagnosis of ASD. Re- lected from consecutively ascertained Psychiatric assessments relied on the
cent studies have identied that pediatric clinic outpatients. Healthy Kiddie Schedule for Affective Disorders
symptoms of autism or autistic traits controls were ascertained from out- and SchizophreniaEpidemiologic Ver-
(ATs) appear in 20% to 30% of children patients referred for routine physical sion,16,17 conducted directly and in-
with ADHD4,6,7 and that such children examinations to its pediatric medical dividually with the mothers and the
are more impaired than other children clinics at each setting identied from children. For children aged ,12 years
with ADHD, particularly in the domains their computerized records as not who could not provide reliable self-
of interpersonal communication and having ADHD. Further information on reports of their symptoms, interviews
empathy. However, these ndings re- the ascertainment of the sample have were conducted with their mothers
quire replication. been published in detail elsewhere.1013 (indirect interviews). Combining data
The main aim of the current study was to In previous articles,14,15 we reported from direct and indirect interviews, we
examine the prevalence and correlates that the rates of other psychiatric dis- considered a diagnosis positive if it
of ATs in youth with ADHD by using data orders in the control sample were low was endorsed in either interview. So-
from an existing, large-scale sample of and consistent with expectations from cial class was assessed by using the
referred youth with and without ADHD in population studies. Hollingshead and Redlich scale18
whom the diagnosis of autism was ex- Participants had a mean 6 SD age of Interviews were administered by highly
clusionary. We hypothesized that ATs 11.3 6 3.2 years, were 99% white, and
trained and supervised psychome-
would be prevalent in children with had a mean socioeconomic status
tricians, blinded to referral source or
ADHD and that their presence would be (SES) score of 1.7 6 0.9. The sample
diagnostic status (ADHD or control).
associated with higher levels of mor- included 274 children (52%) who
Based on 500 assessments from
bidity and disability. reported that he or she was tutored
interviews of children and adults, the
(ADHD: 172 [61%]; controls: 54 [22%]),
median k coefcient of agreement be-
METHODS repeated a grade (ADHD: 69 [25%];
tween a psychometrician and an ex-
controls: 18 [7%]), or took a special
Subjects perienced clinician was .98.
class (ADHD: 74 [26%]; controls: 5
Subjects were youth of both genders [2%]). Of the control children with ac- We used an empirically derived prole
derived from longitudinal, case-control ademic difculty (27% [n = 65]), 34% from the Child Behavior Checklist
family studies conducted at Massa- (n = 22) met DSM-III-R criteria for $1 (CBCL) to dene ATs (CBCL-AT) by using
chusetts General Hospital (MGH).8,9 psychiatric disorder versus 28% (n = a cutoff of 195 from the combined
These studies included participants 49) of those without academic difculty T scores of the withdrawn, social prob-
aged 6 to 18 years with (n = 280) and (n = 177). Of the ADHD children with lems, and the thought problems sub-
without (n = 242) Diagnostic and Sta- academic difculty (75% [n = 209]), scales19 that correctly classied 78% of
tistical Manual of Mental Disorders, 81% (n = 169) met DSM-III-R criteria for all subjects with ASD from a psychiat-
Revised Third Edition (DSM-III-R), ADHD $1 psychiatric disorder versus 73% (n rically referred sample with and with-
ascertained from pediatric clinics at = 52) of those without academic dif- out ASD. Two subscales were created
a large health maintenance organiza- culty (n = 71). These numbers suggest from the CBCL by summing the anxiety/
tion and referrals to a pediatric psy- that the presence of a psychiatric ill- depression, aggression, and attention
chopharmacology clinic. Within each ness may account for the increased scales (severe dysregulation: sum of T
setting, we selected non-ADHD normal prevalence of academic functioning scores $210; decient emotional self-
controls from pediatric medical clinics difculties. Adoption, unavailable nuclear regulation: sum of T scores of 180210).20
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P = .03), hyperactivity (OR: 8.9, P = .001; mood disorders, x 2 = 132.5, P , Decits in Emotion Regulation and
.04), ghts with peers (OR: 6.8, P = .001; multiple anxiety disorders, x2 = Social Disability
.002), and rejection by peers (OR: 24, 63.9, P , .001; language disorders, x2 = ADHD + CBCL-AT participants had a sig-
P = .003) (Fig 1B). 25.5, P , .001; elimination disorders, nicantly higher prevalence of the
x2 = 40.5, P , .001; and substance use CBCL severe emotional dysregulation
Pregnancy, Delivery, and Infancy prole than both ADHD and control
disorders, x2 = 20.9, P , .001). Com-
Complications participants (controls: 0%; ADHD:
pared with ADHD participants, ADHD +
ADHD + CBCL-AT mothers reported more 6.57%; ADHD + CBCL-AT: 72.73% [all P ,
CBCL-AT participants had a signicantly
infections during pregnancy (ADHD + .001]). In contrast, ADHD and ADHD +
higher prevalence of disruptive behav-
CBCL-AT: 28%; ADHD: 11%; controls: 8%; CBCL-AT participants did not differ from
iors (OR: 3.7, P = .001), mood disorders each other in the prevalence of the
x2[4] = 10.7, P = .001), switching for-
(OR: 5.4, P , .001), multiple anxiety CBCLdecient emotional self-regulation
mulas during their childrens infancies
disorders (.2) (OR: 3.7, P , .001), and prole, which assesses a lower level
(ADHD + CBCL-AT: 25%; ADHD: 9%; con-
language disorders (OR: 2.6, P = .01) of emotional dysregulation compared
trols: 6%; x2[4] = 13.6, P , .001), and
(Fig 2A). with the CBCLsevere emotional dys-
described their infants as stiffened
ADHD participants with and without ATs regulation prole. However, both groups
during infancy (ADHD + CBCL-AT: 25%;
had a signicantly higher prevalence
ADHD: 5%; controls: 1%; x 2[4] = 32, P , had signicantly more impaired scores
of the CBCLdecient emotional self-
.001) (Table 2). on each CBCL clinical and composite
regulation prole than control sub-
scale compared with controls (all P , jects (controls: 1.32%; ADHD: 38.89%;
Patterns of Psychiatric Comorbidity .001). ADHD + CBCL-AT participants had ADHD + CBCL-AT: 20.45% [all P , .001])
ADHD participants with and without ATs signicantly more impaired scores on (Fig 3A).
had signicantly higher prevalence of all CBCL clinical and composite scales
all comorbid psychiatric disorders than ADHD participants, including Social Functioning
versus control subjects (ie, disruptive scales that were not used to dene ATs Both ADHD groups had a signicantly
behavior disorders, x2 = 142.4, P , (all P , .001) (Fig 2B). higher prevalence of social disability
TABLE 2 Pregnancy and Infancy Characteristics (Adjusting for Age and SES)
Characteristic Controls (n = 225) ADHD (n = 188) ADHD + CBCL-AT (n = 40) Test Statistic P
Pregnancy characteristics
Excessive nausea 25 (11) 40 (21)a 10 (25)a x 2(4) = 10.4 .03
Infection 19 (8) 20 (11) 11 (28)a,b x 2(4) = 10.7 .03
High blood pressure 24 (11) 39 (21)a 11 (28)a x 2(4) = 14.1 .007
Accidents 2 (1) 9 (5)a 4 (10)a x 2(4) = 11 .003
Family problems 20 (9) 39 (21)a 12 (30)a x 2(4) = 21.2 .003
Medications 47 (21) 58 (31)a 18 (45)a x 2(4) = 13.8 .008
Smoking (3 mo at gestation) 16 (7) 27 (14)a 9 (23)a x 2(4) = 22.2 .002
Infancy characteristics
Switch formulas 13 (6) 16 (9) 10 (25)a,b x 2(4) = 13.6 .009
Crying infant 29 (13) 48 (25)a 12 (30)a x 2(4) = 13.7 .008
Stiffened infant 2 (1) 9 (5)a 10 (25)a,b x 2(4) = 32.0 ,.001
Data are presented as n (%).
a Compared with the control group.
b Compared with the ADHD group.
as dened by the SAICA (all P , .01) sures of school behavior, spare time ADHD + CBCL-AT participants had sig-
than control subjects. However, rates problems, activities and problems with nicantly more impaired scores than
were signicantly higher in ADHD + peers, and problems with siblings and ADHD participants on the CBCL social
CBCL-AT participants versus ADHD parents (all P , .001) (Fig 4A). A sim-
and total competence scales (Fig 4B).
ilar pattern was observed when ana-
participants (controls: 6.77%; ADHD:
lyzing ndings from the CBCL social Cognitive Findings
34.94%; ADHD-AT: 68.57%) (Fig 3B).
functioning scales, which consist of
ADHD + CBCL-AT participants had sig- the activities, social, and total compe- ADHD + CBCL-AT participants scored
nicantly more impaired SAICA scaled tence scales. Of these, only the social signicantly worse than ADHD partic-
scores than ADHD participants in mea- problems scale was used to dene ATs. ipants on the WISC-R Full IQ (ADHD +
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FIGURE 2
Additional related symptoms in the ADHD, ADHD + CBCL-AT, and control groups. A, Prevalence of psychiatric disorders (lifetime). B, CBCL prole. aCompared
with the control group. bCompared with the ADHD group. *P , .05; **P , .005; ***P , .001.
CBCL-AT: 101.96 6 14.90; ADHD: 108.54 6 and interpersonal decits. These re- ordered movement kinetics observed
12.55), freedom from distractibility sults are highly consistent with those of in Aspergers syndrome3336 and what
(ADHD + CBCL-AT: 92.71 6 16.11; ADHD: 3 previous reports4,6,7 that examined has been previously described in chil-
100.28 6 14.35), block design (ADHD + ATs in children with ADHD. dren with the neuropsychological pro-
CBCL-AT: 10.61 6 3.82; ADHD: 12.70 6 The current study found that ADHD le of decits in attention, motor
3.48), digit symbol scaled scores (ADHD + children with a positive AT prole do not control, and perception.3739
CBCL-AT: 8.86 6 3.99; ADHD: 10.57 6 differ from other ADHD children in the Also consistent with the extant litera-
3.13) (all P , .05), and Wisconsin Card core symptoms of ADHD, but they do ture are our ndings on the Kiddie
Sorting Test perseverative errors sub- present with a more severe clinical Schedule for Affective Disorders and
test (T scores: ADHD + CBCL-AT: 28.86 6 picture when additional and ADHD- SchizophreniaEpidemiologic Version
16.88; ADHD: 17.71 6 12.53; controls: relevant symptoms in the diagnostic showing that ADHD + AT children
15.84 6 10.92) (Fig 5). criteria are considered, including exhibited signicantly higher rates of
clumsiness, messiness, and social dif- comorbid psychiatric disorders versus
DISCUSSION culties with peers. Because these ADHD children, especially in the do-
Our ndings revealed that ATs are symptoms are commonly reported in main of disruptive behavior disorders,
present in children with ADHD, and their children with ASDs, it is possible that which included the diagnoses of con-
presence heralds a signicantly more they reect ASD tendencies as well as duct and oppositional deant disor-
compromised clinical presentation ADHD ones.2932 Of note, the presence of der.4,6 Also reecting the impairment
characterized by higher rates of psy- clumsiness in children with ADHD and observed in children with ASDs40,41
chopathological, neuropsychological, ATs may be closely related to the dis- is the nding that ADHD + CBCL-AT
FIGURE 4
Social functioning in the ADHD, ADHD + CBCL-AT, and control groups. A, SAICA individual item scores. B, CBCL social functioning scales. aCompared with the control
group. bCompared with the ADHD group. *P , .05; **P , .005; ***P , .0001.
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FIGURE 5
Neuropsychological functioning in the ADHD, ADHD + CBCL-AT, and control groups. A, WISC-R and Wide Range Achievement Test (WRAT). B, WISC-R. aCompared with
the control group. bCompared with the ADHD group. *P , .05; **P , .005; ***P , .0001.
children were more likely to have children. These ndings suggest im- higher rates of mood, anxiety, dis-
a positive CBCLsevere dysregulation pairments in executive functioning ruptive, and substance use dis-
prole versus ADHD children, in- and cognitive exibility, a pattern ob- orders,52 and school failure, school
dicating that these children experience served in other populations positive dropout, and delinquent offenses53 in
very severe behavioral, emotional, and for ATs,44,45 as well as in children with ADHD + AT children is particularly
educational problems.20,42 The high ASDs.4648 worrisome.
rates of mood dysregulation in the Also consistent with the extant litera- Our ndings that ADHD children with
ADHD + CBCL-AT children are also con- ture are our ndings showing that ADHD ATs had a higher rate of pregnancy
sistent with an emerging body of lit- + AT children were more likely than and infancy complications than other
erature documenting high rates of ADHD children to ght with and be ADHD children could suggest that
mood disorders in children with rejected by peers, to have more school prenatal and perinatal complications
ASDs.43 Further research is needed to behavior problems, more difculties alone or in combination with genetic
better understand the role ATs confer utilizing their spare time, and more risk factors could account for the
on emotion regulation in children with problems with siblings. Considering the development of ATs in some children
ADHD. well-established evidence that social with ADHD. These ndings are in-
ADHD + CBCL-AT children also had sig- difculties are a core component of triguing in light of previous reports
nicantly lower Full IQ, freedom from ASDs,4951 our ndings also suggest yielding support for the role of ma-
distractibility, block design, and digit that the social disability observed in ternal infection during pregnancy5457
symbol WISC-R scores as well as dif- the ADHD + CBCL-AT group may be and the behavioral characteris-
ferences in perseverative errors on the more a reection of underlying ATs tics of infants later classied with
Wisconsin Card Sorting Test than ADHD than the presence of ADHD itself. The ASDs.58
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Autistic Traits in Children With and Without ADHD
Amelia Kotte, Gagan Joshi, Ronna Fried, Mai Uchida, Andrea Spencer, K. Yvonne
Woodworth, Tara Kenworthy, Stephen V. Faraone and Joseph Biederman
Pediatrics 2013;132;e612; originally published online August 26, 2013;
DOI: 10.1542/peds.2012-3947
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