Abstract
Autism spectrum disorder (ASD) and ADHD are neurodevelopmental disorders with high rates of co-occurrence (Leitner, 2014). However, prior to the introduction of Diagnostic and Statistical Manual of Mental Disorders (5th ed.; DSM-5; American Psychiatric Association, 2013), the diagnosis of ASD precluded that of ADHD. Thus, research differentiating those with ASD, ADHD, or comorbid diagnoses has been relatively sparse. The handful of neurocognitive investigations adhering to the DSM-5 clinical classifications has suggested greater attention dysfunction among children with ASD + ADHD and ADHD relative to those with ASD alone, providing evidentiary support for distinct diagnoses. Colombi and Ghaziuddin (2017) reported elevated caregiver-reported symptoms of inattention among children with both ASD + ADHD as compared with those with ASD only, although no group effects were found in executive functions (cognitive flexibility, problem solving). Ghaziuddin’s findings were in part consistent with Lundervold et al.’s (2016) results, which showed children with ASD + ADHD as well as those with ADHD had increased response variability and inconsistency on the Conners’ Continuous Performance Test–Second Edition (CPT-II, Conners & Staff, 2004). Collectively, these findings suggest greater challenges in attentional focus and vigilance in those with ASD + ADHD and ADHD, as compared with ASD alone.
Despite these noted distinctions in attention functioning across children with ADHD, ASD, or ASD + ADHD, these developmental disorders are commonly associated with greater risk of social impairment. Children with ADHD or ASD are more likely to experience greater rates of peer rejection and challenges in developing relationships, albeit the underlying social cognitive factors that contribute to observed functional impairments differ (for a review see, Leitner, 2014). Relative to children with ASD alone, those with ASD + ADHD show more severe deficits in social and adaptive skills (Leitner, 2014; Rao & Landa, 2014), suggesting the additional attention and behavioral regulation difficulties associated with ADHD diagnosis may uniquely contribute to the day-to-day functional deficits.
Currently, however, the specific ADHD symptomatology (inattention, hyperactivity/impulsivity) that contribute to social functional difficulties across the neurodevelopmental disorders remains unclear, although identifying attention correlates may aid in developing targeted treatments, mitigating subsequent risk for chronic or more severe impairment (Nijmeijer et al., 2008). Notably, current medication and behavioral treatment of ASD are largely symptom specific. For instance, research show approximately 6% of a nationally representative sample of youth with ASD were prescribed stimulants despite not fully meeting ADHD diagnosis (Frazier et al., 2011), a practice that has also raised clinical concerns with potential worsening of stereotyped/repetitive behaviors and inadequate treatment efficacy.
In a similar vein, to our knowledge, there is a lack of research comparing the efficacy of behavioral interventions for those with ADHD, ASD, or both diagnoses particularly when applying DSM-5 diagnostic classifications, despite frequent clinical recommendations for social skills interventions (for a review see Antshel, Zhang-James, & Faraone, 2013). Interestingly, as reviewed in Antshel and Russo (2019), the positive effects of social skills training for youth with ADHD and ASD + ADHD are not well-supported by empirical evidence, as compared with those with ASD alone, suggesting the need for targeted treatments as a function of the neurodevelopmental disorder. Alternatively, other behavioral interventions may yield more progress in social functioning among individuals with specific attention profiles (e.g., inattention vs. hyperactive/hyperactive presentation). For example, interventions addressing executive skills, including inhibitory control, problem solving, and organization/planning in youth (for a review see Diamond & Lee,2011) may be essential for those who experience social dysfunction secondary to hyperactivity/impulsivity, whereas other modalities such as mindfulness training may improve social functioning by facilitating attention regulation (Felver, Tipsord, Morris, Racer, & Dishion, 2017). Behavioral modification interventions that incorporate caregivers and potentially teachers may broadly promote self-regulation skills by use of reinforcement contingencies, which in turn may reduce social disinhibition and enhance self-awareness (Hinshaw, Arnold, & MTA Cooperative Group, 2015). In effect, to better ascertain the interventions that may promote social skills more effectively among those with ADHD, ASD, or both diagnoses, systematic research directed toward identifying cognitive and attentional profile (i.e., inattention vs. hyperactive/impulsive symptoms) correlates of social functioning is warranted.
Toward this end, this study aimed to determine the associations between symptom severity of ADHD subtypes (inattention, impulsivity/hyperactivity) with social dysfunction across youth with ADHD, ASD, and ASD + ADHD. Specifically, we included a retrospective review of medical records, including neuropsychological data characterizing intellectual, attention, and social functioning. The data were obtained through a multidisciplinary evaluation within the Department of Psychiatry at the authors’ institute. In contrast to prior investigations, which inconsistently applied behavioral, cognitive, or informant questionnaires, a mixture of objective tests and respondent-ratings of attention and social functioning were used to index these domains. Specifically, patients ranging in age from 7 to 18 years and diagnosed with ADHD, ASD, or ASD + ADHD completed objective measures of intellectual (Wechsler intelligence tests), attention (CPT-II), and social functioning, as well as assessment with the Autism Diagnostic Observation Schedule–Second Edition (ADOS-2, Lord et al., 2012). Caregivers also completed rating scales to assess day-to-day attention, social and behavioral functioning. We focused on group differences across tasks, and subsequently, the associations between objective- and caregiver-report measures of inattention and impulsivity and social impairment. Our primary hypothesis was that we would see greater impairment in objective- and caregiver-report attention measures among ADHD and ASD + ADHD groups, relative to children with ASD alone. Secondarily, we hypothesized that attention measures would be uniquely associated with social functioning among those with ADHD and ASD + ADHD groups, which would lend more evidence that affected youth may benefit from different treatment methods than those with ASD alone.
Method
Participants
This study consisted of a retrospective review of medical records from patients referred for neuropsychological testing in a multidisciplinary clinic for ASD within the Department of Psychiatry at the authors’ institute from 2013 to 2017. Based on caregiver report, 64.9% had a prior diagnosis of ADHD and 18.1% with autistic disorder/Asperger’s disorder/pervasive developmental disorder per Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; American Psychiatric Association, 2000), provided by an external psychiatrist or psychologist, and 13.8% had no prior diagnoses. Approximately 19.1% of patients reportedly had a prior diagnosis of ASD, with half of these individuals diagnosed by an external psychiatrist and the other half provided the designation of ASD through school. Following our assessment, clinical diagnosis was based on the consensus of licensed psychologists and psychiatrists incorporating test results, clinical observations, and clinical interview with the patient and parents, in accordance with the DSM-5 classification criteria.
Following the multidisciplinary evaluation, 27 patients were diagnosed with ADHD (20 males, Mage = 10.23 years, SD = 2.58, range = 7-17 years), 23 with ASD (21 males, Mage = 11.37 years, SD = 3.51, range = 7-18 years), and 44 with ASD + ADHD (39 males, Mage = 10.78 years, SD = 2.39, range = 7-18 years) based on DSM-5 diagnostic classification. Of note, age at testing did not reach significance across groups. Analysis of demographic data between each group did not show significant differences. Table 1 provides patient’s characteristics. As can be seen, ADHD and ASD + ADHD group had similar proportion of inattentive (ADHD = 22.22%, ASD + ADHD = 29.54%), hyperactive/impulsive (ADHD = 3.70%, ASD + ADHD = 2.27%), and combined subtypes (ADHD = 62.96%, ASD + ADHD = 61.36%). Three of the ADHD patients and three children with ASD + ADHD were diagnosed with the “other specified” classifier, as these children had prior diagnosis unspecified or “not otherwise specified” ADHD and were medically treated, but caregivers reported functional impairment in only one setting. The proportion of stimulant medications prescribed for ADHD concerns was greater among ADHD and ASD + ADHD groups relative to ASD patients (χ2 = 16.88, p < .001), but diagnostic groups were comparable on other psychotropic medication use for anxiety, mood, or disruptive behavioral concerns. Exclusionary criteria for this study include significant history of neurological disorders, including brain injury, seizures, and central nervous system disorders. Data of individuals with intellectual disability were excluded in this study, as several patients were administered a different abbreviated measure of intellectual functioning (e.g., Stanford-Binet) with a lower floor in part due to reduced tolerance for testing and were unable to complete the CPT-II due to behavioral regulation difficulties. This retrospective study was approved by the institutional review board of the authors’ affiliated university.
Participants’ Characteristics, Mean Performance Across Cognitive Testing, and Mean Caregiver Ratings on Standardized Inventories.
Note. ASD = autism spectrum disorder; DSM-IV = Diagnostic and Statistical Manual of Mental Disorders (4th ed.); SRS = Social Responsiveness Scale; ADOS-2 = Autism Diagnostic Observation Schedule–Second Edition.
Approximately 33% of the ADHD group met diagnostic criteria for comorbid diagnosis of anxiety, as compared with 24% of the ASD group, and 27% of the ASD + ADHD patients. About 18% of the ADHD group also met criteria for a diagnosis of a mood or depressive disorder relative to 13% of ASD patients and 25% of the ASD + ADHD group. No significant associations between diagnostic group and age with anxiety or mood disorder were observed.
Measures
Intellectual functioning
Patients completed the Wechsler Intelligence Scale for Children–Fourth/Fifth Edition (WISC-IV/V; Wechsler, 2003, 2014) or Wechsler Abbreviated Scale of Intelligence–Second Edition (WASI-II; Wechsler, 2011). WASI-II intellectual estimate is comprised of verbal comprehension and visual reasoning subtests. To maintain an analogous intellectual estimate, of the patients who completed the WISC-IV/V, the General Ability Index (GAI) was considered an estimate of intellectual functioning, as this composite incorporates verbal reasoning and perceptual or visual-spatial reasoning subtests, but excludes indexes of cognitive proficiency (working memory, processing speed; Wechsler, 2014), similar to the full-scale intellectual quotient provided by WASI-II. No significant group effect was observed in regard to the proportion of patients who were administered a WISC versus WASI-II.
Attention functioning
Patients completed the CPT-II (Conners & Staff, 2004), a computerized measure of sustained attention functioning, vigilance, and response inhibition. Response accuracy and speed are recorded, yielding an age and gender norm-referenced T score for omission errors (with higher scores a marker of inattention), commission errors (with higher scores indicating greater impulsivity), and response variability (higher scores indicate greater variability in responding consistent with poor sustained attention). Caregivers also completed caregiver-report version of the Conners Third Edition (Conners 3; Conners, 2008), a measure of day-to-day behavioral and attention functioning. Ratings yield an age and sex norm-reference T score for ADHD Inattentive Symptoms and ADHD Hyperactivity/Impulsivity, in accordance to Diagnostic and Statistical Manual of Mental Disorders (4th ed.; DSM-IV; American Psychiatric Association, 1994). Higher T scores reflect more difficulties within the respective domain. Conners 3 inventories and the CPT has variable (low to moderate) predictive validity when considered independently and as a function of comparison groups (e.g., those with ADHD vs. other psychiatric ailments), resulting with variable sensitivity and specificity rates across investigations (for a review on psychometric background, see Conners, 2008; Hall et al., 2016).
Social functioning
Caregivers completed the Social Responsiveness Scale (SRS; Constantino & Gruber, 2005) as a measure of deficits in social functioning, typically associated with ASD. SRS total composite consists of index scores in the following domains: social awareness, social cognition, social communication, social motivation, and restrictive/repetitive behaviors (RRB). Ratings were converted to age and sex norm-referenced T scores. Prior research as reviewed in Duvekot, van der Ende, Verhulst, and Greaves-Lord (2015) has shown relatively good convergent validity of SRS with other ASD screening measures, albeit insufficient as a diagnostic tool alone.
Of the patients, a total of 23 patients with ADHD, 21 with ASD, and 33 with comorbid diagnosis completed the ADOS-2 (Lord et al., 2012), a semi-structured assessment of interactive play, communication, and RRB that has well-documented diagnostic validity, particularly when compared with nonclinical comparison samples (Kamp-Becker et al., 2013; Maddox et al., 2017). ADOS-2 total raw score comprised of scores obtained for Social Affect and RRB domains. Elevated SRS T scores and ADOS-2 total raw score reflect greater social impairment within domains.
Data Analysis
Multivariate analysis of variance was computed to assess group differences in intellectual, attention, and social functioning. Bivariate Pearson correlations were employed to examine associations between objective testing (CPT-II omission, commission, variability T scores) and parent-report attention measures (Conners 3 DSM-IV ADHD inattentive type T score, ADHD hyperactivity/impulsivity type T score) with social measures (SRS total T score, ADOS-2 social affect raw score, ADOS-2 RRB raw score) to confirm hypothesized relationship across domains, as a function of diagnostic group. Multiple hierarchical linear regressions were used with intellectual functioning index as factors to control in Step 1, and attention measures as Step 2 (CPT-II omission and commission T scores, and Conners-3 DSM-IV ADHD inattentive and hyperactivity/impulsivity T scores). Of note, age was not included as a covariate in regression analyses, as correlations between ages with cognitive, attention, or social indexes did not reach significance and no group effect of age was observed. Collinearity diagnostics were monitored during regression analyses with variance inflation factors (VIFs) < 5, mainly due to high correlation between CPT-II Omission and Variability (r = .65, p < .001); however, given the domains index different attention functions, both were included in regression models. Of note, data analyses were completed both with and without the patients with the diagnosis of ADHD, other specified. However, the following results remained significant; thus, their data were included in final results below.
Results
Group Differences in Intellectual, Attention, and Social Functioning Measures
Table 1 outlines group means across intellectual, attention, and social functioning measures. Group effects were found on caregiver report of attention functioning (F = 7.05, p = .001), but not across CPT-2 indexes. In contrast, a group effect was observed across the following ADOS-2 subscales/composites: total score (F = 13.29, p < .001), social affect (F = 6.07, p = .004), and RRB (F = 7.97, p = .001), with ADHD group yielding lower raw scores compared with other groups (ps < .02). There were no group differences on parent ratings from the SRS.
Correlational Analyses Between Social and Attention Functioning Indexes
Among the ADHD group, greater social impairment as reflected by elevated SRS total was associated with greater parent-reported inattentive (r = .61, p = .001) and hyperactive/impulsive symptoms (r = .70, p < .001), and higher ADOS-2 total score was correlated with more variability (r = .45, p = .032). Among those with ASD alone and ASD + ADHD, SRS total was associated with elevated caregiver-reported inattention problems (ASD: r = .44, p = .037; ASD + ADHD: r = .60, p < .001) and hyperactivity/impulsivity (ASD: r = .48, p = .02; ASD + ADHD: r = .44, p = .003). No correlations were observed with ADOS-2 total and attention measures among ASD and ASD + ADHD groups.
Regression Analyses
In regard to objective testing of social functioning, across diagnostic groups, attention measures were not significantly associated with social difficulties, as measured by ADOS-2 total score.
In contrast, among ADHD and ASD + ADHD groups, attention measures accounted for approximately an additional 48% and 40% of the variance in caregiver report of social functioning (SRS total score). For the ADHD group, caregiver report of hyperactivity/impulsivity was the strongest predictor (B = .62, t = 2.89, p = .007), whereas caregiver report of inattentiveness was not a significant determinant. The opposite pattern was found among those with ASD + ADHD, caregiver report of inattentiveness was the strongest correlate (B = .51, t = 3.25, p = .002), whereas ratings regarding hyperactive/impulsive symptoms was not a significant predictor. Attention indexes were not significant correlates among ASD patients (see Table 2).
Independent Associations Between Attention Functioning Measures and Caregiver-Reported Social Impairment Across Patients With ADHD, ASD, and ASD + ADHD, After Controlling for Intellectual Functioning.
Note. Standardized betas and t statistics (within parentheses) are reported unless otherwise indicated. Social impairment was indexed by caregiver ratings on the Social Responsiveness Scale. ASD = autism spectrum disorder; CPT-II = Continuous Performance Test–Second Edition.
p < .01.
Discussion
The primary goal for this retrospective review was to examine extent and nature of attentional correlates of social dysfunction across youth diagnosed with ADHD, ASD, or ASD + ADHD. Two main findings were observed. First, there was a main group effect found for ADHD symptomatology reported by parents (inattention, hyperactivity/impulsivity) but not on objective tests of attention; in contrast, a group effect was observed in patients who underwent objective measures of autistic symptomatology but not on parent-reported social measures. Second, results showed ADHD symptomatology differentially predicted parent-reported social impairment based on caregiver reports for patients with ADHD and ASD + ADHD, but not among those with ASD alone. Collectively, our findings highlight the importance of using a combination of objective tests and respondent-rating inventories of attention and social functioning in diagnostic and treatment considerations.
In this study, group effects were observed on caregiver-report inventories of ADHD symptoms but not on patients’ performance on objective measures of attention regulation (CPT). Findings contribute to ongoing concerns of using CPT or other objective attention regulation tests as a standalone diagnostic tool, particularly when differentially assessing ADHD versus other developmental disorders (Ogundele, Ayyash, & Banerjee, 2011). These findings may be due to low specificity and sensitivity rates (Edwards et al., 2007), as well as low cognitive demands of the task (Berger & Cassuto, 2014). It should be noted that our patients were on medication during their assessment, which may have contributed to their relatively strong performance on these measures. In addition, the patients included for this report were tested in a clinic environment with a trained and licensed psychometrist with minimal distractors. Thus, patients may have demonstrated better attentional control due to the structured setting. Consistent with this, Berger and Cassuto (2014) propose that increasing environmental distractors and cognitive demand of a CPT may improve its discriminative sensitivity and ecological validity.
Group effects were observed on structured testing of social skills and symptoms related to ASD (i.e., ADOS-2) but not on caregiver-inventories of social functioning (e.g., SRS). It is possible that dysregulated behaviors and hyperactivity observed in children with ADHD may be perceived as part of the constellation of ASD in less structured settings, resulting in elevated caregiver ratings among the ADHD group. In addition, structured assessment and observations such as ADOS provide better insight regarding social skills when distractors are limited. Thus, while the SRS may have relatively strong sensitivity to distinguish those with ASD versus typically developing children, this inventory may not be particularly sensitive to discriminate those with ASD versus other developmental disorders that also have a high risk for social dysfunction, such as ADHD (Charman & Gotham, 2013). ADOS-2 demonstrates relatively high discriminant validity for individuals with ASD versus typically developing children, however, specificity of this measure varies significantly as a function of comparison group, sex, and age (e.g., other psychiatric illness; for a review see, Wigham et al., 2019). Although our results indicate ADOS-2 was more sensitive in distinguishing those with ASD versus ADHD alone, no association between ADOS-2 performances with chronological age was observed contrary to Wigham et al. (2019). In brief, findings add to growing consensus for the need to better understand the psychometric properties of screening and diagnostic tools for ADHD and ASD, and importance of applying both clinic-based tests and informant questionnaires to assess for cognitive and social functioning across contexts.
Different configurations of attention problems were associated with greater social dysfunction, as measured by the SRS, among ADHD versus ASD + ADHD patients despite similar proportion of ADHD subtypes across groups. In contrast, no association between social and attention domains were observed among those with ASD alone. Findings partially support prior investigations, indicating increased ASD symptoms with greater hyperactive/impulsivity symptomatology among children with ADHD (Green et al., 2015). Among children with ADHD, hyperactive and/or impulsive behaviors are likely to result in difficulties in social setting, including communication and cognition. Specifically, hyperactivity and impulsivity is characterized by engagement in rule violations, intrusive behaviors, and aggression (for a review, see Nijmeijer et al., 2008), which in turn elicits negative responses from others, leading to a negative reputation (Hoza, 2007) and perpetual bidirectional negative social experience. Among children with ASD + ADHD, inattention coupled with slightly elevated rate of anxiety in our sample may contribute to more perceived withdrawn behavioral or low social motivation, thus contributing to overall social dysfunction (Hodgens, Cole, & Boldizar, 2000; Maedgen & Carlson, 2000). Notably, given our relatively small diagnostic groups, we focused analysis on social impairment rather than select domains (e.g., social cognition, awareness, etc.). Thus, it should be highlighted that it is unclear whether specific ADHD symptoms were more strongly correlated to specific social problems in our groups (e.g., elevated hyperactivity/impulsivity is related to more impairment in social cognition, and inattention is associated with more severe problems with social motivation). Future research with larger sample of patients with ADHD alone and ASD + ADHD could consider the relationship between specific attention symptoms and specific ASD symptoms.
Inattention was not a significant predictor for social dysfunction among those with ADHD alone, although the proportion of patients with inattentive subtype was similar across the ADHD and ASD + ADHD groups. Given the majority of both diagnostic groups met the ADHD combined subtype, it is possible that the predictive power was not best captured among patients given the small subsamples of ADHD inattentive type. Furthermore, we did not assess the different classes of ADHD medication that was used across diagnostic groups, which may have contributed to differential improvement in concentration versus behavioral regulation. Moving forward, in subsequent investigations, larger clinical samples with different ADHD subtypes will be needed to further determine whether these findings vary as a function of ADHD subgroups.
Notably, no significant associations were observed between total score on ADOS-2 and attentional measures across the clinical groups. It is possible that the restricted range in ADOS-2 raw scores may contribute to underestimation of associations. In addition, whereas ADOS-2 consists of structured tasks, patients may show greater social difficulties in day-to-day settings, when interactions and activities are less predictable and structured, more inclusive of social members (e.g., larger group of children), and may require more cognitive flexibility (i.e., ability to switch tasks quickly). Finally, it should also be noted that SRS and ADOS-2 offers an estimate of social impairment based on gross deficits in social communication, cognition, motivation, awareness, and restricted interests or repetitive behaviors, but does not provide qualitative description of social deficits (e.g., poor social cognition may result in passivity in resolving peer conflict or alternatively, aggressive behaviors). Thus, although SRS T score and performance on the ADOS-2 may be a proxy of gross social impairment, more research applying respondent inventories and objective tests to tap social constructs would elucidate the pathways in which attention/behavioral dysfunction may affect interpersonal skills, and accordingly, focused intervention that may more effective among children with ADHD, ASD, or ASD + ADHD.
It is important to note that our study did not include those with intellectual disability in part due to differences in the adapted test battery administered (e.g., abbreviated Stanford-Binet), comprehension of task instructions, and task compliance with the CPT-II. As such, our clinical sample may not represent the full spectrum of ASD and/or ADHD but rather relatively higher cognitive functioning subgroups. Future research should consider including participants with a wider range of intellectual functioning to better delineate whether our findings are consistent across all individuals with ASD, or specific to higher cognitive functioning youth.
Moreover, a relatively elevated proportion of our clinical sample presented with a mood or anxiety disorder that may have differentially contributed to their observed and caregiver-reported social aberrations. Although the proportion of patients across our clinical groups (ADHD, ASD, ASD + ADHD) were comparable, it is possible that the psychiatric comorbidities affect social skills under different mechanisms for these neurodevelopmental disorders. In the future, to better elucidate the additional effect of emotion functioning on social dysfunction across these diagnostic groups, comprehensive self- and caregiver-report inventories to assess mood and anxiety symptomatology should be considered.
This study has several limitations given the nature of how the data were collected (i.e., retrospective clinic review), which should be considered in prospective investigations. Our estimate of intellectual functioning was comprised of different Wechsler tests, largely due to limitations with data collection within a multidisciplinary clinic, including managing time constraints (e.g., allotted time for the assessment) and patients’ engagement with a flexible battery approach. Future studies should also include teacher-report inventories in an effort to better discern whether ADHD symptoms or social dysfunction are observed across settings. Finally, longitudinal research would be important to better understand whether cognitive factors continue to pose as risk factors to social adjustment consistently across age across youth with ASD and/or ADHD, or vary across maturational periods.
In brief, our retrospective study involving clinic data provide support that different attention functions may be associated with social impairment among children with ADHD versus ASD + ADHD, highlighting the need for targeted cognitive interventions in early childhood among youth with these clinical disorders.
Footnotes
Acknowledgements
The authors thank the undergraduate research assistants, Rasheed Abdullah and William Olvera, for their time and assistance in data entry.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
