J Autism Dev Disord (2014) 44:1347–1356 DOI 10.1007/s10803-013-1995-4

ORIGINAL PAPER

ADHD Symptoms Moderate the Relation Between ASD Status and Internalizing Symptoms in 3–6-Year-Old Children Beverly J. Wilson • Christen N. Manangan Hayley A. Dauterman • Heather N. Davis



Published online: 16 November 2013 Ó Springer Science+Business Media New York 2013

Abstract The current study sought to understand the relation between diagnostic status (autism spectrum disorders [ASD] versus typically developing) and internalizing problems in children with and without co-occurring attention deficit hyperactivity disorder (ADHD) symptoms. Participants were 88 children, ages 3:0–6:11, their parents and teachers. Findings indicated that ADHD symptoms moderated the relation between diagnostic status and depressive and somatic symptoms. High ADHD symptoms in children with ASD were associated with increased depressive and somatic symptoms compared to children with typical development. Findings suggest poor prognostic outcomes for children with ASD and co-occurring ADHD symptoms and highlight the need for early identification and targeted intervention. Keywords ASD  Autism  ADHD  Internalizing problems  Depression  Somatization

Introduction Children with autism spectrum disorder (ASD) often present with internalizing symptoms such as depression and anxiety (Guttmann-Steinmetz et al. 2010; Kim et al. 2000; Leyfer et al. 2006; Sukhodolsky et al. 2008). Some initial research suggests internalizing problems are related to increased rates of social and behavioral problems in

B. J. Wilson (&)  C. N. Manangan  H. A. Dauterman  H. N. Davis Clinical Psychology Department, Seattle Pacific University, 3307 Third Avenue West, Suite 107, Seattle, WA 98119-1997, USA e-mail: [email protected]

children with ASD (Gadow et al. 2009; Kim et al. 2000; Leyfer et al. 2006; Sukhodolsky et al. 2008). A better understanding of factors associated with internalizing problems in this group would facilitate the development of better interventions for children with ASD. Emerging research suggests that the presence of symptoms consistent with attention deficit hyperactivity disorder (ADHD) may be one of these factors (Guttmann-Steinmetz et al. 2010). Children with ASD often present with ADHD symptoms (e.g., Leyfer et al. 2006). Research suggests rates for comorbid attention problems in samples of children with ASD to be as high as 53–87 % (Ames and White 2010; Sinzig et al. 2009). Most previous studies in this area of research have investigated older children, adolescents, or adults. There is a need to understand this issue in younger children with ASD because intervention services are generally more effective when implemented earlier rather than later in childhood (Lovaas 1987; McEachin et al. 1993; O’Conner and Healy 2010). In the following sections we briefly review research on internalizing problems in children with ASD, links between ADHD symptoms and internalizing problems, and recent research on internalizing problems in children with ASD and comorbid ADHD symptoms.

Internalizing Problems in Children with ASD Numerous studies have found higher rates of internalizing problems in individuals with ASD compared to their typically developing (TD) peers (Gadow et al. 2012; Kim et al. 2000). When comparing internalizing symptoms between children with high-functioning ASD and TD children (mean age = 9.74 years) using the parent report scale of the BASC-2, Volker et al. (2010) found that children with

123

1348

ASD were reported to have significantly higher rates of depression and anxiety symptoms. Furthermore, research has demonstrated that rates of internalizing problems found in children with ASD are exceptionally high, ranging from 40 to 80 %, depending on the inclusion criteria of the study (ICD-10 criteria; DSM-IV criteria; and parent-report), age range of participants (childhood through adolescence), or reason for referral (Green et al. 2000; Leyfer et al. 2006; McPheeters et al. 2011). Of the different types of internalizing problems, anxiety and depression co-occur most frequently with ASD (Zahn-Waxler et al. 2000). In a sample of 109 5–17-year-old children with ASD, parental reports on a semi-structured diagnostic interview indicated that 24 % had symptoms of depression, 5 % displayed anxiety symptoms, 19 % were reported to have separation anxiety symptoms, and 10 % had symptoms of social phobia (Leyfer et al. 2006). Notably, these rates do not indicate these children met diagnostic criteria for these disorders, but rather they demonstrated functional impairment due to these symptoms. More recent studies have found rates of depressive and anxiety symptoms among children with ASD to be even higher. Ooi et al. (2011) found that 40.8 % of children with ASD (mean age = 10.24 years) demonstrated depressive symptoms based on parent report. Additionally, a recent meta-analysis reported that 39.6 % of children with ASD (mean ages ranged from 4.2 to 16.3 years) had clinically significant anxiety symptoms (van Steensel et al. 2011). Comorbid anxiety or depressive symptoms have been found to exacerbate social difficulties for children with ASD and have been linked to increased rates of peer rejection and long-term social difficulties (Bellini 2004; Gadow et al. 2009; Ghaziuddin et al. 1998). Due to the high rates of comorbid internalizing symptoms for children with ASD, researchers have investigated factors that may uniquely contribute to depressive and anxiety symptoms for this population of children. Increased rates of internalizing symptoms have been associated with lower ASD symptom severity, as seen in individuals with Asperger’s disorder (Delong and Dwyer 1988) and those with higher verbal IQ, nonverbal IQ, and communicative abilities (Estes et al. 2007; Mazurek and Kanne 2010). It has been suggested that individuals with high functioning ASD exhibit greater internalizing symptoms due to their increased social- and self-awareness (Estes et al. 2007). Insight regarding their social challenges can be distressing and result in a range of subsequent internalizing symptoms (Bellini 2004; Hedley and Young 2006). Additionally, older children with ASD have been found to display both higher rates and greater severity of anxiety and depressive symptoms as compared to younger children with ASD (McPheeter et al. 2011; van Steensel et al. 2011). Comparatively less research has explored the relation between

123

J Autism Dev Disord (2014) 44:1347–1356

ASD and internalizing symptoms in children under the age of 5 years. Investigation with the latter group is needed to further clarify the onset and course of these symptoms. Only limited research to date has examined the developmental trajectory of anxiety and depressive symptoms in children with ASD, however it appears likely that the course for children with ASD is similar to that exhibited by TD children with anxiety and depressive symptoms. Although internalizing symptoms are less common in young TD children than older children, depressive symptoms can manifest as early as 3 years of age (Bolton et al. 2006; Copeland et al. 2009). Of the two symptom profiles, anxiety symptoms are less frequently observed in young TD children (Costello and Angold 1995). Nevertheless, children who exhibit anxiety symptoms early in life are at greater risk for maintaining clinically significant anxiety symptoms into later childhood and adolescence (Bolton et al. 2006). Similarly, depressive symptoms in 5 and 6 years old TD children have been shown to predict depressive symptoms at 4 years follow up (Ialongo et al. 1993). These findings suggest that whereas anxiety and depressive symptoms are more common in older children, they do occur in children as young as 3 and tend to predict the maintenance of symptoms as children mature. One poorly understood internalizing problem in individuals with ASD is somatization. Compared to research on anxiety and depressive symptoms, fewer studies have explored the frequency of somatic symptoms in children with ASD (Kanne et al. 2009; Park et al. 2012; Whitely 2003). In a study examining somatic symptoms in children with ASD between the ages of 3 and 11 years old (mean age = 7.67 years), researchers found that 17.52 % reported constipation and 20.83 % reported ear problems, however no TD control group was included for comparison (Whitely 2003). Similarly, Park et al. (2012) found the presence of somatic symptoms in 13 % of 166 4–15-yearold children (mean age = 5.36 years) with ASD based on parent report. However, researchers failed to provide prevalence rates for their sibling control group. Kanne et al. (2009) compared parent and teacher reports on emotional and behavioral problems for 177 children with ASD (3–18 years old, mean age = 7.3 years) and found prevalence rates for clinically significant somatic problems ranged between 3 and 6 % compared to 1 and 4 % for their sibling group. Lastly, Mazefsky and colleagues (2011) compared the frequency of somatic complaints in children with ASD and TD children (8–18 years old, mean age = 12.3 years). They found 19.5 % of children with ASD exhibited somatic complaints at or above the borderline clinical range whereas only 4.5 % of TD children exhibited such symptoms as determined by parent report of symptoms. These findings suggest that children with ASD experience elevated rates of somatic symptoms compared

J Autism Dev Disord (2014) 44:1347–1356

to TD children. Although little is currently known about the course of somatic symptoms in ASD populations, these symptoms in TD children are regularly maintained into adolescence and adulthood (Chapman 2005). Additionally, the presence of somatic complaints in TD children increases their risk for developing another psychiatric disorder later in adulthood (Lipowski 1988). Further research is needed to assess the course of somatic symptoms in children with ASD. In light of the frequent cooccurrence of ASD and a range of internalizing problems, it is important to explore additional factors, such as ADHD symptoms, that may influence this association.

Internalizing Problems in Individuals with ADHD Symptoms Children with ADHD commonly exhibit comorbid internalizing symptoms (Rietz et al. 2012). In a longitudinal study using a community-based sample, researchers found that 7.7 % of 9–13-year-old children with ADHD had a comorbid anxiety disorder and 3.3 % had a comorbid depressive disorder (Costello et al. 2003). Further, research has linked higher rates of anxiety and depressive symptoms in children with ADHD to increased social impairment (Karustis et al. 2000). In the current study, we were especially interested in how ADHD symptoms in young children with ASD and in TD children would relate to their internalizing problems.

Internalizing Problems in Individuals with ASD and ADHD Symptoms In this and subsequent sections we use the term ADHD symptoms rather than ADHD because DSM-IV-TR (APA 2000) diagnostic guidelines for ASD include an exclusionary criterion for ADHD. Emerging research suggests that children with ASD and co-occurring ADHD symptoms have more severe internalizing problems than children with ASD only (Guttmann-Steinmetz et al. 2010). Children with ASD and co-occurring ADHD symptoms tend to experience more severe symptoms of depression and symptoms related to generalized anxiety including restlessness, irritability, and tension as compared to children with ASD without ADHD symptoms (Gadow et al. 2012; GuttmannSteinmetz et al. 2010). These findings imply that ADHD symptoms may uniquely contribute to the manifestation of internalizing symptoms in children with ASD. Most prior research has examined anxiety and depressive symptoms in school aged children and adolescents with ASD and cooccurring ADHD symptoms (Gadow et al. 2009; Ghaziuddin et al. 1998). No prior research has investigated

1349 Table 1 Demographic information by status group TD sample (N = 57)

ASD sample (N = 31)

t/V2

Gender (% male)

56

84

V2 = 6.88**

Ethnicity (% caucasian) Average age in months

88

55

X2 = 9.03

56.07 (1.49)

66.52 (2.27)

t = 3.99***

Child variables

TD typically developing, ASD autism spectrum disorders * p \ 0.05; ** p \ 0.01; *** p \ 0.001

internalizing problems, specifically depression or anxiety symptoms in children younger than 6 years with ASD who vary in ADHD symptomatology. Further, no prior research has examined somatization in children with ASD who are also exhibiting ADHD symptoms.

Current Study In the present study we compared the rates of ADHD and internalizing symptoms between TD children and children with ASD. Based on previous research, we expected that children with ASD would have significantly higher rates of ADHD, anxiety, depression, and somatic symptoms compared to TD children. In addition, we explored whether ASD diagnostic status and ADHD symptoms interact to predict internalizing problems in young children. Based on our review of previous research we hypothesized that ADHD symptoms would differentially influence internalizing symptoms of anxiety and depression based on children’s diagnostic status. Specifically, we expected that ADHD symptoms would be more strongly related to increased symptoms of anxiety and depression in children with ASD than TD children. Although previous research on somatization symptoms in children with ASD is limited, especially regarding the lack of comparison groups, we reasoned that ADHD symptoms would likely exacerbate somatic symptoms for young children with ASD.

Method Participants Participants were 88 children as well as their parents and teachers who participated in a larger research project examining self-regulation in young children. Families were recruited for participation through local schools, autism organizations, therapy clinics, and by placing advertisements in parenting magazines and listservs. To be included

123

1350

J Autism Dev Disord (2014) 44:1347–1356

in the study, children had to meet the following criteria: (a) be between the ages of 3:0 and 6:11; (b) demonstrate sufficient verbal abilities to participate in tasks; (c) children with ASD needed to have a previous diagnosis of autistic disorder, Asperger’s disorder, or pervasive developmental disorder-not otherwise specified; and (d) TD children could not exhibit symptoms suggestive of ASD as indicated on an autism screening measure, could not have a sibling with ASD, and could not have any other diagnosis. The sample included 31 children with ASD and 57 TD children. Demographic information was collected through parent interviews and is provided in Table 1.

Comprehension (42 items) and Naming Vocabulary (34 items) which assess receptive and expressive language, respectively. Items are scored ‘‘1’’ for a correct response or ‘‘0’’ for an incorrect response. Subtest T-scores are summed to yield an overall ability score for the Verbal Reasoning cluster which is similar to a standard score with a mean of 100 with a standard deviation of 15. Participants were required to have ability scores of 85 or higher for inclusion in the study to ensure that they would be able to comprehend and follow verbal instructions associated with study tasks. In the current sample, the internal consistency for this measure was .74.

Procedure

ADHD Symptoms

Participants were evaluated over two visits, a screening visit which occurred at the family’s home and an experimental visit at the university laboratory. Data for the current study were collected at the screening visit. Children’s language abilities were directly assessed and parents completed measures on children’s ASD and ADHD symptoms. In addition, parents provided consent in order for information to be gathered from teachers. Teacher reports were used to evaluate children’s internalizing symptoms.

The ADHD Index from the Conners’ Parent Rating ScaleRevised, Short Form (CPRS-R; Conners 1997) was used to estimate ADHD symptoms. The CPRS-R (27 items) screens for symptoms of ADHD and is appropriate for use with children between the ages of 3 and 17 years old. Respondents rate items using a four-point Likert scale for the severity of the problem, ranging from 0 (not at all true) to 3 (very much true). The CPRS-R contains four subscales: Oppositional, Cognitive Problems, Hyperactivity, and ADHD Index. The ADHD Index (12 items) was used in the current study because this subscale is comprised of items that are together considered indicative of the presence of ADHD. T-scores greater than 65 are indicative of clinically significant symptoms. The reliability coefficient for the current sample was .90.

Measures Diagnostic Status To confirm children’s ASD diagnosis, parents provided original diagnostic reports or provided consent for diagnosing clinics to release reports. In addition, all parents completed the Autism Behavior Checklist (ABC; Krug et al. 1980) to further ensure that TD children did not display symptoms characteristic of ASD. The ABC is a 57-item parent-report measure that assesses ASD symptoms in children ages 3 and older. Items are presented in a forced choice format (i.e. yes or no). The ABC is comprised of five subscales and yields a total score ranging from 0 to 120. A total score of 68 or above is considered ‘high-probability of autism’ (Krug et al. 1993). TD children in the current study were required to score lower than 68 on this measure. The internal consistency of the ABC for the current study was .96. Verbal Ability The Verbal Reasoning cluster from the Differential Abilities Scale, Version II (DAS-II, Elliott 2007) was used to evaluate verbal abilities and to determine eligibility for study participation. The Verbal Reasoning cluster from DAS-II Early Years battery is appropriate for children ages 2:6–6:11. It is comprised of two subtests, Verbal

123

Internalizing Symptoms The Behavioral Assessment System for Children—2 (BASC—2 TRS, Preschool Version and Elementary Version, Teacher Rating Scales; Reynolds and Kamphaus 2004) was used to assess children’s internalizing symptoms. All items are scored on a four-point Likert scale of frequency ranging from 0 (never) to 3 (almost always). We used subscales from the Internalizing Index which includes Depression, Anxiety and Somatization for the current study. Reliability coefficients in the current sample were .73, .70, and .77 for the depression, anxiety, and somatization subscales on the Elementary Version, respectively. On the Preschool version reliability estimates were .74, .83, and .83 for the subscales of depression, and anxiety and somatization, respectively. Data Analysis First, correlations were run between study variables and pertinent child demographic variables (i.e. age, gender, verbal abilities, ethnicity, family income and parent education) to ensure that variables were related as expected

J Autism Dev Disord (2014) 44:1347–1356

1351

Table 2 Descriptive statistics for study variables by status Variable

TD (N = 57) M

ASD (N = 31) SD

Range

M

SD

t

Cohen’s d

Range

ADHD symptoms

51.26

9.26

40–79

62.00

9.95

43–81

5.06***

1.09

Anxiety symptoms

49.70

9.70

39–74

52.90

9.16

39–72

1.51

0.33

Depressive symptoms

47.39

5.78

40–70

54.71

8.68

40–78

4.74***

1.02

Somatic symptoms

48.98

8.18

38–72

47.81

7.29

40–71

-0.67

0.15

TD typically developing, ASD autism spectrum disorders, ADHD symptoms = T-scores from Conners; anxiety, depressive and somatic symptoms = T-scores from BASC-2 * p \ .05; ** p \ .01; *** p \ .001

Table 3 Percentages of clinically significant symptom scores by status Clinically significant

At-risk

TD (N = 57)

ASD (N = 31)

TD (N = 57)

ADHD symptoms

9.0

29.0

3.6

Anxiety symptoms

5.3

6.4

14.1

9.7

Depressive symptoms

1.8

3.2

1.8

22.6

Somatic symptoms

3.5

3.2

8.8

3.2

ASD (N = 31)

symptoms as compared to TD children. Teacher reports on internalizing symptoms indicated that groups did not significantly differ on symptoms of anxiety and somatization based on diagnostic status. However, children with ASD had significantly greater depressive symptoms than TD children.

25.7

ADHD symptoms = T-scores from Conners 3-parent short form; anxiety, depressive and somatic symptoms = T-scores from BASC-2 Teacher Rating Scales; TD typically developing, ASD autism spectrum disorders, Clinically significant indicates T-scores C70. At-risk indicates T-scores = 61–69

and to determine control variables. Next, a series of hierarchical linear regressions were used to test direct and interactive effects of diagnostic status and ADHD symptoms on levels of anxiety, depressive, and somatic symptoms. Prior to analysis, the moderator variable (i.e. ADHD symptoms) was centered and the predictor variable (i.e. diagnostic status) was coded (TD = 1; ASD = -1). The interaction term was created by multiplying the centered ADHD symptoms variable by the code for status.

Results Prior to data analysis, we verified that all participants in this study had complete data. Additionally data were screened to ensure that the assumptions of normality and independence were not violated. Descriptive Analyses Table 2 presents the means, standard deviations, t-tests, and effect sizes for study variables based on group (i.e. ASD versus TD). As expected, parents of children in the ASD group endorsed significantly greater ADHD

Preliminary Analyses Preliminary correlation analyses found that family income, parent education, and children’s gender were not related to teacher report of children’s anxiety, depression or somatic symptoms. In contrast, both children’s age and verbal skills were significantly related to teacher report of children’s depressive symptoms but not to their anxiety or somatic symptoms (see Table 4). Therefore, we controlled for child age and verbal skills in all analyses involving depressive symptoms. Frequency rates for elevated T-score values on the BASC-2 internalizing subscales and the Conner’s ADHD index were examined with respect to children’s diagnostic status. As shown in Table 3, children with ASD, as compared to TD children, had higher parent reported rates of clinically significant ADHD symptoms, and higher teacher reported rates for anxiety and depressive symptoms. Rates for clinically significant somatic symptoms were similar (0.3 % discrepancy) for TD children and children with ASD. Moderation Analyses Table 5 presents the unstandardized regression coefficients (B) and standard errors, standardized regression coefficients (b), R2, adjusted R2, and the change in R2, after entry of each variable for all regression analyses. In analyses where anxiety and somatization symptoms were the dependent variables, diagnostic status and ADHD symptoms were entered on the first step and the interaction of status and ADHD symptoms was entered on the second step. In analyses where child depressive symptoms was the

123

1352

J Autism Dev Disord (2014) 44:1347–1356

Table 4 Correlations for Study variables Variable

1

1. Age



2. Gender

2

.003

3

4

5

6

7

8



3. Verbal abilities

-.260*

-.293**

4. Status

-.395***

-.279**

5. ADHD symptoms

.320***

-.024

6. Anxiety symptoms

.030

-.023

7. Depressive symptoms 8. Somatic symptoms

.296** -.086

.115 -.049

– .472***



-.355***

-.479***

.006 -.294**



-.160

.048



-.455***

.437***

.449***



.006

.217*

.224*

.118

.072



ADHD symptoms = T-scores from Conners 3-parent short form; anxiety, depressive and somatic symptoms = T-scores from BASC-2 Teacher Rating Scales * p \ .05; ** p \ .01; *** p \ .001

Table 5 Hierarchical multiple regression analyses to test moderator effects

Variable

B

SE B

b

R2

Adjusted R2

DR2

Dependent variable: anxiety symptoms Step 1 Status

-1.782

1.216

-0.179

ADHD symptoms

-0.034

0.109

-.038

-0.116

0.112

0.116

.143*

0.057

0.235

-.128*

0.063

-0.233

0.949

-0.270

0.187*

0.078

0.260

-0.205**

0.077

-0.254

Step 2 Status X ADHD symptoms

0.027

0.004

0.027

0.039

0.005

0.012

0.138

0.118

0.138**

0.279

0.244

0.140**

0.337

0.296

0.058**

0.007

-0.016

0.136

0.105

Dependent variable: depressive symptoms Step 1 Age Verbal abilities Step 2 Status ADHD symptoms = T-scores from Conners 3-Parent Short Form; anxiety, depressive and somatic symptoms = T-scores from BASC-2 Teacher Rating Scales. N = 88. B = unstandardized regression coefficient; b = standardized regression coefficient * p \ .05. ** p \ .01. *** p \ .001

ADHD symptoms

-2.17*

Step 3 Status X ADHD symptoms

Dependent variable: somatic symptoms Step 1 Status

0.795

1.006

0.097

ADHD symptoms

0.039

0.090

0.053

Step 2 Status X ADHD symptoms

dependent variable, child age and verbal skills were entered on the first step, status and ADHD symptoms on the second step and the interaction on the third step.

-0.307**

0.087

0.007

0.129**

-.374

On the second step, the interaction term did not explain significant variance, DFinc (1, 84) = 1.088, p = .300. Depressive Symptoms

Anxiety Symptoms Diagnostic status and ADHD symptoms, entered on the first step, did not account for significant variance in children’s anxiety symptoms, Finc (2, 85) = 1.17, p = .315.

123

With depressive symptoms as the dependent variable, child age and verbal abilities were entered on the first step and explained significant variance, Finc (2, 85) = 6.821, p = .002. An examination of follow-up analyses indicated

J Autism Dev Disord (2014) 44:1347–1356

Fig. 1 Interaction between diagnostic status and ADHD symptoms on depressive symptoms

that both age and verbal skills accounted for significant unique variance in teacher report of children’s depressive symptoms, t(85) = 2.255, p = .027; t(85) = -2.238, p = .028, respectively. As can be seen in Table 5 unstandardized regression coefficients indicated that greater depressive symptoms were associated with being older and having lower verbal skills. The influence of children’s diagnostic status and ADHD symptoms on the second step was also significant, DFinc (2, 83) = 8.078, p = .001, and uniquely accounted for 3 and 8 % of the variance in depressive symptoms, respectively. Follow-up analyses indicated that both status and ADHD symptoms explained unique variance in children’s depressive symptoms, t(83) = -2.287, p = .025; t(83) = 2.386, p = .019, respectively. Further, the interaction between status and ADHD symptoms predicted children’s depressive symptoms, DFinc (1, 82) = 7.191, p = .009, and accounted for 6 % of the variance. We graphed this interaction using the procedures suggested by Aiken and West (1991). As can be seen in Fig. 1, children with ASD and high levels of ADHD symptoms, which was defined as 1 standard deviation above the mean (T score = 65.83), had higher levels of depressive symptoms than children with ASD and low levels of ADHD symptoms, defined as 1 standard deviation below the mean (T score = 44.28). This was not true for children with typical development. These children’s depressive symptoms did not differ based on their ADHD symptomology. Somatic Symptoms For analyses of teacher-reported child somatization symptoms, diagnostic status and ADHD symptoms were entered on the first step and were not significantly related to children’s somatic symptoms, Finc (2, 85) = .314, p = .731. In contrast, the interaction between status and ADHD

1353

Fig. 2 Interaction between diagnostic status and ADHD symptoms on somatic symptoms

symptoms, entered on the second step, significantly predicted somatic symptoms, DFinc (1, 84) = 12.540, p = .001, and explained 13 % of the variance in children’s symptoms. As can be seen in the graph of this interaction (Fig. 2), children with ASD were generally less likely to have somatic symptoms than children with typical development but the presence of ADHD symptoms appeared to be linked to the frequency of somatic complaints for children with ASD. Children with ASD and high ADHD symptoms had higher levels of somatic symptoms than children with ASD and low ADHD symptoms. Rates for somatic symptoms for children with typical development did not appear to be strongly linked to their ADHD symptoms. In other words, children with typical development who had high versus low ADHD symptoms did not differ much in their somatic symptoms.

Discussion Results from the current study confirmed previous research demonstrating that children with ASD exhibit greater ADHD symptoms (Ames and White 2010; Sinzig et al. 2009) and depressive symptoms (Gadow et al. 2012; Leyfer et al. 2006) than TD children. We also found that comorbid ADHD symptoms were related to increased rates for certain internalizing problems for young children with ASD. The presence of comorbid ADHD symptoms was related to greater depressive symptoms for children with ASD when they had high ADHD symptoms versus children with ASD and low ADHD symptoms. A parallel pattern was not found for children with typical development. Somatic symptoms were also greater for children with ASD when they had high ADHD symptoms than children with ASD who had low ADHD symptoms, although in general children with ASD versus typical development did not differ significantly in their somatic symptoms. Similar to

123

1354

the pattern found for depressive symptoms, somatic symptoms in TD children did not vary significantly based on their ADHD symptoms. Our study adds to the limited research examining the associations between ADHD symptoms and internalizing problems in young children with ASD and TD children. Furthermore, the findings of this study extend previous research with older children and adolescents by demonstrating that depressive and somatic symptoms of younger children with ASD vary based on their level of ADHD symptomatology. Specifically, our study suggests that ADHD symptoms are associated with greater depressive and somatic symptoms for children on the autism spectrum. However, few of the children who participated in our study exceeded the cutoff for clinically significant internalizing problems. Therefore, while ADHD symptoms were associated with greater depressive and somatic symptoms, the majority of this study’s participants displayed internalizing symptoms within the normative range. Rates of internalizing symptoms for our sample of children with ASD were lower than found in previous studies (e.g. Leyfer et al. 2006; Mazefsky et al. 2011; Ooi et al. 2011). Recent studies have shown that older children with ASD exhibited higher rates of anxiety and depressive symptoms compared to younger children with ASD (McPheeters et al. 2011; van Steensel et al. 2011). Similarly, in TD children, internalizing symptoms become increasingly prevalent as they mature, particularly in early adolescence (Sterba et al. 2007). As such, it is likely that the young age of our sample contributed to the lower rates of internalizing symptoms found in our study. In the current sample we found elevated rates of depressive symptoms in children with ASD compared to TD children. These higher rates of borderline levels of depression symptoms may reflect challenges associated with emotion regulation, which is common among this population (Estes et al. 2007). In contrast, we found comparable rates of anxiety and somatic symptoms across both groups. In addition to the young age of our sample, the lack of group differences for anxiety and somatic symptoms may be due to the way in which internalizing symptoms are typically manifested during the preschool years. Previous research has found that underlying internalization is often difficult to recognize in young children due to the fact that it is commonly displayed through externalizing behaviors such as opposition and aggression (Mireault et al. 2008). Our findings are consistent with previous research indicating that depressive symptoms among children with ASD are positively associated with age (Estes et al. 2007; Mazurek and Kanne 2010). In contrast to previous research (Estes et al. 2007), we found that depressive symptoms were associated with lower, rather than higher, verbal ability. A potential explanation for these different results

123

J Autism Dev Disord (2014) 44:1347–1356

may be the characteristics of our sample. For the current study, we recruited children with ASD who demonstrated verbal abilities in the average range and above. Therefore, lower verbal ability within the current sample represents relatively proficient expressive and receptive language skills. Alternately, children with ASD who have lower verbal skills may experience more difficulties in both social relationships and activities, which may serve as risk factors for depressive symptoms. Clinical Implications of Findings The results of the current study have important clinical implications. First, the results suggest poor prognostic outcomes for children with ASD and co-occurring ADHD symptoms. The ASD group with high ADHD symptoms demonstrated greater depression and somatic symptoms than children with ASD and low ADHD symptoms. Thus, interventions targeting children with these comorbid issues should be developed to address the specific challenges faced by these children. Early identification of these problems is also important so that interventions can be initiated as early as possible. Strengths and Limitations This study had a number of strengths as well as limitations. A significant strength of the present study was its relatively large sample (n = 88) of very young children. Second, this study is one of only a few to include co-occurring ASD and ADHD symptoms, and a control group. One limitation of the current study is that it lacked a comparison group of children with ADHD only. A number of other previous studies have included this additional comparison group (Gadow et al. 2009; Gadow et al. 2012; Guttmann-Steinmetz et al. 2010). In addition, the lack of longitudinal data on children in our study limits our ability to understand the stability of the difficulties encountered by children with ASD and ADHD symptoms. A third limitation is that children in the ASD group did not receive an additional standardized assessment to confirm their diagnostic status above and beyond the clinical reports received from medical offices and hospitals. Another limitation is that we did not ascertain how long teachers had known study participants prior to rating their anxiety, depressive, and somatic symptoms, which could potentially impact their ratings of these behaviors. Similarly, the utilization of parent and teacher report measures to assess ADHD and internalizing symptoms, respectively, limits the ability to assess these symptoms across contexts and thus gain a broad understanding of children’s functioning. Finally, although the study had a relatively large sample it was limited in that the groups were unequal size and specifically the size of the ASD group was smaller (n = 31).

J Autism Dev Disord (2014) 44:1347–1356

Future Research Due to the high rates of internalizing problems in children with ASD and the exacerbation of those problems by ADHD symptoms, future research needs to explore the nature of internalizing problems across different ages and ability levels in individuals with ASD with and without ADHD symptoms in order to more fully understand their co-occurrence. Research is also needed on specific interventions targeting children with ASD and co-morbid ADHD. Acknowledgments This study was funded by a grant to Beverly J. Wilson from the School of Psychology, Family, and Community at Seattle Pacific University. We wish to thank the parents, children, and teachers who participated in this study. We could not have completed this study without their assistance. Additionally, the team of graduate and undergraduate students assisted in collecting these data. We thank them for their assistance. Preliminary analysis of a subset of these data was previously presented at the International Meeting for Autism Research.

References Aiken, L. S., & West, S. G. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks: Sage. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders-text revision. Washington: APA. Ames, C. S., & White, S. J. (2010). Brief Report: are ADHD traits dissociable from the autistic profile? Links between cognition and behavior. Journal of Autism and Developmental Disorders, 41, 357–363. doi:10.1007/s10803-010-1049-0. Bellini, S. (2004). Social skill deficits and anxiety in high-functioning adolescents with autism spectrum disorders. Focus on Autism and Other Developmental Disabilities, 19, 78–86. doi:10.1177/ 10883576040190020201. Bolton, D., Eley, T. C., O’Connor, T. G., Perrin, S., Rabe-Hesketh, S., Rijsdijk, F., et al. (2006). Prevalence and genetic and environmental influences on anxiety disorders in 6-year-old twins. Psychological Medicine, 36(3), 335–344. doi:10.1017/ S0033291705006537. Chapman, M. V. (2005). Neighborhood quality and somatic complaints among American youth. Journal of Adolescent Health, 36(3), 244–252. doi:10.1016/j.jadohealth.2004.02.029. Conners, C. K. (1997). Conners’ Rating Scales—revised. Toronto: Multi-Health Systems Inc. Copeland, W. E., Shanahan, L., Costello, J., & Angold, A. (2009). Childhood and adolescent psychiatric disorders as predictors of young adult disorders. Archives of General Psychiatry, 66(7), 764–772. doi:10.1001/archgenpsychiatry.2009.85. Costello, E. J., & Angold, A. (1995). Epidemiology (pp. 109–124). New York, NY: Guilford Press. Costello, E. J., Mustillo, S., Erkanli, A., Keeler, G., & Angold, A. (2003). Prevalence and development of psychiatric disorders in childhood and adolescence. Archives of General Psychiatry, 60, 837–844. Delong, G. R., & Dwyer, J. T. (1988). Correlation of family history with specific autistic subgroups: Asperger’s syndrome and bipolar affective disease. Journal of Autism and Developmental Disorder, 18(4), 593–600. Elliott, C. D. (2007). Differential Ability Scales (2nd ed.). San Antonio: Harcourt Assessment. Estes, A. M., Dawson, G., Sterling, L., & Munson, J. (2007). Level of intellectual functioning predicts patterns of associated symptoms

1355 in school-age children with autism spectrum disorder. American Journal of Mental Retardation, 112(6), 439–449. Gadow, K. D., DeVincent, C. J., & Schneider, J. (2009). Comparative study of children with ADHD only, autism spectrum disorder ? ADHD, and chronic multiple tic disorder ? ADHD. Journal of Attention Disorders, 12, 474–485. doi:10.1177/ 1087054708320404. Gadow, K. D., Guttmann-Steinmetz, S., Rieffe, C., & DeVincent, C. J. (2012). Depression symptoms in boys with autism spectrum disorder and comparison samples. Journal of Autism Developmental Disorders, 42, 1353–1363. doi:10.1007/s10803-0111367-x. Ghaziuddin, M., Weidmer-Mikhail, E., & Ghaziuddin, N. (1998). Comorbidity of Asperger syndrome: A preliminary report. Journal of Intellectual Disability Research, 42, 279–283. Green, J., Gilchrist, A., Burton, D., & Cox, A. (2000). Social and psychiatric functioning in adolescents with Asperger syndrome compared with conduct disorder. Journal of Autism and Developmental Disorders, 30(4), 279–293. doi:2048/10.1023/A: 1005523232106. Guttmann-Steinmetz, S., Gadow, K. D., DeVincent, C. J., & Crowell, J. (2010). Anxiety symptoms in boys with autism spectrum disorder, attention-deficit hyperactivity disorder, or chronic multiple tic disorder and community control. Journal of Autism Developmental Disorders, 40, 1006–1016. doi:10.1007/s10803010-0950-x. Hedley, D., & Young, R. (2006). Social comparison process and depressive symptoms in children and adolescents with Asperger syndrome. Autism, 10(2), 139–153. doi:10.1177/13623613060 62020. Ialongo, N., Edelsohn, G., Werthamer-Larsson, L., Crockett, L., & Kellam, S. (1993). Are self-reported depressive symptoms in first-grade children developmentally transient phenomena? A further look. Development and Psychopathology, 5(3), 433–457. Kanne, S. M., Abbacchi, A. M., & Constantino, J. N. (2009). Multiinformant ratings of psychiatric symptom severity in children with autism spectrum disorders: The importance of environmental context. Journal of Autism and Developmental Disorders, 39(6), 856–864. doi:10.1007/s10803-009-0694-7. Karustis, J. L., Power, T. J., Rescorla, L. A., Eiraldi, R. B., & Gallagher, P. R. (2000). Anxiety and depression in children with ADHD: Unique associations with academic and social functioning. Journal of Attention Disorders, 4(3), 133–149. Kim, J. A., Szatmari, P., Bryson, S. E., Streiner, D. L., & Wilson, F. J. (2000). The prevalence of anxiety and mood problems among children with autism and Asperger syndrome. Autism, 4(2), 117–132. doi:0126081362-3613(2000006)4:2. Krug, D. A., Arick, J. R., & Almond, P. G. (1980). Behavior checklist for identifying severely handicapped individuals with high levels of autistic behavior. Journal of Child Psychology and Psychiatry, 21, 221–229. Krug, D., Arick, J., & Almond, P. (1993). Autism screening instrument for educational planning (2nd ed.). Austin: PRO-ED. Leyfer, O. T., Folstein, S. E., Bacalman, S., Davis, N. O., Dinh, E., Morgan, J., et al. (2006). Comorbid psychiatric disorders in children with autism: Interview development and rates of disorders. Journal of Autism and Developmental Disorders, 36, 849–861. doi:10.1007/s10803-006-0123-0. Lipowski, Z. J. (1988). Somatization: The concept and its clinical application. The American Journal of Psychiatry, 145(11), 1358–1368. Lovaas, O. I. (1987). Behavioral treatment and normal educational and intellectual functioning in young autistic children. Journal of Consulting and Clinical Psychology, 55, 3–9. Mazefsky, C. A., Anderson, R., Conner, C. M., & Minshew, N. (2011). Child behavior checklist scores for school-aged children

123

1356 with autism: Preliminary evidence of patterns suggesting the need for referral. Journal of Psychopathology and Behavioral Assessment, 33(1), 31–37. doi:10.1007/s10862-010-9198-1. Mazurek, M. O., & Kanne, S. M. (2010). Friendship and internalizing symptoms among children and adolescents with ASD. Journal of Autism and Developmental Disorders, 40, 1512–1520. doi:10. 1007/s10803-010-1014-y. McEachin, J. J., Smith, T., & Lovaas, O. I. (1993). Long-term outcome for children with autism who received early intensive behavioral treatment. American Journal of Mental Retardation, 97(4), 104–112. McPheeters, M. L., Davis, A., Navarre, J. R., I. I., & Scott, T. A. (2011). Family report of ASD concomitant with depression or anxiety among US children. Journal of Autism and Developmental Disorders, 41(5), 646–653. doi:10.1007/s10803-0101085-9. Mireault, G., Rooney, S., Kouwenhoven, K., & Hannan, C. (2008). Oppositional behavior and anxiety in boys and girls: A crosssectional study in two community samples. Child Psychiatry and Human Development, 39, 519–527. O’Conner, A. B., & Healy, O. (2010). Long-term post-intensive behavioral intervention outcomes for five children with autism spectrum disorder. Research in Autism Spectrum Disorders, 4, 594–604. doi:10.1016/j.rasd.2009.12.002. Ooi, Y. P., Tan, Z. J., Lim, C. X., Goh, T. J., & Sung, M. (2011). Prevalence of behavioural and emotional problems in children with high-functioning autism spectrum disorders. Australian and New Zealand Journal of Psychiatry, 45(5), 370–375. doi:10. 3109/00048674.2010.534071. Park, S., Cho, S., Cho, I. H., Kim, B., Kim, J., Shin, M., et al. (2012). Sleep problems and their correlates and comorbid psychopathy of children with autism spectrum disorders. Research in Autism Spectrum Disorders, 6, 1068–1072. doi:10.1016/j.rasd.2012.02. 004. Reynolds, C. R., & Kamphaus, R. W. (2004). BASC-2: Behavior assessment system for children (2nd ed.). Circle Pines: American Guidance Service.

123

J Autism Dev Disord (2014) 44:1347–1356 Rietz, C. S., Hasselhorn, M., & Labuhn, A. S. (2012). Are externalizing and internalizing difficulties of young children with spelling impairment related to their ADHD symptoms? Dyslexia, 18, 174–185. doi:10.1002/dys.1442. Sinzig, J., Walter, D., & Doepfner, M. (2009). Attention deficit/ hyperactivity disorder in children and adolescents with autism spectrum disorder: Symptom or syndrome? Journal of Attention Disorders, 13(2), 117–126. doi:10.1177/1087054708326261. Sterba, S. K., Prinstein, M. J., & Cox, M. J. (2007). Trajectories of internalizing problems across childhood: Heterogeneity, external validity, and gender differences. Development and Psychopathology, 19(2), 345–366. doi:10.1017/S0954579407070174. Sukhodolsky, D. G., Scahill, L., Gadow, K. D., Arnold, L. E., Aman, M. G., McDougle, C. J., et al. (2008). Parent-rated anxiety symptoms in children with pervasive developmental disorders: Frequency and association with core autism symptoms and cognitive functioning. Journal of Abnormal Child Psychology, 36, 117–128. doi:10.1007/s10802-007-9165-9. van Steensel, Francisca. J. A., Bo¨gels, S. M., & Perrin, S. (2011). Anxiety disorders in children and adolescents with autistic spectrum disorders: A meta-analysis. Clinical Child and Family Psychology Review, 14(3), 302–317. doi:10.1007/s10567-0110097-0. Volker, M. A., Lopata, C., Smerbeck, A. M., Knoll, V. A., Thomeer, M. L., Toomey, J. A., et al. (2010). BASC-2 PRS profiles for students with high-functioning autism spectrum disorders. Journal of Autism Developmental Disorders, 40, 188–199. doi:10. 1007/s10803-009-0849-6. Whitely, P. (2003). Developmental, behavioural and somatic factors in pervasive developmental disorders: Preliminary analysis. Child: Care, Heath, and Development, 30(1), 5–11. Zahn-Waxler, C., Klimes-Dougan, B., & Slattery, M. J. (2000). Internalizing problems of childhood and adolescence: Prospects, pitfalls, and progress in understanding the development of anxiety and depression. Development and Psychopathology, 12, 443–466. doi:0.1017/S0954579400003102.

ADHD symptoms moderate the relation between ASD status and internalizing symptoms in 3-6-year-old children.

The current study sought to understand the relation between diagnostic status (autism spectrum disorders [ASD] versus typically developing) and intern...
240KB Sizes 0 Downloads 0 Views