Psychiatry and Clinical Neurosciences 2014; 68: 542–550
doi:10.1111/pcn.12164
Regular Article
Age- and sex-related emotional and behavioral problems in children with autism spectrum disorders: Comparison with control children Fumie Horiuchi, MD,1* Yasunori Oka, MD, PhD,4 Hiroyuki Uno, PhD,5 Kentaro Kawabe, Fumi Okada, MA,1,6 Isao Saito, MD, PhD,2,3 Takeshi Tanigawa, MD, PhD2 and Shu-ichi Ueno, MD, PhD1
MD,1
Departments of 1Neuropsychiatry and Neuroscience, 2Public Health, 3Basic Nursing and Health Science, and 4Center for Sleep Medicine, Ehime University Graduate School of Medicine, Toon, 5Department of Education for Disabled Children, Hyogo University of Teacher Education, Kato-gun, and 6Center for Developmental Clinical Psychology and Psychiatry, Nagoya University, Nagoya, Japan
Aim: Children with autism spectrum disorders (ASD) often present with emotional and behavioral problems, which could change the clinical course, especially during childhood, and affect future quality of life. The aim of this study was to clarify the ageand sex-related differences of these problems in ASD. Methods: The study subjects were 173 patients with ASD (age: 4–16 years) and 173 age- and sex-matched community children (control group). The parent version of the Strengths and Difficulties Questionnaire was used for comparison of the emotional and behavioral problems between the two groups. Results: The Strengths and Difficulties Questionnaire scores were significantly higher in children with ASD than controls at all ages. The score of total difficulties was significantly higher in girls with ASD than in boys, while the score in male controls was significantly higher than in female controls. Age-related differences in emotional and behavioral problems were
UTISM SPECTRUM DISORDERS (ASD) are characterized by difficulties in reciprocal social interaction skills, deficits in communication skills,
A
*Correspondence: Fumie Horiuchi, MD, Department of Neuropsychiatry and Neuroscience, Ehime University Graduate School of Medicine, Shitsukawa, Toon-city, Ehime 791-0295, Japan. Email: [email protected] Received 31 May 2013; revised 23 November 2013; accepted 15 January 2014.
542
observed both in children with ASD and controls, but the characteristics were different: in children with ASD, emotional symptoms and peer problems in both sexes and conduct problems in girls increased significantly with age, while none of the problems in the controls changed with age except for a decrease in the score of hyperactivity/inattention developmentally in both sexes. Prosocial behaviors of children with ASD and controls showed small changes with age.
Conclusion: Emotional and behavioral problems are common in children with ASD and showed age- and sex-related differences. Our study emphasizes the importance of recognizing those differences among children with ASD for early intervention. Key words: autism spectrum disorders, emotional and behavioral problems, Strengths and Difficulties Questionnaire.
stereotypic, obsessive, or repetitive behaviors, and restricted patterns of interests and activities.1 Prevalence of autism and related ASD is up to 1% among children and adolescents, which is greater than previously recognized.2 Emotional and behavioral problems are common in children with ASD.3 These problems often develop into comorbid psychiatric disorders, such as anxiety disorder, attention-deficit/hyperactivity disorder (ADHD), and oppositional defiant disorder (ODD). However, identifying emotional and behavioral prob-
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Age- and sex-related problems in ASD 543
lems that require specific intervention is often difficult. One reason for the difficulty is that children with ASD cannot provide sufficient information for clinicians to identify the presence of co-existent emotional and behavioral problems because of their impairments in social communication. The second reason is that the developmental trajectories of ASD may affect the symptom topography of emotional and behavioral problems that have been observed in the general population. The third reason is that emotional and behavioral problems of children with ASD change with age and are different among male and female patients.4 However, there is little information on the extent of these problems in girls and boys with ASD, or the effect of age on emotional and behavioral problems. To determine the age-related differences in emotional and behavioral problems in children with ASD, comparison with that of control children is necessary. Failure to detect co-existent emotional and behavioral problems, rather than ASD-related symptoms, can forestall specific intervention and increase the risk of further functional impairment. In fact, the presence of emotional and behavioral problems is associated with poor clinical outcome.5 Thus, early detection of such problems is important to avoid suffering of the patients and their families.6 It is vital to have a screening instrument to detect emotional and behavioral problems in children with ASD for early intervention. Several rating scales are available to detect ASD, such as the Modified Checklist for Autism in Toddlers (M-CHAT),7 the Social Communication Questionnaire (SCQ),8 and the Social Responsiveness Scale (SRS).9 However, there are only a few screening measures of emotional and behavioral problems designed specifically for children with ASD. The Strengths and Difficulties Questionnaire (SDQ) is a screening instrument of emotional and behavioral problems in children aged 4–16 years and their worldwide application for screening, clinical, and research purposes has been facilitated by the availability of officially authorized translated versions in over 60 languages.10 The SDQ might be useful for screening emotional and behavioral problems in children with developmental disorders, including ASD. The aims of this study were: (i) to identify any modifiable factors associated with emotional and behavioral problems in 4–16-year-old children; (ii) to delineate sex differences in emotional and behav-
ioral problems by comparing SDQ scores in children with ASD and control children; and (iii) to characterize the age-related differences of emotional and behavioral problems in children with ASD in comparison with control children.
METHODS Participants and instruments ASD group The ASD group consisted of 173 children with ASD, including 84 children aged 4–6 years, 32 children aged 7–9 years, 38 children aged 10–12 years, and 19 children aged 13–16 years (Table 1). These children represented all those referred to Ehime University Hospital for assessment of developmental disorders, including ASD, between 2003 and 2012 and were later diagnosed clinically with ASD based on the DSM-IV-TR criteria by board-certified child psychiatrists. None of the children had any perinatal events or uncontrolled seizure disorders. The parent version of the SDQ was completed by the parents or caregivers. The SDQ describes the child’s functioning during the preceding 6 months and is used for the detection of emotional and behavioral problems.11,12 It comprises 25 items, organized into the following five subscales: emotional symptoms, conduct problems, hyperactivity/inattention, peer relationship problems, and prosocial behavior. Each item is accompanied by a response option ‘0 = not true’, ‘1 = somewhat true’, and ‘2 = certainly
Table 1. Characteristics of participating subjects Age (years): Mean (SD)
Control group ASD group 7.92 (3.28) 7.92 (3.28)
Number of participants (boys/girls) All 173 (129/44) 4–6 years 84 (63/21) 7–9 years 32 (28/4) 10–12 years 38 (24/14) 13–16 years 19 (14/5) IQ (n = 148) Full IQ: Mean (SD) – IQ range –
173 (129/44) 84 (63/21) 32 (28/4) 38 (24/14) 19 (14/5) 88.3 (20.1) 40–132
ASD, autism spectrum disorders.
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
544 F. Horiuchi et al.
true’. The scores of the 20 items on emotional symptoms, conduct problems, hyperactivity/inattention and peer relationship problems were summed to generate the ‘total difficulties score’, ranging from 0 to 40. The scores of prosocial behavior were summed to generate the ‘strength score’. A high total difficulties score reflected difficulties, whereas a high score for the prosocial behavior subscale reflected strengths.10 The cut-off values for total and subscale scores of the SDQ were set so that roughly 80% of children were normal, 10% were on the borderline range, and the remaining 10% had clinical range of SDQ. The cutoff values for the English version, including borderline range and clinical range, were used in this study.10 To assess intellectual functioning, the Wechsler Intelligence Scale for Children-Third Edition (WISC-III) or the Wechsler Intelligence Scale for Children-Fourth Edition (WISC-IV) was used to measure IQ for children aged > 5 years. There were no missing data on the SDQ or WISC among the ASD children. Control group The control subjects were recruited from a pool of children from the local community who participated in the Toon Child Study, which was designed to review the lifestyle and behavior of children.13 The Toon Child Study was conducted in 2009 and all children of Toon city aged 3–18 years (n = 4212) were involved. The total population of Toon city during that year was approximately 35 000, with about 280 births/year. Questionnaires including the SDQ were provided to the parents or primary caregivers. The number of answered questionnaires was 3687, and subjects with any missing data (n = 247) were excluded (the proper response rate: 81.6%). There were no significant differences between subjects with missing data and those without missing data (n = 3440) in terms of sex (χ2 = 0.261, d.f. = 1, P = 0.610) and age (P = 0.814). For this analysis, the subjects were enrolled by stratified two-stage sampling, then 173 age- and sex-matched children were selected. The study was approved by the Institutional Review Board of Ehime University Graduate School of Medicine. Questionnaires were provided to the parents or primary caregivers, together with written information about the project. A signed informed consent was obtained from the parents/caregivers of each participant.
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Statistical analysis To elucidate the main factor(s) that affect the total difficulties, variables such as age, sex, and IQ were entered into multiple regression analysis. Backwards stepwise regression was performed, and a P-value greater than 0.05 was used for variable removal. The exact test was used to analyze the proportion of individuals who scored ‘clinical range’, ‘borderline range’, and ‘normal range’. The mean scores of girls and boys with ASD, and male and female control children, were compared by the Mann–Whitney U-test. Both the ASD subjects (n = 173) and the control subjects (n = 173) were divided into four age groups. The data for each of the four age groups of children with ASD and control children were compared by the Student’s t-test. To clarify the age-related differences in emotional and behavioral problems in the two sex groups, differences among the four groups were assessed using Pearson correlation. All statistical analyses were conducted using SPSS 11.5 for Windows (IBM, Chicago, IL, USA). Significance level was set at P < 0.05.
RESULTS Demographic data The mean age of the children with ASD at the time of evaluation was 7.92 ± 3.3 years and 129 of the 173 children (74.6%) were male (Table 1). The mean IQ score of those who were tested by the WISC-III or WISC-IV (n = 148) was 88.3 ± 20.1. Twenty-eight children with ASD (male/female = 18/10) out of 148 children with ASD (male/female = 114/34) had intellectual disability. The remaining 25 children could not be tested due to cognitive limitation (n = 23) or children’s refusal (n = 2). The control children were not given the cognitive ability test. There were no comorbid psychiatric disorders, except for one girl with well-controlled epilepsy.
Effects of IQ on the total difficulties score of SDQ in children with ASD Multiple regression analysis of the total score of SDQ and various demographic factors showed that the total score of SDQ correlated significantly with age (B = 0.330, β = 0.204, P = 0.011) and sex (B = –2.802, β = –0.224, P = 0.006), but not with IQ (B = –0.006, β = –0.022, P = 0.781).
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Age- and sex-related problems in ASD 545
Table 2. Proportion of ASD and control children in the normal, borderline, and clinical range of the SDQ Normal range SDQ scales Boys Total difficulties Emotional symptoms Conduct problems Hyperactivity/inattention Peer problems Prosocial behavior Girls Total difficulties Emotional symptoms Conduct problems Hyperactivity/inattention Peer problems Prosocial behavior
Borderline range
Clinical range
Raw
Control
ASD
Raw
Control
ASD
Raw
Control
ASD
0–13 0–3 0–2 0–5 0–2 6–10
100 (77.5)* 105 (81.4)* 82 (63.6)* 102 (79.1)* 90 (69.8)* 68 (52.7)*
41 (31.8) 85 (65.9) 60 (46.5) 54 (41.9) 31 (24.0) 36 (27.9)
14–16 4 3 6 3 5
12 (9.3) 10 (7.8) 20 (15.5) 13 (10.1) 20 (15.5)* 29 (22.5)
31 (24.0)* 20 (15.5)* 30 (23.3)* 21 (16.3)* 15 (11.6) 26 (20.2)
17–40 5–10 4–10 7–10 4–10 0–4
17 (13.2) 14 (10.9) 27 (20.9) 14 (10.9) 19 (14.7) 32 (24.8)
57 (44.2)* 24 (18.6)* 39 (30.2)* 54 (41.9)* 83 (64.3)* 67 (51.9)*
0–13 0–3 0–2 0–5 0–2 6–10
42 (95.5)* 38 (86.4)* 35 (79.5)* 41 (93.2)* 37 (84.1)* 26 (59.1)*
9 (20.5) 20 (45.5) 15 (34.1) 10 (22.7) 12 (27.3) 14 (31.8)
14–16 4 3 6 3 5
2 (4.5) 4 (9.1) 2 (4.5) 0 (0) 5 (11.4) 8 (18.2)*
11 (25.0)* 6 (13.6)* 9 (20.5)* 5 (11.4)* 4 (9.1) 4 (9.1)
17–40 5–10 4–10 7–10 4–10 0–4
0 (0) 2 (4.5) 7 (15.9) 3 (6.8) 2 (4.5) 10 (22.7)
24 (54.5)* 18 (40.9)* 20 (45.5)* 29 (65.9)* 28 (63.6)* 26 (59.1)*
Data are numbers of patients (percentages). *P < 0.05, compared with the control of the same group. ASD, autism spectrum disorders; SDQ, Strengths and Difficulties Questionnaire.
prosocial behavior scales among boys with ASD and in all subscales among girls with ASD.
Patterns of emotional and behavioral problems in children with ASD Table 2 shows the range of the total and subscale scores of SDQ using the cut-off values. The percentages of children with ASD in total difficulties and all subscales were significantly higher than those of control children (P ≤ 0.005), indicating more emotional and behavioral problems in patients than the controls. Moreover, the percentages of children in the clinical range were more than 40% in the hyperactivity/inattention, peer problems, and
Sex differences in SDQ scores in children with ASD and in control children The mean scores of total difficulties, hyperactivity/ inattention, and conduct problems were significantly higher in girls with ASD than in boys (Table 3). On the other hand, the scores of total difficulties and hyperactivity/inattention in control boys were significantly higher than those of girls.
Table 3. Differences in mean SDQ scores between boys and girls with ASD and control subjects Control
ASD
SDQ scales
Boys (n = 129)
Girls (n = 44)
P
Boys (n = 129)
Girls (n = 44)
P
Total difficulties Emotional symptoms Conduct problems Hyperactivity/inattention Peer problems Prosocial behavior
9.75 (5.8) 1.87 (2.0) 2.33 (1.8) 3.70 (2.3) 1.85 (1.6) 5.71 (2.0)
7.11 (3.5) 1.32 (1.6) 1.80 (1.3) 2.73 (2.0) 1.27 (1.1) 6.02 (2.0)
0.013* 0.175 0.142 0.006* 0.068 0.346
16.08 (5.1) 2.93 (2.1) 2.78 (1.9) 5.91 (2.3) 4.45 (2.3) 4.28 (2.5)
18.48 (5.4) 3.80 (2.7) 3.34 (1.7) 6.70 (2.1) 4.64 (2.5) 4.30 (2.8)
0.020* 0.077 0.041* 0.029* 0.612 0.862
*P-values for differences between boys and girls of the same group (by Mann–Whitney U-test). ASD, autism spectrum disorders; SDQ, Strengths and Difficulties Questionnaire.
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
546 F. Horiuchi et al.
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Age-related differences in emotional and behavioral problems in children with ASD The total and subscale scores of the SDQ stratified by age are shown in Table 4. In each age group, the total SDQ difficulty score was significantly higher in children with ASD than control children and this was true in both boys and girls. The total SDQ scores of girls and boys with ASD increased with age (boys: r = 0182, P = 0.039; girls: r = 0.483, P = 0.001). On the other hand, the same scores for control children remained unchanged during development (boys: r = –0.168, P = 0.057; girls: r = –0.025, P = 0.871). The scores of emotional symptoms of boys with ASD increased significantly with age (r = 0.221,
P = 0.012) and the scores of children with ASD were higher than those of control children in both sexes. In contrast, the emotional score of male controls over 13 years of age was significantly lower than that of male controls aged 10–12 years. Accordingly, the gap between boys over 13 years with ASD and control boys of the same age was larger. The scores of female controls increased significantly and matched the level of children with ASD. Consequently, there seemed no emotional discrepancy between girls with ASD and control girls in this age group. The score of conduct problems of boys with ASD did not increase with age (r = –0.011, P = 0.900) and there were no significant differences between children with ASD and control children. In contrast, the score
Table 4. Chronological changes in the mean score of the SDQ 4–6 years: 84 (63/21) Age: n (M/F) Total difficulties Boys ASD Control Girls ASD Control Emotional symptoms Boys ASD Control Girls ASD Control Conduct problems Boys ASD Control Girls ASD Control Hyperactivity/inattention Boys ASD Control Girls ASD Control Peer problems Boys ASD Control Girls ASD Control Prosocial behavior Boys ASD Control Girls ASD Control
7–9 years: 32 (28/4)
10–12 years: 38 (24/14)
Mean (SD)
P*
Mean (SD)
P*
Mean (SD)
14.84 (4.8) 10.27 (5.7) 15.62 (4.2) 7.38 (3.5)
doi:10.1111/pcn.12164
Regular Article
Age- and sex-related emotional and behavioral problems in children with autism spectrum disorders: Comparison with control children Fumie Horiuchi, MD,1* Yasunori Oka, MD, PhD,4 Hiroyuki Uno, PhD,5 Kentaro Kawabe, Fumi Okada, MA,1,6 Isao Saito, MD, PhD,2,3 Takeshi Tanigawa, MD, PhD2 and Shu-ichi Ueno, MD, PhD1
MD,1
Departments of 1Neuropsychiatry and Neuroscience, 2Public Health, 3Basic Nursing and Health Science, and 4Center for Sleep Medicine, Ehime University Graduate School of Medicine, Toon, 5Department of Education for Disabled Children, Hyogo University of Teacher Education, Kato-gun, and 6Center for Developmental Clinical Psychology and Psychiatry, Nagoya University, Nagoya, Japan
Aim: Children with autism spectrum disorders (ASD) often present with emotional and behavioral problems, which could change the clinical course, especially during childhood, and affect future quality of life. The aim of this study was to clarify the ageand sex-related differences of these problems in ASD. Methods: The study subjects were 173 patients with ASD (age: 4–16 years) and 173 age- and sex-matched community children (control group). The parent version of the Strengths and Difficulties Questionnaire was used for comparison of the emotional and behavioral problems between the two groups. Results: The Strengths and Difficulties Questionnaire scores were significantly higher in children with ASD than controls at all ages. The score of total difficulties was significantly higher in girls with ASD than in boys, while the score in male controls was significantly higher than in female controls. Age-related differences in emotional and behavioral problems were
UTISM SPECTRUM DISORDERS (ASD) are characterized by difficulties in reciprocal social interaction skills, deficits in communication skills,
A
*Correspondence: Fumie Horiuchi, MD, Department of Neuropsychiatry and Neuroscience, Ehime University Graduate School of Medicine, Shitsukawa, Toon-city, Ehime 791-0295, Japan. Email: [email protected] Received 31 May 2013; revised 23 November 2013; accepted 15 January 2014.
542
observed both in children with ASD and controls, but the characteristics were different: in children with ASD, emotional symptoms and peer problems in both sexes and conduct problems in girls increased significantly with age, while none of the problems in the controls changed with age except for a decrease in the score of hyperactivity/inattention developmentally in both sexes. Prosocial behaviors of children with ASD and controls showed small changes with age.
Conclusion: Emotional and behavioral problems are common in children with ASD and showed age- and sex-related differences. Our study emphasizes the importance of recognizing those differences among children with ASD for early intervention. Key words: autism spectrum disorders, emotional and behavioral problems, Strengths and Difficulties Questionnaire.
stereotypic, obsessive, or repetitive behaviors, and restricted patterns of interests and activities.1 Prevalence of autism and related ASD is up to 1% among children and adolescents, which is greater than previously recognized.2 Emotional and behavioral problems are common in children with ASD.3 These problems often develop into comorbid psychiatric disorders, such as anxiety disorder, attention-deficit/hyperactivity disorder (ADHD), and oppositional defiant disorder (ODD). However, identifying emotional and behavioral prob-
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Age- and sex-related problems in ASD 543
lems that require specific intervention is often difficult. One reason for the difficulty is that children with ASD cannot provide sufficient information for clinicians to identify the presence of co-existent emotional and behavioral problems because of their impairments in social communication. The second reason is that the developmental trajectories of ASD may affect the symptom topography of emotional and behavioral problems that have been observed in the general population. The third reason is that emotional and behavioral problems of children with ASD change with age and are different among male and female patients.4 However, there is little information on the extent of these problems in girls and boys with ASD, or the effect of age on emotional and behavioral problems. To determine the age-related differences in emotional and behavioral problems in children with ASD, comparison with that of control children is necessary. Failure to detect co-existent emotional and behavioral problems, rather than ASD-related symptoms, can forestall specific intervention and increase the risk of further functional impairment. In fact, the presence of emotional and behavioral problems is associated with poor clinical outcome.5 Thus, early detection of such problems is important to avoid suffering of the patients and their families.6 It is vital to have a screening instrument to detect emotional and behavioral problems in children with ASD for early intervention. Several rating scales are available to detect ASD, such as the Modified Checklist for Autism in Toddlers (M-CHAT),7 the Social Communication Questionnaire (SCQ),8 and the Social Responsiveness Scale (SRS).9 However, there are only a few screening measures of emotional and behavioral problems designed specifically for children with ASD. The Strengths and Difficulties Questionnaire (SDQ) is a screening instrument of emotional and behavioral problems in children aged 4–16 years and their worldwide application for screening, clinical, and research purposes has been facilitated by the availability of officially authorized translated versions in over 60 languages.10 The SDQ might be useful for screening emotional and behavioral problems in children with developmental disorders, including ASD. The aims of this study were: (i) to identify any modifiable factors associated with emotional and behavioral problems in 4–16-year-old children; (ii) to delineate sex differences in emotional and behav-
ioral problems by comparing SDQ scores in children with ASD and control children; and (iii) to characterize the age-related differences of emotional and behavioral problems in children with ASD in comparison with control children.
METHODS Participants and instruments ASD group The ASD group consisted of 173 children with ASD, including 84 children aged 4–6 years, 32 children aged 7–9 years, 38 children aged 10–12 years, and 19 children aged 13–16 years (Table 1). These children represented all those referred to Ehime University Hospital for assessment of developmental disorders, including ASD, between 2003 and 2012 and were later diagnosed clinically with ASD based on the DSM-IV-TR criteria by board-certified child psychiatrists. None of the children had any perinatal events or uncontrolled seizure disorders. The parent version of the SDQ was completed by the parents or caregivers. The SDQ describes the child’s functioning during the preceding 6 months and is used for the detection of emotional and behavioral problems.11,12 It comprises 25 items, organized into the following five subscales: emotional symptoms, conduct problems, hyperactivity/inattention, peer relationship problems, and prosocial behavior. Each item is accompanied by a response option ‘0 = not true’, ‘1 = somewhat true’, and ‘2 = certainly
Table 1. Characteristics of participating subjects Age (years): Mean (SD)
Control group ASD group 7.92 (3.28) 7.92 (3.28)
Number of participants (boys/girls) All 173 (129/44) 4–6 years 84 (63/21) 7–9 years 32 (28/4) 10–12 years 38 (24/14) 13–16 years 19 (14/5) IQ (n = 148) Full IQ: Mean (SD) – IQ range –
173 (129/44) 84 (63/21) 32 (28/4) 38 (24/14) 19 (14/5) 88.3 (20.1) 40–132
ASD, autism spectrum disorders.
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
544 F. Horiuchi et al.
true’. The scores of the 20 items on emotional symptoms, conduct problems, hyperactivity/inattention and peer relationship problems were summed to generate the ‘total difficulties score’, ranging from 0 to 40. The scores of prosocial behavior were summed to generate the ‘strength score’. A high total difficulties score reflected difficulties, whereas a high score for the prosocial behavior subscale reflected strengths.10 The cut-off values for total and subscale scores of the SDQ were set so that roughly 80% of children were normal, 10% were on the borderline range, and the remaining 10% had clinical range of SDQ. The cutoff values for the English version, including borderline range and clinical range, were used in this study.10 To assess intellectual functioning, the Wechsler Intelligence Scale for Children-Third Edition (WISC-III) or the Wechsler Intelligence Scale for Children-Fourth Edition (WISC-IV) was used to measure IQ for children aged > 5 years. There were no missing data on the SDQ or WISC among the ASD children. Control group The control subjects were recruited from a pool of children from the local community who participated in the Toon Child Study, which was designed to review the lifestyle and behavior of children.13 The Toon Child Study was conducted in 2009 and all children of Toon city aged 3–18 years (n = 4212) were involved. The total population of Toon city during that year was approximately 35 000, with about 280 births/year. Questionnaires including the SDQ were provided to the parents or primary caregivers. The number of answered questionnaires was 3687, and subjects with any missing data (n = 247) were excluded (the proper response rate: 81.6%). There were no significant differences between subjects with missing data and those without missing data (n = 3440) in terms of sex (χ2 = 0.261, d.f. = 1, P = 0.610) and age (P = 0.814). For this analysis, the subjects were enrolled by stratified two-stage sampling, then 173 age- and sex-matched children were selected. The study was approved by the Institutional Review Board of Ehime University Graduate School of Medicine. Questionnaires were provided to the parents or primary caregivers, together with written information about the project. A signed informed consent was obtained from the parents/caregivers of each participant.
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Statistical analysis To elucidate the main factor(s) that affect the total difficulties, variables such as age, sex, and IQ were entered into multiple regression analysis. Backwards stepwise regression was performed, and a P-value greater than 0.05 was used for variable removal. The exact test was used to analyze the proportion of individuals who scored ‘clinical range’, ‘borderline range’, and ‘normal range’. The mean scores of girls and boys with ASD, and male and female control children, were compared by the Mann–Whitney U-test. Both the ASD subjects (n = 173) and the control subjects (n = 173) were divided into four age groups. The data for each of the four age groups of children with ASD and control children were compared by the Student’s t-test. To clarify the age-related differences in emotional and behavioral problems in the two sex groups, differences among the four groups were assessed using Pearson correlation. All statistical analyses were conducted using SPSS 11.5 for Windows (IBM, Chicago, IL, USA). Significance level was set at P < 0.05.
RESULTS Demographic data The mean age of the children with ASD at the time of evaluation was 7.92 ± 3.3 years and 129 of the 173 children (74.6%) were male (Table 1). The mean IQ score of those who were tested by the WISC-III or WISC-IV (n = 148) was 88.3 ± 20.1. Twenty-eight children with ASD (male/female = 18/10) out of 148 children with ASD (male/female = 114/34) had intellectual disability. The remaining 25 children could not be tested due to cognitive limitation (n = 23) or children’s refusal (n = 2). The control children were not given the cognitive ability test. There were no comorbid psychiatric disorders, except for one girl with well-controlled epilepsy.
Effects of IQ on the total difficulties score of SDQ in children with ASD Multiple regression analysis of the total score of SDQ and various demographic factors showed that the total score of SDQ correlated significantly with age (B = 0.330, β = 0.204, P = 0.011) and sex (B = –2.802, β = –0.224, P = 0.006), but not with IQ (B = –0.006, β = –0.022, P = 0.781).
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Age- and sex-related problems in ASD 545
Table 2. Proportion of ASD and control children in the normal, borderline, and clinical range of the SDQ Normal range SDQ scales Boys Total difficulties Emotional symptoms Conduct problems Hyperactivity/inattention Peer problems Prosocial behavior Girls Total difficulties Emotional symptoms Conduct problems Hyperactivity/inattention Peer problems Prosocial behavior
Borderline range
Clinical range
Raw
Control
ASD
Raw
Control
ASD
Raw
Control
ASD
0–13 0–3 0–2 0–5 0–2 6–10
100 (77.5)* 105 (81.4)* 82 (63.6)* 102 (79.1)* 90 (69.8)* 68 (52.7)*
41 (31.8) 85 (65.9) 60 (46.5) 54 (41.9) 31 (24.0) 36 (27.9)
14–16 4 3 6 3 5
12 (9.3) 10 (7.8) 20 (15.5) 13 (10.1) 20 (15.5)* 29 (22.5)
31 (24.0)* 20 (15.5)* 30 (23.3)* 21 (16.3)* 15 (11.6) 26 (20.2)
17–40 5–10 4–10 7–10 4–10 0–4
17 (13.2) 14 (10.9) 27 (20.9) 14 (10.9) 19 (14.7) 32 (24.8)
57 (44.2)* 24 (18.6)* 39 (30.2)* 54 (41.9)* 83 (64.3)* 67 (51.9)*
0–13 0–3 0–2 0–5 0–2 6–10
42 (95.5)* 38 (86.4)* 35 (79.5)* 41 (93.2)* 37 (84.1)* 26 (59.1)*
9 (20.5) 20 (45.5) 15 (34.1) 10 (22.7) 12 (27.3) 14 (31.8)
14–16 4 3 6 3 5
2 (4.5) 4 (9.1) 2 (4.5) 0 (0) 5 (11.4) 8 (18.2)*
11 (25.0)* 6 (13.6)* 9 (20.5)* 5 (11.4)* 4 (9.1) 4 (9.1)
17–40 5–10 4–10 7–10 4–10 0–4
0 (0) 2 (4.5) 7 (15.9) 3 (6.8) 2 (4.5) 10 (22.7)
24 (54.5)* 18 (40.9)* 20 (45.5)* 29 (65.9)* 28 (63.6)* 26 (59.1)*
Data are numbers of patients (percentages). *P < 0.05, compared with the control of the same group. ASD, autism spectrum disorders; SDQ, Strengths and Difficulties Questionnaire.
prosocial behavior scales among boys with ASD and in all subscales among girls with ASD.
Patterns of emotional and behavioral problems in children with ASD Table 2 shows the range of the total and subscale scores of SDQ using the cut-off values. The percentages of children with ASD in total difficulties and all subscales were significantly higher than those of control children (P ≤ 0.005), indicating more emotional and behavioral problems in patients than the controls. Moreover, the percentages of children in the clinical range were more than 40% in the hyperactivity/inattention, peer problems, and
Sex differences in SDQ scores in children with ASD and in control children The mean scores of total difficulties, hyperactivity/ inattention, and conduct problems were significantly higher in girls with ASD than in boys (Table 3). On the other hand, the scores of total difficulties and hyperactivity/inattention in control boys were significantly higher than those of girls.
Table 3. Differences in mean SDQ scores between boys and girls with ASD and control subjects Control
ASD
SDQ scales
Boys (n = 129)
Girls (n = 44)
P
Boys (n = 129)
Girls (n = 44)
P
Total difficulties Emotional symptoms Conduct problems Hyperactivity/inattention Peer problems Prosocial behavior
9.75 (5.8) 1.87 (2.0) 2.33 (1.8) 3.70 (2.3) 1.85 (1.6) 5.71 (2.0)
7.11 (3.5) 1.32 (1.6) 1.80 (1.3) 2.73 (2.0) 1.27 (1.1) 6.02 (2.0)
0.013* 0.175 0.142 0.006* 0.068 0.346
16.08 (5.1) 2.93 (2.1) 2.78 (1.9) 5.91 (2.3) 4.45 (2.3) 4.28 (2.5)
18.48 (5.4) 3.80 (2.7) 3.34 (1.7) 6.70 (2.1) 4.64 (2.5) 4.30 (2.8)
0.020* 0.077 0.041* 0.029* 0.612 0.862
*P-values for differences between boys and girls of the same group (by Mann–Whitney U-test). ASD, autism spectrum disorders; SDQ, Strengths and Difficulties Questionnaire.
© 2014 The Authors Psychiatry and Clinical Neurosciences © 2014 Japanese Society of Psychiatry and Neurology
546 F. Horiuchi et al.
Psychiatry and Clinical Neurosciences 2014; 68: 542–550
Age-related differences in emotional and behavioral problems in children with ASD The total and subscale scores of the SDQ stratified by age are shown in Table 4. In each age group, the total SDQ difficulty score was significantly higher in children with ASD than control children and this was true in both boys and girls. The total SDQ scores of girls and boys with ASD increased with age (boys: r = 0182, P = 0.039; girls: r = 0.483, P = 0.001). On the other hand, the same scores for control children remained unchanged during development (boys: r = –0.168, P = 0.057; girls: r = –0.025, P = 0.871). The scores of emotional symptoms of boys with ASD increased significantly with age (r = 0.221,
P = 0.012) and the scores of children with ASD were higher than those of control children in both sexes. In contrast, the emotional score of male controls over 13 years of age was significantly lower than that of male controls aged 10–12 years. Accordingly, the gap between boys over 13 years with ASD and control boys of the same age was larger. The scores of female controls increased significantly and matched the level of children with ASD. Consequently, there seemed no emotional discrepancy between girls with ASD and control girls in this age group. The score of conduct problems of boys with ASD did not increase with age (r = –0.011, P = 0.900) and there were no significant differences between children with ASD and control children. In contrast, the score
Table 4. Chronological changes in the mean score of the SDQ 4–6 years: 84 (63/21) Age: n (M/F) Total difficulties Boys ASD Control Girls ASD Control Emotional symptoms Boys ASD Control Girls ASD Control Conduct problems Boys ASD Control Girls ASD Control Hyperactivity/inattention Boys ASD Control Girls ASD Control Peer problems Boys ASD Control Girls ASD Control Prosocial behavior Boys ASD Control Girls ASD Control
7–9 years: 32 (28/4)
10–12 years: 38 (24/14)
Mean (SD)
P*
Mean (SD)
P*
Mean (SD)
14.84 (4.8) 10.27 (5.7) 15.62 (4.2) 7.38 (3.5)
