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Research in Autism Spectrum Disorders 6 (2012) 413–421

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Research in Autism Spectrum Disorders


Journal homepage: http://ees.elsevier.com/RASD/default.asp

Sleep problems in children with autism, attention-deficit hyperactivity


disorder, and epilepsy
Fang-Ju Tsai a,b,1, Huey-Ling Chiang a,c,1, Chi-Mei Lee a,d, Susan Shur-Fen Gau a,e,*,
Wang-Tso Lee f, Pi-Chuan Fan f, Yu-Yu Wu g, Yen-Nan Chiu a
a
Department of Psychiatry, National Taiwan University Hospital, Taipei, Taiwan
b
Department of Psychiatry, En Chu Kong Hospital, New Taipei City, Taiwan
c
Department of Psychiatry, New Taipei City Hospital, Taipei, Taiwan
d
Department of Psychiatry, Eastern Michigan University, Ypsilanti, United States
e
Department of Psychiatry, College of Medicine, National Taiwan University, Taipei, Taiwan
f
Department of Pediatrics, National Taiwan University Hospital, Taipei, Taiwan
g
Department of Child Psychiatry, Chang Gung Memorial Hospital-Linkou Medical Center, Chang Gung University College of Medicine, Taoyuan, Taiwan

A R T I C L E I N F O A B S T R A C T

Article history: This study aimed to examine sleep problems in children with autism spectrum disorders
Received 30 June 2011 (ASD), attention-deficit/hyperactivity disorder (ADHD), and epilepsy in clinical settings.
Accepted 1 July 2011 We assessed 64 children with ASD, 64 with ADHD, 64 with epilepsy, and 64 typically
Available online 31 July 2011
developing children without any neuropsychiatric disorders by using a sex-and age-
matched case–control study design. The parents reported their children’s sleep problems.
Keywords:
Parents of children with ASD and ADHD reported more current and lifetime sleep problems
Autism spectrum disorders
of their children than parents of children with epilepsy, especially in snoring and restless
Attention-deficit/hyperactivity disorder
Epilepsy legs syndrome. Current or lifetime sleep problems did not differ between children with
Sleep problems ASD and children with ADHD, or between children with epilepsy and typically developing
Children children. Demographic characteristics and medication status could not fully explain the
increased risk of sleep problems in children with ASD and ADHD. Our findings lend
evidence to support more sleep problems in children with ASD and ADHD than typically
developing children. Our study adds that children with epilepsy do not. These findings
emphasize the importance to assess sleep problems in children with neurodevelopmental
disorders highly comorbid with ASD or ADHD in clinical practice.
ß 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Autism spectrum disorders (ASD), attention-deficit/hyperactivity disorder (ADHD), and epilepsy are three common
neurodevelopmental disorders which are frequently seen in pediatric or psychiatric clinics (Friedman & Sharieff, 2006; In-
Albon, Zumsteg, Muller, & Schneider, 2010; Levy, Mandell, & Schultz, 2009). Children with ASD are also more likely to have
sleep problems including (1) dyssomnias: sleep onset delay (Giannotti, Cortesi, Cerquiglini, Vagnoni, & Valente, 2011;
Goldman, Richdale, Clemons, & Malow, 2011), night awakenings (Giannotti et al., 2011; Goldman, McGrew, et al., 2011;
Souders et al., 2009), early morning waking (Wiggs & Stores, 2004), shortened sleep duration (Cotton & Richdale, 2010;

* Corresponding author at: Department of Psychiatry, National Taiwan University Hospital and College of Medicine, No. 7, Chung-Shan South Road, Taipei
10002, Taiwan. Tel.: +886 2 23123456x66802; fax: +886 2 23812408.
E-mail address: gaushufe@ntu.edu.tw (S.-F. Gau).
1
These authors have equal contribution to this paper.

1750-9467/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.rasd.2011.07.002
414 F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421

Goldman, McGrew, et al., 2011; Richdale & Prior, 1995), sleep–wake cycle disturbance (Wiggs & Stores, 2004) and periodic
limb movements (PLMS) (Godbout, Bergeron, Limoges, Stip, & Mottron, 2000); (2) parasomnias: sleep talking, sleep walking,
sleep terrors, and nightmares (Paavonen et al., 2008). SDB is not consistently found to be associated with ASD (Couturier et
al., 2005). Sleep problems may exacerbate symptoms of autism, and correlate with behavior problems (Goldman, McGrew,
et al., 2011), autistic symptom severity (Mayes & Calhoun, 2009), social skills deficits and stereotyped behaviors (Schreck,
Mulick, & Smith, 2004). Therefore, treating sleep problems may improve the behavior problems of children with ASD
(Malow, McGrew, Harvey, Henderson, & Stone, 2006). Besides, both parents of children with autism suffered from more
psychopathology and less dyadic consensus than parents of typically developing children (Gau, Chou, et al., 2011). Manage
sleep problems in children with autism might decrease their behavior problems. Then it might help parents of children with
autism to have psychological well-being and benefit children with autism in their family.
Sleep problems are also common in children with ADHD including (1) dyssomnias: problems in initiating and
maintaining sleep (Gau & Chiang, 2009) and PLMS during sleep (Sadeh, Pergamin, & Bar-Haim, 2006); (2) sleep-disordered
breathing (SDB): snoring (Chiang et al., 2010; Gau & Chiang, 2009) and obstructive sleep apnea (OSA) (Chervin et al., 2002);
and (3) parasomnias: sleep terrors, and bruxism (Chiang et al., 2010; Gau & Chiang, 2009). A comorbid condition between
ADHD and sleep problems, symptoms of ADHD and the consequences of sleep problems frequently overlap (Chervin et al.,
2002). Some primary sleep disorders are found to be associated with daytime inattention and hyperactivity, which often can
be mistaken for the symptoms of ADHD (Chervin et al., 2002). Other comorbid psychiatric disorders with ADHD and/or the
effects of psychostimulants on sleep may also confound the diagnosis of a primary sleep problem or may contribute to the
development of a sleep problem (Gau & Chiang, 2009). When we need to make the diagnosis of a primary sleep problem in
children with ADHD, we need to exclude the effects of other psychiatric comorbid conditions and/or psychostimulants on
sleep problems.
Several sleep problems that have been frequently reported in children with epilepsy with prevalence ranged from 0.4 to
1.0% (Ong, Yang, Wong, Alsiddiq, & Khu, 2010). These sleep problems are initiating and maintaining sleep disorders, longer
sleep latency to rapid eye movement (REM), some parasomnias, sleep–wake transition disorders, SDB, and excessive
sleepiness (Byars et al., 2008; Maganti et al., 2006; Ong et al., 2010). The manifestations of parasomnia and nocturnal frontal
lobe epilepsy are similar, and polysomnographic study is needed to make differential diagnosis (Derry, Harvey, Walker,
Duncan, & Berkovic, 2009). Sleep problems significantly relate to impaired neuropsychological functioning (Byars et al.,
2008), result in increased distress for the parents and their children, and are associated with greater psychological
dysfunction (Stores, Wiggs, & Campling, 1998).
Sleep problems are more prevalent in children with neuropsychiatric disorders than in healthy children. Although
abundant studies have investigated the association between sleep problems and ADHD in western countries (Sadeh et al.,
2006) and Taiwan (Gau & Chiang, 2009), the evidence for sleep problems in ASD and epilepsy are relatively lacking and
inconsistent. Therefore, whether sleep problems are common features of neurodevelopmental disorders or only associated
with a specific neurodevelopmental disorder is still unknown. Previous studies have been limited by only including children
with one disorder as compared with typically developing children without comparing several neurodevelopmental
disorders in one study. Since the prevalence of various sleep problems vary by gender and age (Gau, 2006), we conducted a
matched case control study (age- and gender-matched) to further elucidate the prevalence and types of sleep problems in
children with these neurodevelopmental disorders. Our aims were to compare the rates and types of sleep problems in
children with ASD, ADHD, epilepsy and in typically developing children. We hypothesized that children with ASD, ADHD and
epilepsy suffered from more sleep problems than typically developing children, and that the types of sleep problems would
be different across the four groups.

2. Method

2.1. Participants

The participants consisted of 64 children (39 boys, 60.9%), aged 6–17, who were clinically diagnosed with ASD according
to the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) criteria for autistic disorder or
Asperger’s disorder; 64 children (39 boys, 60.9%), aged 6–16, who met the International League Against Epilepsy (ILAE)
criteria for epilepsy; 64 children (39 boys, 60.9%), aged 6–16, who were clinically diagnosed with ADHD according to the
DSM-IV criteria; and 64 age-, gender-, and parental educational level-matched typically developing children (Table 1). The
participants were recruited from pediatric neurological and child and adolescent psychiatric outpatient departments.
Because the estimated sample size for each group was sixty participants, the broad age range was necessary to recruit
enough participants. Therefore, we used a matched case–control study design to eliminate the confounding effects of age and
gender as well. These participants were recruited consecutively from a university hospital in northern Taiwan with similar
age and sex distributions from January 2008 to December 2008.

2.2. Clinical participants with ASD, ADHD, and epilepsy

The clinical diagnoses of ASD and ADHD were made by board-certificated child psychiatrists. The Autism Diagnostic
Interview-Revised (ADI-R) (Chien et al., 2010) and the Chinese versions of the Kiddie epidemiologic version of the Schedule
F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421 415

for Affective Disorders and Schizophrenia (K-SADS-E) (Gau, Chong, Chen, & Cheng, 2005) were used to confirm the diagnosis
of ASD and ADHD by well-trained interviewers, respectively. The interviewer training of the Chinese K-SADS-E (Gau &
Chiang, 2009; Gau et al., 2010) and ADI-R (Gau, Lee, et al., 2011) have been described elsewhere in details. Children who met
the ILAE criteria, defined as recurrent unprovoked seizures, based on the clinical diagnosis of two board-certificated pediatric
neurologists, were recruited to the epilepsy group.
Children who were clinically diagnosed with ASD, ADHD, and epilepsy according to the DSM-IV criteria (confirmed by the
ADI-R and K-SADS-E for ASD and ADHD, respectively) and ILAE criteria (for epilepsy) without meeting the following exclusion
criteria were recruited in the study. Participants were excluded if they had a serious medical or neurological illness, such as a
cardiovascular disease; had a Full-Scale Intelligence Quotient (FIQ) score less than 80; had a history of bipolar I or II disorders,
psychosis, and any substance abuse; had major depression; and had severe anxiety disorders based on the DSM-IV criteria at
study entry. If clinical participants were comorbid with either disorder of the other two clinical groups, they would be excluded
from the study. For example, ADHD participants were excluded from the study if they were comorbid with ASD and/or epilepsy.

2.3. Typically developing children

Sixty-four typically developing children were recruited from the schools rather than from advertisement. The teachers
referred students who performed average without overt physical and mental problems according to the distribution of age,
sex, and parent educational level of the three clinical groups. They were assessed to be without lifetime ASD, ADHD, or
epilepsy by inquiring into childhood and current symptoms using the screening questions about ASD and the Chinese K-
SADS-E and epilepsy by trained interviewers. If they met the above-mentioned exclusion criteria for clinical participants,
they were excluded from the study.

2.4. Measures

Sleep-related problems: Items regarding sleep problems were modified from the Sleep Habits Questionnaire (SHQ) (Gau,
2006) using the operational definitions for each sleep problem in accordance with the relevant DSM-IV sleep disorders (Gau
& Chiang, 2009). The SHQ was designed to survey children’s and adolescents’ lifetime and current (past 6 months) sleep-
related problems based on maternal reports. These sleep problems, lasting for at least 1 month during the past 6 months,
included early insomnia (sleep latency more than half an hour at least three times a week for 1 month), middle insomnia
(waking up more than half an hour, at least once per night, three times a week for 1 month), disturbed circadian rhythm
(different sleep–wake pattern from conventional schedules), sleep terrors (DSM-IV criteria), sleep-walking (DSM-IV
criteria), sleep-talking, nightmares, bruxism, noisy snoring, sleep apnea, restless legs syndrome (Chiang et al., 2010; Gau &
Chiang, 2009). The kappa values of the test–retest reliability for each exposure at a 2-week interval using 136 children age 7–
9 ranged from 0.54 to 0.85 (Gau, Soong, & Merikangas, 2004). The 4-week test–retest reliability of these questions in the
sleep parameters of a sample of 73 college students ranged from a low of 0.50 (lifetime sleep terrors) to a high of 0.79
(current bruxism) (Gau et al., 2007).

2.5. Procedures

The Research Ethics Committee of a university hospital in northern Taiwan approved this study prior to
implementation. Written informed consent was obtained from the participants and their parents after explanation of
the purpose and procedure of the study, as well as reassurance of confidentiality. The authors made the clinical diagnoses.
In addition to clinical diagnosis, the parents were interviewed by the Chinese ADI-R (Gau et al., 2011a,b) to confirm the
diagnosis of ASD, and all of the participants and their parents were interviewed separately by well-trained interviewers
using the Chinese K-SADS-E (Gau & Chiang, 2009) to confirm the diagnosis of ADHD. Information about medication used in
children was obtained by interviewing the participants and their parents and was confirmed by medical prescription
records. Parent reported their and children’s demographic data (age, sex, and educational level) when they completed
Sleep Habits Questionnaire (SHQ).

2.6. Statistical analyses

Data were analyzed using SAS 9.1 (SAS Institute Inc., Cary, NC, USA). The 4 comparison groups were (1) participants who had
diagnosis of ADHD without ASD and/or epilepsy; (2) participants who had diagnosis of ASD without ADHD and/or epilepsy; (3)
participants who had diagnosis of epilepsy without ADHD and/or ASD; and (4) matched typically developing children without a
lifetime diagnosis of ASD, ADHD, developmental problems, or epilepsy. The descriptive results were displayed as frequencies,
percentages, means and standard deviations. Categorical variables were compared using the chi-square test; continuous
variables were compared using analysis of variance. We used analysis of covariance (ANCOVA) for age, parental education, and
use of medication as covariates to compare the sleep-related problems among the four groups. All data analyses used 2-tailed
tests; P values of 0.05 or less were considered indicative of significant differences. Logistic regression was used to compare the
rates of sleep problems among the comparison groups. Odds ratios (OR) and 95% confidence intervals (CI) were computed. For
all of the analyses, we started with four-way interactions (age  parental education  medication  group).
416 F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421

3. Results

3.1. Sample description

Because of the age-, sex-, and parental education-matched study design, there were no significant differences among the
four groups in terms of sex, age, and parental educational levels. In addition, there was no difference in the ages of their parents
(Table 1). The proportion of children on medication for the index disorders, currently or lifetime, was highest in participants
with epilepsy (90.6%, 100%), followed by participants with ADHD (59.4%, 64.1%), and participants with ASD (10.9%, 20.3%) were
the least (Table 1). Five children with ASD who did not meet ADHD diagnosis with some ADHD-related symptoms were treated
with methylphenidate and two with fluoxetine. There were 20 (31.3%), 14 (21.9%), 7 (10.9%), 4 (6.3%), and 1 (1.6%) children with
epilepsy currently taking carbamazepine, valprotae, topiramate, lamotrigine, and levetiracetam, respectively.

3.2. Sleep problems

Table 2 displays the current sleep problems for children with ADHD, ASD, epilepsy, and typically developing children.
Participants with ADHD and with ASD were more likely to have problems of snoring and restless legs syndrome than
typically developing children. Participants with ASD had a higher likelihood of having sleep onset insomnia. Snoring, and
restless legs syndrome were also more prevalent in participants with ADHD than in participants with epilepsy. In addition,
participants with ADHD were reported to have more sleep terrors than participants with epilepsy. Snoring, restless leg
syndrome, early (sleep onset) insomnia, sleep-talking and nightmares were more prevalent in participants with ASD than
participants with epilepsy. There were no statistically significant differences between the ADHD and ASD groups, and
between the epilepsy and typically developing groups for any of the sleep-related problems.
Regarding lifetime sleep problems, the ADHD and ASD groups had more significant sleep problems than the epilepsy group.
However, there were no significant differences in sleep problems between the ADHD and ASD groups (Table 3). Parents of
participants with ADHD were more likely to report sleep onset insomnia, night waking insomnia, sleep terrors, sleep-talking,
bruxism, and restless legs syndrome on their children than parents of participants with epilepsy. Participants with ASD were
more likely to have sleep terrors, sleep-talking, and restless legs syndrome than participants with epilepsy (Table 3).

3.3. Effect of age, parental education, and medication

Examining the effect of the child’s age, the parental educational level, and the use of medication on the risk for a current
sleep problem in the whole sample, we found that the rates of sleep terrors (OR = 0.81, 95% CI = 0.67–0.98) decreased with
age. Lower parental education level increased the risk for sleep terrors (OR = 2.43, 95% CI = 1.02–5.76). Receiving medication
did not have an effect on any of the sleep problems (P > 0.05) except for an increased risk for sleep terrors (OR = 4.00, 95%

Table 1
Demographic characteristics by children with ADHD, ASD, epilepsy, and control groups.

ADHD ASD Epilepsy Control Comparison

Chi-square/F value P value

Child (n = 64) (n = 64) (n = 64) (n = 64)


Age, range 6–16 6–17 6–16 6–16 – –
Age (mean  SD) 9.89  2.57 10.08  2.73 9.83  2.61 9.91  2.43 0.11 0.955
Sex, N (%)
Male 39 (60.9) 39 (60.9) 39 (60.9) 39 (60.9) – –
Female 25 (39.1) 25 (39.1) 25 (39.1) 25 (39.1)
Father
Age (mean  SD) 42.85  5.33 44.43  6.65 42.98  6.00 42.29  3.88 1.18 0.318
Education, %
College/university 73 69.8 56.9 56 7.03 0.318
Senior high 19.1 27 34.5 32
Junior high and below 7.9 3.2 8.6 12
Education years (mean  SD) 14.68  2.30 14.70  2.06 14.02  2.43 13.88  2.60 1.62 0.185
Mother
Age (mean  SD) 40.18  4.98 41.16  4.77 39.61  4.60 39.10  4.86 1.78 0.152
Education, %
College/university 60.9 58.7 44.3 46.1 6.54 0.365
Senior high 34.4 38.1 49.2 43.6
Junior high and below 4.7 3.2 6.6 10.3
Education years (mean  SD) 14.30  2.23 14.25  2.16 13.57  2.30 13.54  2.47 1.85 0.138
Medication, %
Current use 59.4 10.9 90.6 0 Epilepsy > ADHD > ASD
Ever used 64.1 20.3 100 0 Epilepsy > ADHD > ASD

Note: SD = standard deviation, ADHD = attention-deficit hyperactivity disorder, ASD = autism spectrum disorders.
F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421
Table 2
Comparison of current sleep problems by children with ADHD, ASD, and epilepsy, and typically developing children.

Sleep problems ADHD ASD Epilepsy Control Odds ratio (CI)

N (%) N (%) N (%) N (%) ADHD vs control ASD vs control Epilepsy vs control ADHD vs ASD ADHD vs epilepsy ASD vs epilepsy

Early insomnia 5 (7.8) 11 (17.2) 2 (3.1) 3 (4.7) 1.72 (0.39–7.54) 4.22 (1.12–15.93) 0.66 (0.11–4.06) 0.41 (0.13–1.25) 2.63 (0.49–14.07) 6.43 (1.37–30.33)
Middle insomnia 4 (6.3) 4 (6.3) 0 (0) 0 (0) 0.060a 0.060a – 1.00 (0.24–4.18) 0.060a 0.060a
Disturbed 1 (1.6) 3 (4.7) 1 (1.6) 1 (1.6) 1.00 (0.06–16.34) 3.10 (0.31–30.61) 1.00 (0.06–16.34) 0.32 (0.03–3.19) 1.00 (0.06–16.34) 3.10 (0.31–30.61)
circadian rhythm
Sleep terrors 8 (12.5) 7 (10.9) 1 (1.6) 8 (12.5) 1.00 (0.35–2.85) 0.86 (0.29–2.53) 0.11 (0.01–0.92) 1.16 (0.40–3.42) 9.00 (1.09–74.22) 7.74 (0.92–64.83)
Sleep-walking 0 (0) 0 (0) 0 (0) 1 (1.6) 0.500 a 0.500 a 0.500 a – – –
Sleep-talking 13 (20.3) 19 (29.7) 9 (14.1) 13 (20.3) 1.00 (0.42–2.37) 1.66 (0.74–3.73) 0.64 (0.25–1.63) 0.60 (0.27–1.36) 1.56 (0.61–3.95) 2.58 (1.06–6.26)
Nightmares 7 (10.9) 11 (17.5) 3 (4.7) 14 (21.9) 0.44 (0.16–1.17) 0.76 (0.31–1.82) 0.18 (0.05–0.65) 0.58 (0.21–1.61) 2.50 (0.62–10.13) 4.30 (1.14–16.25)
Bruxism 16 (25) 14 (21.9) 10 (15.6) 10 (15.6) 1.80 (0.75–4.34) 1.51 (0.62–3.71) 1.00 (0.39–2.60) 1.19 (0.53–2.70) 1.80 (0.75–4.34) 1.51 (0.62–3.71)
Snoring 17 (26.6) 18 (28.1) 6 (9.4) 2 (3.1) 11.21 (2.47–50.90) 12.13 (2.68–54.87) 3.21 (0.62–16.52) 0.92 (0.43–2.01) 3.50 (1.28–9.57) 3.78 (1.39–10.30)
Sleep apnea 1 (1.6) 2 (3.1) 0 (0) 0 (0) 0.500a 0.248a – 0.49 (0.04–5.57) 0.050a 0.248a
Restless legs syndrome 23 (35.9) 28 (43.8) 9 (14.1) 4 (6.3) 8.41 (2.71–26.14) 11.67 (3.78–35.98) 2.45 (0.72–8.43) 0.72 (0.35–1.47) 3.43 (1.44–8.19) 4.75 (2.01–11.24)

Note: ADHD = attention-deficit hyperactivity disorder, ASD = autism spectrum disorders.


a
Fisher’s exact P value.

417
418 F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421

Table 3
Comparison of lifetime sleep problems by children with ADHD, ASD, and epilepsy.

Sleep problems ADHD ASD Epilepsy Odds ratio (CI)

N (%) N (%) N (%) ADHD vs epilepsy ASD vs epilepsy ADHD vs ASD


(N = 64) (N = 64) (N = 64)

Early insomnia 25 (39.1) 21 (32.8) 13 (20) 2.52 (1.14–5.54) 1.92 (0.86–4.27) 1.31 (0.64–2.71)
Middle insomnia 13 (20.3) 6 (9.4) 5 (7.8) 3.01 (1.00–9.01) 1.22 (0.35–4.22) 2.46 (0.87–6.96)
Disturbed circadian rhythm 6 (9.4) 8 (12.5) 5 (7.8) 1.22 (0.35–4.22) 1.69 (0.52–5.46) 0.72 (0.24–2.22)
Sleep terrors 16 (25) 15 (23.4) 5 (7.8) 3.93 (1.34–11.51) 3.61 (1.23–10.64) 1.09 (0.49–2.45)
Sleep-walking 7 (10.9) 2 (3.1) 3 (4.7) 2.50 (0.62–10.13) 0.66 (0.11–4.06) 3.81 (0.76–19.08)
Sleep-talking 32 (50) 31 (48.4) 16 (25) 3.00 (1.42–6.34) 2.82 (1.33–5.96) 1.07 (0.53–2.13)
Nightmares 17 (26.6) 16 (25) 10 (16) 1.95 (0.82–4.68) 1.80 (0.75–4.34) 1.09 (0.49–2.40)
Bruxism 34 (53.1) 26 (40.6) 21 (33) 2.32 (1.13–4.75) 1.40 (0.68–2.88) 1.66 (0.82–3.34)
Snoring 26 (40.6) 23 (35.9) 16 (25) 2.05 (0.97–4.36) 1.68 (0.89–3.61) 1.22 (0.60–2.49)
Sleep apnea 2 (3.1) 3 (4.7) 3 (4.7) 0.66 (0.11–4.06) 1.00 (0.19–5.15) 0.66 (0.11–4.06)
Restless legs syndrome 31 (48.4) 31 (48.4) 19 (30) 2.23 (1.08–4.60) 2.23 (1.08–4.60) 1.00 (0.50–2.00)

Note: ADHD = attention-deficit hyperactivity disorder, ASD = autism spectrum disorders.

CI = 1.20–13.29) and a decreased risk for sleep-talking (OR = 0.50, 95% CI = 0.27–0.95). There were no significant interaction
effects between diagnostic group, gender, age, parental education, and medication for the risk of sleep problems.

4. Discussion

This is the first study to compare sleep problems among three common childhood-onset neuropsychiatric disorders seen
in pediatric psychiatric or neurological clinics and a group of typically developing children simultaneously. The major
findings were that children with ASD or ADHD had more current and lifetime sleep problems than children with epilepsy;
and that these two groups did not significantly differ from each other in current and lifetime sleep problems. Our findings
also indicate that demographic characteristics and medication status cannot fully explain the increased risk of sleep
problems in children and adolescents with ASD or ADHD.

4.1. Sleep problems in ASD

Our finding of increased number of sleep problems, such as sleep–wake schedule disturbance, sleep-talking, and bruxism, in
children and adolescents with ASD is also concordant with previous reports (Couturier et al., 2005; Limoges, Mottron, Bolduc,
Berthiaume, & Godbout, 2005; Richdale & Prior, 1995), although significant differences were noted only for sleep onset
insomnia, snoring and restless leg syndrome in this study. We found that the prevalence of snoring and sleep apnea was higher
in the ASD group, which is contrary to previous finding by questionnaire (Couturier et al., 2005), but supported by results of
polysomnography (Ming, Sun, Nachajon, Brimacombe, & Walters, 2009). This controversy warrants further investigation to
provide more understanding of the risk of sleep apnea in ASD, because effective treatment of sleep apnea in children with ASD
may improve their daytime behaviors, including social communication, attention, repetitive behaviors, and hypersensitivity
(Malow et al., 2006).

4.2. Sleep problems in ADHD

Consistent with previous studies (Chervin et al., 2002; Gau & Chiang, 2009), snoring and the restless leg syndrome were two
of the most prominent sleep problems in children with ADHD. Some relatively rare sleep problems, such as sleep apnea, did not
show statistically significant differences because of the study’s small sample size. For the other sleep problems, the trend that
children with ADHD had higher comorbid sleep problems (sleep onset insomnia and bruxism) than typically developing
children is similar to other studies (Chervin et al., 2002; Corkum, Moldofsky, Hogg-Johnson, Humphries, & Tannock, 1999; Gau
& Chiang, 2009).
We did not find a medication effect on sleep problems, including methylphenidate, which is consistent with our previous
study (Gau & Chiang, 2009) and other reports (Corkum, Panton, Ironside, Macpherson, & Williams, 2008; Souders et al.,
2009), but contrasts with other findings (Corkum et al., 1999). Since methylphenidate was not designed to be randomly
assigned in our study, its effect may be confounded by other self-selective factors. Therefore, we controlled for medication
effect on sleep problems for all groups, and found that increased sleep problems in children and adolescents with ADHD
could not be explained by use of medication.

4.3. Sleep problems in epilepsy

In contrast to previous research (Byars et al., 2008; Maganti et al., 2006; Ong et al., 2010), we did not find increased rates
of any sleep problems in the categories of dyssomnia or parasomnia in children with epilepsy. These negative findings might
be explained by the fact that our epileptic participants were recruited from pediatric clinics, they had normal intelligence
F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421 419

and were optimally controlled by medication, and majority of them were under antiepileptic drugs. Antiepileptic drugs have
been reported to be effective in improving sleep quality by reducing interictal discharges and electroencephalography (EEG)
arousal patterns (Sammaritano & Sherwin, 2000); however, these findings have not been supported by others (Foldvary-
Schaefer, Grigg-Damberger, Foldvary-Schaefer, & Grigg-Damberger, 2009). In addition, parents may underestimate sleep
problems of children with epilepsy because they may pay relatively more attention to seizure severity, the effectiveness and
side effects of medication, and their children’s academic performance and behavioral problems than to sleep problems.

4.4. Comparison of sleep problems among ADHD, ASD, and epilepsy

In addition to the findings of higher rates of sleep problems in children with either ASD or ADHD than typically developing
counterparts, our novel finding is that the risk of current and lifetime sleep problems did not differ between children with
ASD and those with ADHD. No previous study has directly compared the sleep problems in these two groups. Recently, ASD
and ADHD have been proposed to be the frequently comorbid conditions. Evidence based on both family and twin studies
(Rommelse, Franke, Geurts, Hartman, & Buitelaar, 2010), and shared biomarkers (Bradstreet, Smith, Baral, & Rossignol, 2010)
has supported the hypothesis that ASD and ADHD originate partially from similar biological factors. Some intrinsic biological
abnormalities contributing significantly to the behavioral symptoms of ASD, ADHD and sleep problems have been proposed
(Ming & Walters, 2009). Similar sleep problems in these two disorders in our study indirectly lend support to these
hypotheses.
We also found that children with ASD and ADHD had more current and lifetime sleep problems than those with epilepsy.
In previous studies, the presence of a sleep problem is more likely to be a trait marker of ADHD (Chiang et al., 2010), but a
state marker of epilepsy (Ong et al., 2010). In children with a diagnosis of ADHD, the increased risk of sleep problems is not
fully explained by the severity of current ADHD symptoms (Chiang et al., 2010), while increased severity of epilepsy is
associated with more sleep disturbance (Ong et al., 2010). Lack of increased sleep problems in our children with epilepsy
can also partially be explained by optimal control of their seizures by anti-epileptic medication (Sammaritano & Sherwin,
2000).
Our finding of no significantly increased rates of sleep problems in children with epilepsy may be explained by only
including epileptic children without being comorbid with ADHD and/or other neurodevelopment disorders. For example, the
prevalence of ADHD in children with epilepsy ranges from 30 to 50%, which is much higher than those without epilepsy
(Schubert, 2005). Epileptic children, if being comorbid with ADHD, may still have increased risk of sleep problems. Since
epileptic children tend to be comorbid with other neurodevelopment disorders, including ASD (Tuchman, Cuccaro, &
Alessandri, 2010) and ADHD (Schubert, 2005), child health-care providers should still identify sleep problems for children
with epilepsy, and make efforts to manage sleep problems symptoms by getting better seizure control and treating the
comorbid conditions (Parisi, Moavero, Verrotti, & Curatolo 2010). We also recommend that the comorbidities of sleep
problems, epilepsy, ADHD and ASD needs to be carefully addressed and managed in clinical and research settings. However,
our study recruited only pediatric patients with epilepsy without comorbid ADHD and ASD, and cannot provide further
evidence.

4.5. Methodological consideration

This is the first study to directly compare sleep problems among children with ASD, ADHD, epilepsy and typically
developing children. A wide range of sleep problems were measured and the possible confounding factors (age, sex,
parental education level, medication use) were controlled in the model. Finally, clinical assessments were performed by
experienced board-certified child psychiatrists and pediatric neurologists and confirmed by research-oriented, well-
validated, structured instruments; namely, the K-SADS-E and ADI-R to obtain accurate diagnoses of ADHD, ASD, epilepsy,
and sleep problems.
The limitations of the study include questionable generalization of our findings; relatively small sample sizes for each
group; the potential confounding effects from medication; and sleep problems based on parental observation and reports
without objective measurements. However, the literature documents that most sleep disorders can be diagnosed reliably by
clinical interview or parental report only (Chiang et al., 2010; Gau & Chiang, 2009), with the exception of OSA and PLMS in
which polysomnography is needed.

5. Conclusions

Combining our results with several other lines of data, there is strong evidence suggesting that children with ASD
and ADHD are more likely to have sleep problems than matched typically developing children. Therefore, the findings
imply the need to assess sleep problems in children with ASD and ADHD. Although sleep problems are not common
features of neurodevelopmental disorders, children with epilepsy and other developmental disorders still warrant more
awareness in consideration of much increased risk of comorbid ASD and ADHD. These groups are especially important to
screen in clinical practice. Briefly, standardized sleep problem screening questionnaires (such as the Sleep Habits
Questionnaire), followed by a more comprehensive assessment for high risk children should be employed in clinical
settings.
420 F.-J. Tsai et al. / Research in Autism Spectrum Disorders 6 (2012) 413–421

Conflict of interest

The authors have no competing interests.

Acknowledgements

This work is supported by grants from National Science Council, Taiwan (NSC96-2628-B-002-069-MY3, NSC98-3112-B-
002-004), and National Taiwan University Hospital (NTUH98-1093).

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