Abstract
BACKGROUND
Sleep problems are associated with problems of cognitive functioning, learning, attention and school performance. It has been found that sleep problems are highly prevalent in children with Autistic spectrum disorders (ASD), with rates ranging from 40% to 80%. We aimed to identify the prevalence of sleep problems on children with ASD in Indonesia and Japan.
METHODS
A cross-sectional study was conducted in Surabaya, Indonesia and Kobe, Japan. Children aged 4 – 10 years old were enrolled using stratified cluster sampling. Children’s Sleep Habits Questionnaire-Abbreviated (CSHQ-A) was used in this research to assess the sleep problems, consisted of 22 questions (NICHD SECCYD—Wisconsin). Data were analyzed with Mann-Whitney U test to compare the CSHQ-A scores between Indonesian and Japanese children, while the proportion of sleep problems was evaluated by chi-square test with 95% confidence interval.
RESULTS
Fifty children with ASD were included in this study, 25 children from Kobe, Japan and 25 children from Surabaya, Indonesia. The prevalence of sleep problems on children with ASD was 60% (15 children) in Indonesia and 16% (4 children) in Japan respectively. There were significant differences in total waking during the night and in morning wake for the CSHQ-A between children from Indonesia and Japan (p<0.005).
CONCLUSIONS
The prevalence of sleep problems on children with ASD was higher in children from Indonesia than from Japan.
Keywords: Children, Autistic spectrum disorders, Sleep problems, Children’s Sleep Habits Questionnaire-Abbreviated
INTRODUCTION
Autism Spectrum Disorder (ASD) is a developmental disorder characterized by deficits in social interaction and communication, restricted, repetitive interests and behaviors beginning in infancy and toddler years (1). The prevalence of autism has been estimated at 13/10,000 and is believed to be increasing (3,7). The etiology of autism is still unknown. There is insufficient evidence to implicate any prenatal factor in autism etiology although, there is some evidence to suggest that exposure to pregnancy complications may increase the risk (8). Several researchers have reported on the increasing numbers of sleep problems in children with ASD (4,10,12,15,16,24,34). Sleep problems commonly reported across a range of conditions such as difficulty in settling to sleep, night waking, irregular sleep patterns, short-duration sleep and daytime sleepiness (15,23,34).
Many of the sleep problems are associated with problems of cognitive functioning, learning, attention and school performance (11,17,25,26,31,35). Fewer hours of sleep per night is a predictor of symptoms of ASD and social skills deficits (4,27). Children with ASD who sleep problems were found to have had more internalizing and externalizing behavior problems and poorer adaptive skill development than children with ASD who did not sleep problems (18,19,28,29). However, exploration of the types of sleep difficulties and associated etiological factors in the ASD is still in its infancy (24).
A variety of measurement tools are utilized in sleep assessment, including Electroencephalography (EEG), Polysomnography, Actigraphy and Children’s Sleep Habits Questionnaire (CSHQ). The CSHQ is used to screen sleep problems. Although CSHQ alone is not sufficient for diagnosis or treatment planning. It can provide supplemental information beyond the clinical interview. In addition, questionnaires may be a useful way to monitor treatment progress. To date there has been a limited number of studies on this topic published in Indonesia and Japan. For this study we used the CSHQ-A, to identify sleep problems of children with ASD in Indonesia and Japan. A high total CSHQ score of children with ASD has recently been reported in a study of the sleep disturbances in children with ASD (20). This study investigated the prevalence of sleep problem in children with ASD. Our previous research, showed 3% of Indonesian typically developing (TD) sustained sleep problems. The hypothesis in this study is the prevalence of sleep problems on children with ASD is high. This data could be used to support the management on children with ASD in Indonesia and Japan.
MATERIALS AND METHODS
Methods
A cross sectional study was conducted in Surabaya, Indonesia and Kobe, Japan, from June 1 to December 30, 2014. The sample of this study consisted of 50 children diagnosed with ASD, 25 from Surabaya, Indonesia and 25 from Kobe, Japan. Sample size was calculated based on the total sampling. Children enrolled in the study met the following criteria: age between 4 and 10 years old, stable medical conditions, and no change in medication related to sleep or health status in the past 3 months. ASD diagnosis was made by a pediatrician and confirmed by The Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5) (1). The researcher interviewed the parents/caregivers and filled in a CHSQ-A after the parents were being informed of the study and gave their written consents.
Data were analyzed with Mann-Whitney U test to compare the CSHQ-A scores between Indonesia and Japan, while the proportion of sleep problems was evaluated by chi-square test with 95% confidence interval. Analysis were performed using SPSS 16.0.
This study was approved by the Ethics Committee Faculty of Medicine, Airlangga University, Surabaya, Indonesia and Graduate School of Health Sciences, Kobe University, Japan.
Materials
The CSHQ-A (NICHD SECCYD-Wisconsin) was used in this research to assess the sleep problems, was modified The CSHQ by Owen and only a subset of items was administered, and the response scale was expanded to 5 points (1 = always, 5 = never). The CSHQ-A consisted of 22 questions. These questionnaires were attained primarily by retrospective method with the parents/caregivers recalling on sleep patterns, disturbances, or behaviors (e.g., bed time, sleep behavior, waking during the night, morning wake up). Items of the CSHQ-A are rated on a five point scale ranging from “always” if the sleep behavior occurred 7 times in the past week, “usually” if the behavior occurred 5–6 times in the past week, “sometimes” for 2 to 4 times that week, “rarely” for 1 time that week, and “never” for 0 times that week. A total score of more than 41 on CSHQ was taken as abnormal and indicative of sleep problems (21,22).
RESULT
Fifty children with ASD included in this research, 25 children from Kobe, Japan and 25 children from Surabaya, Indonesia. Eighty two percent (41) children were male and only 18% (9) children were female (Table I)
I. Distribution
Table I.
Characteristics of children with ASD (N = 50)
| Participants | Indonesian Children with ASD (n=25) | Japanese Children with ASD (n=25) | P |
|---|---|---|---|
|
| |||
| Age (Mean ±SD) | 4.8±1.5 | 7.7±1.7 | * |
|
| |||
| Gender | |||
| Male (%) | 21 (84) | 20 (80) | NS |
| Female (%) | 4 (16) | 5 (20) | |
P<0.05(Mann-Whitney U test, Chi-square test)
II. Total score of Children’s Sleep Habits Questionnaire-Abbreviated (CSHQ-A)
The children with ASD in Indonesia had more sleep problems on 2 out of 4 domains of CSHQ-A than Japanese children with ASD (Table II).
Table II.
Total score of CSHQ-A
| Indonesia | Japan | P | |
|---|---|---|---|
| Total bed time | 18.88 ±3.07 | 17.88 ±2.24 | NS |
| Total sleep behavior | 12.36 ±2.29 | 11.04 ±1.24 | NS |
| Total waking during the night | 2.76 ±1.01 | 2.36 ±0.95 | * |
| Total morning wake up | 7.12 ±1.71 | 6.00 ±1.19 | * |
| Total Score | 41.12 ±5.49 | 37.28 ±2.81 | * |
P< 0.05 (Mann-Whitney U test)
Based on CSHQ-A, the prevalence of sleep problems for children with ASD was 60% in Indonesia and 16% in Japan respectively (Table III)
Table III.
Children with ASD who had Sleep Problems
| Sleep Problems | Indonesia (N=25) (%) | Japan (N=25) (%) | P |
|---|---|---|---|
| Yes | 15 (60) | 4 (16) | 0.001* |
| No | 10 (40) | 21 (84) |
Significant (Chi-Square test)
DISCUSSION
The present study showed that the prevalence of sleep problems on children with ASD was 60% in Indonesia and 16% in Japan respectively. The most commonly reported behaviors were child falls asleep in parent’s or sibling’s bed, child goes to bed at the same time at night, child sleeps about the same amount each day and child wakes up by him/herself. An individual sleep problem also was defined as a sleep problem occurring at least two nights per week (37). Children who don’t have enough sleep time or have a poor quality sleep have been shown to have more behavior difficulty, especially in children with ASD (27,28).
Sleep problems in ASD might occur as a result of complex interactions between biological, psychological, social/environmental, and family factors, including child rearing practices that are not conducive to good sleep (5,31). This could be due to sleep being a dynamic and regulated set of behavioral and physiological states and stages (36).
The high prevalence of Indonesian children with ASD in our study (60%) was similar to other studies that found sleep problems are highly prevalent in children with ASD, with rates ranging from 40% to 80% (5,19,23,26,27,32,33). The higher prevalence of sleep disturbance in Indonesian children with ASD due to different characteristics with Japan population that Indonesian children showed higher severity of ASD. Meanwhile, the low prevalence of sleep problems in Japan of children with ASD may not due to the difference in the mean age of children with ASD between two countries (4.8±1.5 vs 7.7±1.7). A study by Hodge (13) found that the sleep problems of children with ASD were not associated with age, but to the reduced sleep duration in children with ASD since the age of 30 months and persisted to adolescence (14). Sleep problems in children with ASD were related to poor quality of life (6) with sleep onset delay being particularly related to melatonin pathway genes (9,32).
Children with ASD who had sleep problems had more internalizing and externalizing behavior problems and poorer adaptive skill development than children with ASD who had no sleep problems (28). Children with ASD had poorer daytime performance and behavior than the TD children (28,29). Comparing our subjects to the TD children in Indonesia, we found 3% of TD children have sleep problems.
In CSHQ-A four specific sleep parameters were assessed, namely bedtime; sleep behavior; waking during the night; and morning wake up. There were significant differences in total waking during the night and morning wake up which showed children with ASD in Indonesia had more sleep problems on 2 out of 4 domains of CSHQ-A when compared to Japanese children with ASD. Thirty one children with ASD (62%) in our study had a good sleep. However Sikora (2012) found the CSHQ have a negative relationship with daytime behavior (30). Insomnia (in particular sleep onset, settling, and night-waking problems) issues are a hallmark of sleep problems in ASD (24). The good sleepers with ASD did not differ from the TD children on CSHQ-A domains (18).
In this study, 41 children (82%) were male and only 9 children (18%) were female. The gender difference in this study was similar to data in the United States that showed ASD affected 1 in 80 boys and the ratio of male and female was 4:1 (3). The gender and age differences in sleep problems may be the reflection of developmental characteristics of children. Gender difference exists in growth pace and physical trait, and equality in personality and temperament, which may result in different behavioral tendency and disease sensitivity (30,37). The mean age in our study was 4.8±1.5 years in Indonesia and 7.7±1.7 years in Japan. To date it is unclear if sleep problems in children with ASD will improve with age. There has been mixed evidence in the literature that show sleep problems in children with ASD might improve with age (23) however, Mayes and Calhoun found no relationship between sleep problems and age (19). Parent-report sleep problems were associated with more daytime sleepiness and more behavior problems (2).
In summary, the prevalence of sleep problems in our study is 60% in Indonesia and 16% in Japan.
ACKNOWLEDGEMENT
The authors wish to thank Director of Dr Soetomo Hospital, Surabaya, Indonesia and Director of Kobe University Hospital for their support of the field investigation.
REFERENCES
- 1.American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Arlington, VA: American Psychiatric Association; 2013. pp. 50–9. [Google Scholar]
- 2.Anders T, Iosif AM, Schwichtenberg AJ, Tang K, Goodlin-Jones B. Sleep and Daytime Functioning: A Short-term Longitudinal Study of Three Preschool-age Comparison Groups. Am J Intellect Dev Disabil. 2012;117(4):275–90. doi: 10.1352/1944-7558-117.4.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Baker SM, Milivojevich A. Gender differences among children with autism spectrum disorder: differential symptom patterns. Glob Adv Health Med. 2013;2(6):8–18. doi: 10.7453/gahmj.2013.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Cohen S, Conduit R, Lockley SW, Rajaratnam SM, Cornish KM. The relationship between sleep and behavior in autism spectrum disorder (ASD): a review. J Neurodev Disord. 2014;6(1):44. doi: 10.1186/1866-1955-6-44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Cortesi F, Giannotti F, Ivanenko A, Johnson K. Sleep in children with autistic spectrum disorder. Sleep Med. 2010;11(7):659–64. doi: 10.1016/j.sleep.2010.01.010. [DOI] [PubMed] [Google Scholar]
- 6.Delahaye J, Kovacs E, Sikora D, Hall TA, Orlich F, Clemons TE, van der Weerd E, Glick L, Kuhlthau K. The relationship between Health-Related Quality of Life and sleep problems in children with Autism Spectrum Disorders. Res Autism Spectr Disord. 2014;8:292–303. [Google Scholar]
- 7.Fombonne E. The changing epidemiology of autism. J Appl Res Intellect Disabil. 2005;18:281–94. [Google Scholar]
- 8.Gardener H, Spiegelman D, Buka SL. Prenatal Risk Factors for Autism: A Comprehensive Meta-analysis. Br J Psychiatry. 2009;195(1):7–14. doi: 10.1192/bjp.bp.108.051672. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Glickman G. Circadian rhythms and sleep in children with autism. Neurosci Biobehav Rev. 2010;34:755–68. doi: 10.1016/j.neubiorev.2009.11.017. [DOI] [PubMed] [Google Scholar]
- 10.Goodlin-Jones BL, Tang K, Liu J, Anders TF. Sleep patterns in preschool-age children with autism, developmental delay, and typical development. J Am Acad Child Adolesc Psychiatry. 2008;47(8):930–8. doi: 10.1097/CHI.ObO13e3181799f7c. [DOI] [PubMed] [Google Scholar]
- 11.Johnson EO, Breslau N. Sleep problems and substance use in adolescence. Drug Alcohol Depend. 2001;64(1):1–7. doi: 10.1016/s0376-8716(00)00222-2. [DOI] [PubMed] [Google Scholar]
- 12.Johnson KP, Giannotti F, Cortesi F. Sleep patterns in autism spectrum disorders. Child Adolesc Psychiatr Clin N Am. 2009;18(4):917–28. doi: 10.1016/j.chc.2009.04.001. [DOI] [PubMed] [Google Scholar]
- 13.Hodge D, Carollo TM, Lewin M, Hoffman CD, Sweeney DP. Sleep patterns in children with and without autism spectrum disorders: developmental comparisons. Res Dev Disabil. 2014;35(7):1631–8. doi: 10.1016/j.ridd.2014.03.037. [DOI] [PubMed] [Google Scholar]
- 14.Humphreys JS, Gringras P, Blair PS, Scott N, Henderson J, Fleming PJ, Emond AM. Sleep patterns in children with autistic spectrum disorders: a prospective cohort study. Arch Dis Child. 2014;99:114–18. doi: 10.1136/archdischild-2013-304083. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Krakowiak P, Goodlin-Jones B, Hertz-Picciotto I, Croen LA, Hansen RL. Sleep problems in children with autism spectrum disorders, developmental delays, and typical development: a population-based study. J Sleep Res. 2008;17(2):197–206. doi: 10.1111/j.1365-2869.2008.00650.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Liu X, Hubbard JA, Fabes RA, Adam JB. Sleep Disturbances and Correlates of Children with Autism Spectrum Disorders. Child Psychiatry Hum Dev. 2006;37:179–91. doi: 10.1007/s10578-006-0028-3. [DOI] [PubMed] [Google Scholar]
- 17.Malow BA. Sleep disorders, epilepsy, and autism. Ment Retard Dev Disabil Res Rev. 2004;10:122–25. doi: 10.1002/mrdd.20023. [DOI] [PubMed] [Google Scholar]
- 18.Malow BA, Marzec ML, McGrew SG, Wang L, Henderson LM, Stone WL. Characterizing sleep in children with autism spectrum disorders: a multidimensional approach. Sleep. 2006;29(12):1563–71. doi: 10.1093/sleep/29.12.1563. [DOI] [PubMed] [Google Scholar]
- 19.Mayes SD, Calhoun SL. Variables related to sleep problems in children with autism. Res Autism Spectr Disord. 2009;3:931–941. [Google Scholar]
- 20.Mushtaq I, Suman P. Study of the Sleep Disturbances in Children with Autism Spectrum Disorder. European Academic Research. 2014;II(1):1100–17. [Google Scholar]
- 21.NICHD SECCYD-Wisconsin Children’s Sleep Habits Questionnaire (Abbreviated) [Cited 20 May 2014]. Available from: http://www.education.uci.edu/childcare/pdf/instrumental_docs/Childrens%20Sleep%20Habits%20Questionnaire%20ID.pdf.
- 22.Owens JA, Spirito A, McGuinn M. The Children’s Sleep Habits Questionnaire (CSHQ): Psychometric Properties of a Survey Instrument for School-Aged Children. Sleep. 2000;23(8):1043–51. [PubMed] [Google Scholar]
- 23.Richdale AL, Prior MR. The sleep/wake rhythm in children with autism. Eur Child Adolesc Psychiatry. 1995;4(3):175–86. doi: 10.1007/BF01980456. [DOI] [PubMed] [Google Scholar]
- 24.Richdale AL. Sleep problems in autism: prevalence, cause and intervention. Dev Med Child Neurol. 1999;41(1):60–6. doi: 10.1017/s0012162299000122. [DOI] [PubMed] [Google Scholar]
- 25.Richdale AL, Schreck KA. Sleep problems in autism spectrum disorders: prevalence, nature, & possible biopsychosocial aetiologies. Sleep Med Rev. 2009;13(6):403–11. doi: 10.1016/j.smrv.2009.02.003. [DOI] [PubMed] [Google Scholar]
- 26.Sadeh A, Gruber R, Raviv A. Sleep, neurobehavioral functioning, and behavior problems in school-age children. Child Dev. 2002;73(2):405–17. doi: 10.1111/1467-8624.00414. [DOI] [PubMed] [Google Scholar]
- 27.Sadeh A, Gruber R, Raviv A. The effects of sleep restriction and extension on school-age children: what a difference an hour makes. Child Dev. 2003;74(2):444–55. doi: 10.1111/1467-8624.7402008. [DOI] [PubMed] [Google Scholar]
- 28.Schreck KA, Mulick JA. Parental report of sleep problems in children with autism. J Autism Dev Disord. 2000;30(2):127–35. doi: 10.1023/a:1005407622050. [DOI] [PubMed] [Google Scholar]
- 29.Shahid A, Wilkinson K, Marcu S, Shapiro CM. Children’s Sleep Habits Questionnaire (CSHQ) in Stop. In: Shahid A, Wilkinson K, Marcu S, Shapiro CM, editors. That and One hundred other sleep scales. 2012. pp. 119–122. [Google Scholar]
- 30.Sikora DM, Johnson K, Clemons T, Katz T. The Relationship between sleep problems and daytime behavior in children of different ages with Autism Spectrum Disorders. Pediatrics. 2012;130:S83–S90. doi: 10.1542/peds.2012-0900F. [DOI] [PubMed] [Google Scholar]
- 31.Sivertsen B, Posserud MB, Gillberg C, Lundervold AJ, Hysing M. Sleep problems in children with autism spectrum problems: a longitudinal population-based study. Autism. 2012;16(2):139–50. doi: 10.1177/1362361311404255. [DOI] [PubMed] [Google Scholar]
- 32.Smedje H, Broman JE, Hetta J. Associations between disturbed sleep and behavioural difficulties in 635 children aged six to eight years: a study based on parents’ perceptions. Eur Child Adolesc Psychiatry. 2001;10(1):1–9. doi: 10.1007/s007870170041. [DOI] [PubMed] [Google Scholar]
- 33.Veatch OJ, Pendergast JS, Allen MJ, Leu RM, Johnson CH, Elsea SH, Malow BA. Genetic variation in melatonin pathway enzymes in children with autism spectrum disorder and comorbid sleep onset delay. J Autism Dev Disord. 2015;45(1):100–10. doi: 10.1007/s10803-014-2197-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Wiggs L. Sleep problems in children with developmental disorders. J R Soc Med. 2001;94:177–9. doi: 10.1177/014107680109400406. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Wiggs L, Stores G. Sleep patterns and sleep disorders in children with autistic spectrum disorders: insights using parent report and actigraphy. Dev Med Child Neurol. 2004;46(6):372–80. doi: 10.1017/s0012162204000611. [DOI] [PubMed] [Google Scholar]
- 36.Wolfson AR, Carskadon MA. Understanding adolescents’ sleep patterns and school performance: a critical appraisal. Sleep Med Rev. 2003;7(6):491–506. doi: 10.1016/s1087-0792(03)90003-7. [DOI] [PubMed] [Google Scholar]
- 37.Zhang Z, Chen T, Jin X, Yan C, Shen X, Li S. Sleep Patterns, Sleep Problems and Associations with Reported Sleep Quality in Chinese School-Aged Children. Am J Public Health Res. 2013;1(4):93–100. [Google Scholar]