RESEARCH ARTICLE Assessment of Sleep Problems and Related Risk Factors Observed in Turkish Children with Autism Spectrum Disorders Tuba Mutluer, Sevcan Karakoc Demirkaya, and Osman Abali Sleep problems are common and difficult to manage in children with autism spectrum disorders (ASD). Another major adverse impact of sleep problems is that they exacerbate behavioral problems. To assess sleep problems and possible behavioral risk factors in detail, we aimed to compare sleep habits of children with ASD, with healthy children. The relationship between sleep difficulties and concomitant behavioral problems such as repetitive behaviors, hyperactivity, and social withdrawal were also examined. Hundred and seventeen children and adolescents including 64 with the diagnosis of ASD and 53 healthy subjects were enrolled in the study. Diagnostic Interview for ASD was performed according to DSM-IV-TR. Socio-demographical data form and childhood autism rating scale were filled by researchers. Aberrant behavior checklist (ABC), child behavior checklist and pediatric sleep questionnaire (PSQ) were completed by the parents of the children. Children with ASD had higher frequency of sleep problems, snoring, breathing problems, behavioral problems compared with healthy children (for all parameters; P < 0.001). A positive correlation was identified between the total score of PSQ and the total score of ABC (P < 0.05, Spearman correlation coefficient: 0.347). Sleep latency was prolonged in children with ASD compared with healthy subjects (P < 0.001). In accordance with the current literature, children with ASD were subject to sleep problems significantly more than the control group. Identified risk factors for sleep problems in ASD children were behavioral factors such as stereotyC 2015 International Socipies, self-mutilation, hyperactivity, and social withdrawal. Autism Res 2016, 9: 536–542. V ety for Autism Research, Wiley Periodicals, Inc. Keywords: autism; spectrum; sleep; disorder; neurodevelopmental; behavior
Introduction Sleep is essential for human life and involves both physiological and behavioral processes. The relationship between sleep and brain development is complicated [Ednick et al., 2009]. Sleep problems and psychiatric problems are mostly affected by each other [Dahl, 2007]. Previous research suggests that sleep problems are more common in autism spectrum disorders (ASD) children than healthy individuals. Sleep disorders are detected in 70–75% of the children with ASD, vs. 45– 50% of healthy children [Liu, Hubbard, Fabes, & Adam, 2006; Polimeni, Richdale, & Francis, 2005; Richdale, 1999; Wiggs, 2001]. Although more studies on sleep problems and related risk factors in ASD children have been published in the last decade, exact correlations are yet to be revealed [Aitken, 2012]. When negative impacts of disturbances in sleep on cognitive development, memory, learning, attention, mood, and behaviors are considered, it is naturally expected that these would also have some negative
effects on clinical course of children with ASD [Mitchell & Thompson, 2003; Souders et al., 2009]. Sleep disturbances may lead to worsening of autistic symptoms, and may alter attention, together with learning which in turn decrease effectivity of special education programs for autism, and social functioning [Souders et al., 2009]. Recent findings suggest that sleep disturbances in children may negatively affect parents’ sleep and mental health. Parents who have a child with a disability like ASD are known to suffer more often with such sleep problems [Hodge, Hoffman, Sweeney, & Riggs, 2013]. Core symptoms in ASD, high rate of concomitant behavioral problems and its unknown etiopathogenesis may affect sleep [Souders et al., 2009]. The most recent study on relationship between autism symptom severity and sleep problems was conducted by Adams et al. The results of this analysis suggest a bidirectional relationship. Adams et al. emphasize the severity of ASD as a strong predictor for sleep disturbances and that
From the Van Regional Education and Research Hospital, Child and Adolescent Psychiatry Clinic (T.M.,); Department of Child and Adolescent Psychiatry, Adnan Menderes University (S.K.D.,); Department of Child and Adolescent Psychiatry, Istanbul University Istanbul Medical Faculty (O.A.) Received March 03, 2015; accepted for publication July 28, 2015 Conflict of interest: None to declare. Address for correspondence and reprints: Tuba Mutluer, Van Regional Education and Research Hospital, Child and Adolescent Psychiatry Clinic. E-mail: [email protected] Published online 13 October 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1542 C 2015 International Society for Autism Research, Wiley Periodicals, Inc. V
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Autism Research 9: 536–542, 2016
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disordered sleep exacerbates daytime symptoms [Adams, Matson, Cervantes, & Goldin, 2014]. While there is an increase in number of studies in sleep problems in ASD children, sleep related symptoms have not been assessed in detail with standardized measures. No study on sleep habits of ASD children in our country, Turkey, has been conducted. Hereby, we aimed: 1. To investigate sleep problems encountered in ASD and healthy children. 2. To investigate sleep related problems observed in these two groups in detail. 3. To identify the risk/protective behavioral factors which may cause a sleep problem in ASD group.
Methods Sample Size Prior to selection of sample, a power analysis (alfa 5 0.05, power of 0.80, 1:1 ratio) was conducted. When we used expected prevalence of sleep problems in ASD group and healthy group as 70% and 45%, respectively, minimum sample size for each group was calculated as 41 [Aitken, 2012]. Sample Sixty-four children and adolescents (aged 6–18 years old) with a clinical diagnosis of ASD “study group,” and 53 healthy children and adolescents “control group” were enrolled in our study. These two groups were matched for age, gender, and monthly family income. The study group and their parents who were eligible for inclusion criteria, were randomly recruited from special education centers on autism. Control group was composed of typically developing children who had no psychiatric history, who were enrolled randomly from state elementary school located in the same region as those special education centers. Inclusion criteria included the followings: (a) having the diagnosis of ASD confirmed by expert clinicians for the study group; (b) being mentally and physically healthy for the control group; and (c) having parents with at least elementary school level education. Exclusion criteria were: (a) use of pharmacological agents within the last month; (b) diagnosis of a genetic, metabolic, neurological, respiratory, or chronic infectious disorder; and (c) history of severe head injury and organic brain damage. Instruments and Procedure Socio-demographic data form: This form, which sets out detailed information about children’s sociodemographic status, psychomotor development, medi-
INSAR
cal, clinical, and family history, was prepared by the investigators. It was completed by the investigators during the assessment of children and their family. Childhood autism rating scale (CARS): CARS was developed by Shopler and colleagues in 1971 [Schopler & Reichler, 1971]. The Turkish version of the CARS was shown to be reliable and valid by Sucuoglu et al. CARS is a behavior observation scale in which a trained observer rates the child’s behavior on each of 15 dimensions or symptoms. It yields a total score which is useful as a continuous measure of the severity of autism. It is also possible to categorize the individual based on this total score as; not autism, mild-moderate autism, and severe autism [Sucuoglu, Oktem, Akkok, & Gokler, 1996]. Aberrant behavior checklist (ABC): ABC was developed by Aman and his colleagues in 1987 [Aman, Singh, & Turbott, 1987]. The reliability and validity of the Turkish version of ABC was approved [Karabekiroglu & Aman, 2009]. It has 58 items that are rated on a fourpoint scale ranging from 0 (“no problem at all”) to 3 (“the problem is severe in degree”). The items are scored on basis of following five subscales: (a) ABC- I: Irritability, Agitation, Crying; (b) ABC-II: Lethargy and social withdrawal; (c) ABC-III: Stereotypic Behavior; (d) ABCIV: Hyperactivity, Noncompliance; and (e) ABC-V: Inappropriate Speech. It has been shown that ABC subscales are significantly correlated with analogous scores derived by direct observation of behavior. Pediatric sleep questionnaire (PSQ): PSQ was designed by [Chervin, Hedger, Dillon & Pituch, 2000]. The reliability and validity of the Turkish version of PSQ was demonstrated [Oner et al., 2000]. PSQ has essentially two versions: A shorter one, which has been validated for sleep-related breathing disorders, and an extended version, which deals with a wider range of sleep disturbances. The extended version was used in this study. Child behavior checklist (CBCL) for ages 4–18: (CBCL) is designed by Achenbach in 1991 to obtain ratings of child’s behavioral/emotional problems from parents [Achenbach, 1991]. It is composed of 118 items related to several childhood problems. It was translated to Turkish by Akcakin and Savasir which was later standardized by Erol et al. Behavioral problems are classified in three major groups: Total behavior, internalizing behavior (withdrawal, somatic complaints, and anxious/depressed behavior), and externalizing behavior (delinquent and aggressive behavior) [Erol, Arslan, & Akcakın, 1995]. Ethics Study was approved by Ethical Committee of Medical Faculty of Istanbul University, and permissions were acquired from relevant authorities. Informed consent was obtained from all parents and their children.
Mutluer et al./Sleep problems and related risk factors in autism
537
Table 1. Sleep Related Problems in ASD Group and the Control Group Sleep related problem scores Snoring Breathing problems Other sleep problems Total sleep problems Periodic movement disorder of sleep Insomnia Sleepiness
ASD (M 6 SD)
Control (M 6 SD)
t
P
1.3 6 1.4 2.9 6 2.2 2.08 6 1.5 23.8 6 11.7 0.29 6 0.6 1.84 6 0.87 2.15 6 1.62
0.3 6 0.7 1.1 6 1.5 0.7 6 0.8 10.7 6 6.8 0.07 6 0.26 0.58 6 0.66 0.89 6 1.01
4.61 4.91 5.54 7.05 2.37 8.56 4.89
Introduction Sleep is essential for human life and involves both physiological and behavioral processes. The relationship between sleep and brain development is complicated [Ednick et al., 2009]. Sleep problems and psychiatric problems are mostly affected by each other [Dahl, 2007]. Previous research suggests that sleep problems are more common in autism spectrum disorders (ASD) children than healthy individuals. Sleep disorders are detected in 70–75% of the children with ASD, vs. 45– 50% of healthy children [Liu, Hubbard, Fabes, & Adam, 2006; Polimeni, Richdale, & Francis, 2005; Richdale, 1999; Wiggs, 2001]. Although more studies on sleep problems and related risk factors in ASD children have been published in the last decade, exact correlations are yet to be revealed [Aitken, 2012]. When negative impacts of disturbances in sleep on cognitive development, memory, learning, attention, mood, and behaviors are considered, it is naturally expected that these would also have some negative
effects on clinical course of children with ASD [Mitchell & Thompson, 2003; Souders et al., 2009]. Sleep disturbances may lead to worsening of autistic symptoms, and may alter attention, together with learning which in turn decrease effectivity of special education programs for autism, and social functioning [Souders et al., 2009]. Recent findings suggest that sleep disturbances in children may negatively affect parents’ sleep and mental health. Parents who have a child with a disability like ASD are known to suffer more often with such sleep problems [Hodge, Hoffman, Sweeney, & Riggs, 2013]. Core symptoms in ASD, high rate of concomitant behavioral problems and its unknown etiopathogenesis may affect sleep [Souders et al., 2009]. The most recent study on relationship between autism symptom severity and sleep problems was conducted by Adams et al. The results of this analysis suggest a bidirectional relationship. Adams et al. emphasize the severity of ASD as a strong predictor for sleep disturbances and that
From the Van Regional Education and Research Hospital, Child and Adolescent Psychiatry Clinic (T.M.,); Department of Child and Adolescent Psychiatry, Adnan Menderes University (S.K.D.,); Department of Child and Adolescent Psychiatry, Istanbul University Istanbul Medical Faculty (O.A.) Received March 03, 2015; accepted for publication July 28, 2015 Conflict of interest: None to declare. Address for correspondence and reprints: Tuba Mutluer, Van Regional Education and Research Hospital, Child and Adolescent Psychiatry Clinic. E-mail: [email protected] Published online 13 October 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1542 C 2015 International Society for Autism Research, Wiley Periodicals, Inc. V
536
Autism Research 9: 536–542, 2016
INSAR
disordered sleep exacerbates daytime symptoms [Adams, Matson, Cervantes, & Goldin, 2014]. While there is an increase in number of studies in sleep problems in ASD children, sleep related symptoms have not been assessed in detail with standardized measures. No study on sleep habits of ASD children in our country, Turkey, has been conducted. Hereby, we aimed: 1. To investigate sleep problems encountered in ASD and healthy children. 2. To investigate sleep related problems observed in these two groups in detail. 3. To identify the risk/protective behavioral factors which may cause a sleep problem in ASD group.
Methods Sample Size Prior to selection of sample, a power analysis (alfa 5 0.05, power of 0.80, 1:1 ratio) was conducted. When we used expected prevalence of sleep problems in ASD group and healthy group as 70% and 45%, respectively, minimum sample size for each group was calculated as 41 [Aitken, 2012]. Sample Sixty-four children and adolescents (aged 6–18 years old) with a clinical diagnosis of ASD “study group,” and 53 healthy children and adolescents “control group” were enrolled in our study. These two groups were matched for age, gender, and monthly family income. The study group and their parents who were eligible for inclusion criteria, were randomly recruited from special education centers on autism. Control group was composed of typically developing children who had no psychiatric history, who were enrolled randomly from state elementary school located in the same region as those special education centers. Inclusion criteria included the followings: (a) having the diagnosis of ASD confirmed by expert clinicians for the study group; (b) being mentally and physically healthy for the control group; and (c) having parents with at least elementary school level education. Exclusion criteria were: (a) use of pharmacological agents within the last month; (b) diagnosis of a genetic, metabolic, neurological, respiratory, or chronic infectious disorder; and (c) history of severe head injury and organic brain damage. Instruments and Procedure Socio-demographic data form: This form, which sets out detailed information about children’s sociodemographic status, psychomotor development, medi-
INSAR
cal, clinical, and family history, was prepared by the investigators. It was completed by the investigators during the assessment of children and their family. Childhood autism rating scale (CARS): CARS was developed by Shopler and colleagues in 1971 [Schopler & Reichler, 1971]. The Turkish version of the CARS was shown to be reliable and valid by Sucuoglu et al. CARS is a behavior observation scale in which a trained observer rates the child’s behavior on each of 15 dimensions or symptoms. It yields a total score which is useful as a continuous measure of the severity of autism. It is also possible to categorize the individual based on this total score as; not autism, mild-moderate autism, and severe autism [Sucuoglu, Oktem, Akkok, & Gokler, 1996]. Aberrant behavior checklist (ABC): ABC was developed by Aman and his colleagues in 1987 [Aman, Singh, & Turbott, 1987]. The reliability and validity of the Turkish version of ABC was approved [Karabekiroglu & Aman, 2009]. It has 58 items that are rated on a fourpoint scale ranging from 0 (“no problem at all”) to 3 (“the problem is severe in degree”). The items are scored on basis of following five subscales: (a) ABC- I: Irritability, Agitation, Crying; (b) ABC-II: Lethargy and social withdrawal; (c) ABC-III: Stereotypic Behavior; (d) ABCIV: Hyperactivity, Noncompliance; and (e) ABC-V: Inappropriate Speech. It has been shown that ABC subscales are significantly correlated with analogous scores derived by direct observation of behavior. Pediatric sleep questionnaire (PSQ): PSQ was designed by [Chervin, Hedger, Dillon & Pituch, 2000]. The reliability and validity of the Turkish version of PSQ was demonstrated [Oner et al., 2000]. PSQ has essentially two versions: A shorter one, which has been validated for sleep-related breathing disorders, and an extended version, which deals with a wider range of sleep disturbances. The extended version was used in this study. Child behavior checklist (CBCL) for ages 4–18: (CBCL) is designed by Achenbach in 1991 to obtain ratings of child’s behavioral/emotional problems from parents [Achenbach, 1991]. It is composed of 118 items related to several childhood problems. It was translated to Turkish by Akcakin and Savasir which was later standardized by Erol et al. Behavioral problems are classified in three major groups: Total behavior, internalizing behavior (withdrawal, somatic complaints, and anxious/depressed behavior), and externalizing behavior (delinquent and aggressive behavior) [Erol, Arslan, & Akcakın, 1995]. Ethics Study was approved by Ethical Committee of Medical Faculty of Istanbul University, and permissions were acquired from relevant authorities. Informed consent was obtained from all parents and their children.
Mutluer et al./Sleep problems and related risk factors in autism
537
Table 1. Sleep Related Problems in ASD Group and the Control Group Sleep related problem scores Snoring Breathing problems Other sleep problems Total sleep problems Periodic movement disorder of sleep Insomnia Sleepiness
ASD (M 6 SD)
Control (M 6 SD)
t
P
1.3 6 1.4 2.9 6 2.2 2.08 6 1.5 23.8 6 11.7 0.29 6 0.6 1.84 6 0.87 2.15 6 1.62
0.3 6 0.7 1.1 6 1.5 0.7 6 0.8 10.7 6 6.8 0.07 6 0.26 0.58 6 0.66 0.89 6 1.01
4.61 4.91 5.54 7.05 2.37 8.56 4.89
