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Pediatrics International (2015) 57, 690–693
doi: 10.1111/ped.12620
Original Article
Behavioral symptoms and sleep problems in children with anxiety disorder Yoshitaka Iwadare,1 Yuichi Kamei,2 Masahide Usami,1 Hirokage Ushijima,1 Tetsuya Tanaka,1 Kyota Watanabe,1 Masaki Kodaira3 and Kazuhiko Saito3 1 Department of Child and Adolescent Psychiatry, National Center for Global Health and Medicine, Kohnodai Hospital, Ichikawa, 2Department of Clinical Laboratory, National Center Hopsital, National Center of Neurology and Psychiatry, Kodaira and 3Department of Child and Adolescent Psychiatry, Aiiku Hospital, Minato, Japan Abstract
Background: Sleep disorders are frequently associated with childhood behavioral problems and mental illnesses such as anxiety disorder. To identify promising behavioral targets for pediatric anxiety disorder therapy, we investigated the associations between specific sleep and behavioral problems. Methods: We conducted retrospective reviews of 105 patients aged 4–12 years who met the DSM-IV criteria for primary diagnosis of generalized anxiety disorder (n = 33), separation anxiety disorder (n = 23), social phobia (n = 21), or obsessive compulsive disorder (n = 28). Sleep problems were evaluated using the Children’s Sleep Habits Questionnaire (CSHQ) and behavioral problems by the Spence Children’s Anxiety Scale, Oppositional Defiant Behavior Inventory (ODBI), and Depression Self-Rating Scale for Children. Results: Depressive behavior was weakly correlated with CSHQ subscores for sleep onset delay and night waking but not with total sleep disturbance. Anxiety was correlated with bedtime resistance, night waking, and total sleep disturbance score. Oppositional defiance was correlated with bedtime resistance, daytime sleepiness, sleep onset delay, and most strongly with total sleep disturbance. On multiple regression analysis ODBI score had the strongest positive association with total sleep disturbance and the strongest negative association with total sleep duration. Conclusions: Sleep problems in children with anxiety disorders are closely related to anxiety and oppositional defiant symptoms.
Key words anxiety disorder, child, Children’s Sleep Habits Questionnaire, oppositional defiance, sleep.
Sleep disruption in children is associated with a more severe form of anxiety illness and independently predicts impairment in daytime functioning beyond anxiety symptomatology.1,2 In addition, sleep deficiency and sleep problems interfere with cognitive function and induce several problematic daytime behaviors, including hyperkinesis, attention deficit, and emotional instability, in children.3–9 Sleep-related problems in early childhood predict later emotional and behavioral disturbances, including clinical anxiety.10,11 Sleep problems are highly prevalent among children with psychiatric disorders, including anxiety disorder, and sleep quality is an important consideration in pediatric psychiatry. Little research has focused, however, on sleep disturbance in children presenting clinically significant anxiety disorders1,2,12,13 or on the relationships between behavioral symptoms and sleeprelated problems. The aim of this study was to assess these
Correspondence: Yoshitaka Iwadare, MD PhD, Department of Child and Adolescent Psychiatry, National Center of Global Health and Medicine, Kohnodai Hospital, 1-7-1 Kohnodai, Ichikawa, Chiba 2728516, Japan. Email: [email protected] Received 3 September 2014; revised 24 December 2014; accepted 23 January 2015.
© 2015 Japan Pediatric Society
relationships by examining the correlation between sleep quality and behavioral problems in children with anxiety disorder.
Methods Participants
Retrospective chart reviews of children presenting to the National Center for Global Health and Medicine, Kohnodai Hospital, were conducted between September 2007 and February 2011. Participants were 105 children aged 4–12 years (mean ± SD: 9.1 ± 2.1 years; 54 girls) who were referred to Kohnodai Hospital, National Center for Global Health and Medicine, Child and Adolescent Psychiatry. All patients met the DSM-IV criteria for a primary diagnosis of generalized anxiety disorder (GAD; n = 33), separation anxiety disorder (SAD; n = 23), social phobia (SP; n = 21), or obsessive compulsive disorder (OCD; n = 28). Eighteen patients (17.1%) also met the criteria for at least one other disorder. The most common comorbid diagnoses were pervasive developmental disorder (n = 13) and Tourette syndrome (n = 2). The exclusion criteria included a history of psychotropic drugs, bipolar disorder, psychosis, suicidal ideation, and mental retardation. (Mental retardation was added to the exclusion criteria because this study included self-report questionnaire.) This study
Table 1 lists the correlations among CSHQ subscore, age, and behavioral symptom scores (SCAS, DSRS-C, and ODBI scores). Age was significantly negatively correlated with CSHQ subscore for bedtime resistance (r = −0.36, P < 0.01), sleep anxiety (r = −0.26, P < 0.01), parasomnias (r = −0.32, P < 0.01), and total
– −0.04 – 0.67** −0.10 – −0.12 0.12 −0.05 – 0.15 0.10 0.42** 0.04 – 0.15 −0.05 0.13 0.42** 0.02 – 0.23* 0.31** 0.19 0.10 0.13 0.18 0.04 0.29** 0.36** −0.09 – −0.01 0.27* 0.13 0.08 0.25* 0.34** 0.07 0.05 0.10 0.27* −0.18 – 0.30* 0.22 −0.02 0.23* 0.17 0.00 0.24* −0.02 −0.09 0.10 0.10 −0.22
3 2
1 – 0.15 −0.08 −0.21* −0.36** 0.09 0.19 −0.26** −0.01 −0.32** 0.00 0.11 −0.14 −0.30** 2.14 5.64 16.02 14.11 3.23 0.77 1.68 2.42 1.34 1.69 0.62 3.26 7.86 69.24
SD Mean
9.09 12.70 32.14 22.62 11.35 1.64 4.44 7.08 3.90 9.04 3.30 12.43 49.11 528.98 Age (years) DSRS-C SCAS ODBI Bedtime resistance Sleep onset delay Sleep duration Sleep anxiety Night waking Parasomnias Sleep-disordered breathing Daytime sleepiness Total sleep disturbance Total sleep duration (min)
Results
Table 1 Age, behavioral symptom scores and CSHQ subscores: Correlations
Spearman’s correlation coefficients were calculated to assess the relationship between specific sleep problems (CSHQ total and subscores) and individual behavioral trait scores (total SCAS, ODBI, and DSRS-C scores). The relationship between age and all psychometric/behavioral test scores was also assessed. Statistical analysis was performed using SPSS version 19 (SPSS Inc., Chicago, IL, USA). Full model multiple regression analysis was used for the following. First, it was performed to estimate the relative influence of behavioral trait and sleeping problems (CSHQ subscores) on anxiety problems (SCAS). The following variables were tested in the analysis for individual traits: (i) age; (ii) DSRS-C; (iii) ODBI; and (iv) CSHQ subscore. Second, it was performed to estimate the relative influence of each behavioral trait on specific sleeping problems (CSHQ subscore). The following variables were tested in the analysis for individual traits: (i) age’ (ii) DSRS-C; (iii) SCAS; and (iv) ODBI. Variables with P < 0.05 were considered statistically significant.
4
Statistical analysis
691
*P < 0.05, **P < 0.01. CSHQ, Children’s Sleep Habits Questionnaire; DSRS-C, Birleson Depression Self-Rating Scale For Children; ODBI, Oppositional Defiant Behavior Inventory; SCAS, Spence Children’s Anxiety Scale.
5
6
CSHQ items
The Spence Children’s Anxiety Scale (SCAS) is a 38-item selfreport questionnaire that assesses multiple symptoms of childhood anxiety disorders on the basis of the current diagnostic criteria.15 The Oppositional Defiant Behavior Inventory (ODBI) is composed of 18 items describing concrete oppositional behaviors that are graded on a 4-point scale ranging from 0 (rarely) to 3 (always).16,17 The Birleson Depression Self-Rating Scale for Children (DSRS-C) is an 18-item measure of depressive symptoms in children.18
7
8
Behavioral symptom scores
– 0.33** 0.14 0.04 0.24* 0.67** 0.00
9
10
11
The Children’s Sleep Habits Questionnaire (CSHQ) is a selfreport questionnaire for parents on the sleep habits and sleep status of children aged 4–12 years.14 The questionnaire includes 38 items that are designed to assess child sleep behavior over the past week and are rated on a 3-point scale. CSHQ yields a total sleep problem score and subscores corresponding to specific problem areas including bedtime resistance, sleep anxiety, sleep onset delay, parasomnias, night waking, sleep-disordered breathing, and daytime sleepiness.
– −0.04 0.06 0.10 0.03 0.29** 0.41** −0.21*
Children’s Sleep Habits Questionnaire
– 0.37** 0.17 0.34** 0.03 0.04 0.42** 0.55** 0.07
12
Measures
– 0.30** 0.04 0.84** 0.30** 0.21* 0.09 0.23* 0.74** 0.03
13
14
was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of the National Center for Global Health and Medicine.
–
Sleep problems and anxiety disorder
© 2015 Japan Pediatric Society
692 Y Iwadare et al. Discussion
Table 2 Significant indicators of CSHQ score Total sleep disturbance Age DSRS-C SCAS ODBI R = 0.433; F(4,58) = 3.334; P < 0.05
β 0.007 −0.068 0.251 0.389
P 0.953 0.605 0.054 0.003
Bedtime resistance Age DSRS-C SCAS ODBI R = 0.501; F(4,58) = 4.850; P < 0.01
β −0.314 −0.147 0.316 0.143
P 0.011 0.244 0.012 0.247
Night waking Age DSRS-C SCAS ODBI R = 0.433; F(4,58) = 3.417; P < 0.05
β 0.085 0.049 0.369 0.227
P 0.497 0.705 0.005 0.078
Daytime sleepiness Age DSRS-C SCAS ODBI R = 0.403; F(4,58) = 2.809; P < 0.05
β 0.193 −0.099 −0.004 0.413
P 0.132 0.455 0.976 0.002
Total sleep duration Age DSRS-C SCAS ODBI R = 0.418; F(4,58) = 2.907; P < 0.05
β −0.345 0.034 −0.171 −0.322
P 0.010 0.804 0.207 0.019
DSRS-C, Birleson Depression Self-Rating Scale For Children, ODBI, Oppositional Defiant Behavior Inventory, SCAS, Spence Children’s Anxiety Scale.
sleep duration (r = −0.30 P < 0.01). DSRS-C score was significantly positively correlated with sleep onset delay (r = 0.23, P < 0.05) and night waking (r = 0.24, P < 0.05). SCAS score was significantly positively correlated with bedtime resistance (r = 0.27, P < 0.05), sleep anxiety (r = 0.25, P < 0.05), night waking (r = 0.34, P < 0.01), and total sleep disturbance (r = 0.27, P < 0.05). ODBI score was significantly positively correlated with bedtime resistance (r = 0.23, P < 0.05), sleep onset delay (r = 0.31, P < 0.01), daytime sleepiness (r = 0.29, P < 0.01), and total sleep disturbance (r = 0.36, P < 0.01). On multiple regression analysis with SCAS as the dependent variable, there were no factors significantly associated with SCAS. Table 2 presents multiple regression analysis showing the relative strength of the associations between behavioral symptom tests and each CSHQ subscore (sleep problem). Total sleep disturbance was most strongly associated with ODBI. Bedtime resistance was mainly influenced by SCAS, followed by age. Night waking was influenced by SCAS and daytime sleepiness by ODBI. Total sleep duration (min) was influenced most strongly by age, followed by ODBI. © 2015 Japan Pediatric Society
CSHQ score, age, and behavioral symptom score
In this group of children with anxiety disorders (GAD, SAD, SP, or OCD), anxiety symptoms were associated with general sleep disturbance and with several more specific sleep-related problems. Depression as measured using DSRS-C was only weakly correlated with two CSHQ subscores but not with the total score, possibly because of the age limit of the study group (≤12 years). Alfano et al. reported that anxiety symptoms are associated with sleep problems in youth of all ages, whereas depressive symptoms are more strongly associated with sleep problems among adolescents.19 Parents of anxious young children have reported greater bedtime resistance, sleep anxiety, and parasomnias in children.1 Their findings are consistent with the present findings of significant negative correlations between age and bedtime resistance, sleep anxiety, parasomnias, and total sleep duration (Table 1). Influence of factors on SCAS and CSHQ score
There were no significant influencing factors on SCAS, indicating that there are other factors involved in anxiety, and illustrating the limitations of the present study. In contrast, the factor most strongly influencing CSHQ subscores for bedtime resistance and night waking was anxiety (SCAS), indicating that anxiety symptoms affect the capacity to fall and stay asleep. Total sleep disturbance, daytime sleepiness, and total sleep duration were most strongly influenced by oppositional defiance. Previous reports have also identified an association between sleep disturbance and oppositional defiant symptoms,20–22 and conduct problems have been linked to other sleep disorder symptoms such as sleep-disordered breathing, restless legs syndrome (RLS), and periodic limb movement syndrome (PLMS).20 It has also been reported that patients with conduct disorder/oppositional defiant disorder (CD/ODD) sleep fewer hours and their sleep is less restorative.21 Further, Shanahan et al. found that sleep problems predict an increased prevalence of ODD later in life and that ODD predicts an increase in sleep problems over time.22 Children with anxiety disorder and sleep problems are more likely to have daytime sleepiness, which in turn can lead to oppositional defiant behavior as younger children cannot verbalize their own sleep problems. Sleep complains are common in child anxiety disorders.23 Additionally, sleep problems induced a variety of cognitive function and problematic behaviors (hyperkinesis, attention deficit, and unstable emotions).3–7,9,24 Improving sleep problems with anxiety disorder in children may ease these cognitive and behavioral problems. Therefore medical treatment of anxiety disorders in children should focus on the symptoms of oppositional defiance. While sleep problems are related to depressive symptoms in adolescents,25,26 sleep problems in children with anxiety disorders are more closely related to anxiety and oppositional defiance symptoms. A limitation of this study is that CSHQ was completed by parents, who were asked whether they were aware of problems in their children’s sleep behavior. Therefore, unless parents are
Sleep problems and anxiety disorder aware of the problems, the CSHQ may not be reliable. In addition, there was no control group and no long-term follow-up assessment. To confirm the present findings, it will be necessary to objectively evaluate sleep status in children with anxiety disorders in a controlled environment (a sleep laboratory) using polysomnography. Because the relationship between sleep disturbance, anxiety, and defiant behaviors is complicated, more specific studies are needed.
Acknowledgments This work was supported by a grant from the National Center for Global Health and Medicine (22-120).
References 1 Alfano CA, Ginsburg GS, Kingery JN. Sleep-related problems among children and adolescents with anxiety disorders. J. Am. Acad. Child Adolesc. Psychiatry 2007; 46: 224–32. 2 Storch EA, Murphy TK, Lack CW, Geffken GR, Jacob ML, Goodman WK. Sleep-related problems in pediatric obsessivecompulsive disorder. J. Anxiety Disord. 2008; 22: 877–85. 3 Nixon GM, Thompson JMD, Han DY et al. Short sleep duration in middle childhood: Risk factors and consequences. Sleep 2008; 31: 71–8. 4 Ng EP, Ng DK, Chan CH. Sleep duration, wake/sleep symptoms, and academic performance in Hong Kong Secondary School Children. Sleep Breath. 2009; 13: 357–67. 5 Sampei M, Dakeishi M, Wood DC, Murata K. Impact of total sleep duration on blood pressure in preschool children. Biomed. Res. 2006; 27: 111–15. 6 Owens JA, Fernando S, McGuinn M. Sleep disturbance and injury risk in young children. Behav. Sleep Med. 2005; 3: 18– 31. 7 Fallone G, Acebo C, Seifer R, Carskadon MA. Experimental restriction of sleep opportunity in children: Effects on teacher ratings. Sleep 2005; 28: 1561–67. 8 Kaneita Y, Ohida T, Osaki Y et al. Association between mental health status and sleep status among adolescents in Japan: A nationwide cross-sectional survey. J. Clin. Psychiatry 2007; 68: 1426– 35. 9 Carvalho Bos S, Gomes A, Clemente V et al. Sleep and behavioral/ emotional problems in children: A population-based study. Sleep Med. 2009; 10: 66–74. 10 Gregory AM, Eley TC, O’Connor TG, Plomin R. Etiologies of associations between childhood sleep and behavioral problems in a large twin sample. J. Am. Acad. Child Adolesc. Psychiatry 2004; 43: 744–51.
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11 Gregory AM, O’Connor TG. Sleep problems in childhood: A longitudinal study of developmental change and association with behavioral problems. J. Am. Acad. Child Adolesc. Psychiatry 2002; 41: 964–71. 12 Alfano CA, Pina AA, Zerr AA, Villalta IK. Pre-sleep arousal and sleep problems of anxiety-disordered youth. Child Psychiatry Hum. Dev. 2010; 41: 156–67. 13 Chase RM, Pincus DB. Sleep-related problems in children and adolescents with anxiety disorders. Behav. Sleep Med. 2011; 9: 224–36. 14 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: 1043–51. 15 Spence SH. A measure of anxiety symptoms among children. Behav. Res. Ther. 1998; 36: 545–66. 16 Harada Y, Saitoh K, Iida J et al. The reliability and validity of the Oppositional Defiant Behavior Inventory. Eur. Child Adolesc. Psychiatry 2004; 13: 185–90. 17 Harada Y, Saitoh K, Iida J et al. Establishing the cut-off point for the Oppositional Defiant Behavior Inventory. Psychiatry Clin. Neurosci. 2008; 62: 120–22. 18 Birleson P, Hudson I, Buchanan DG, Wolff S. Clinical evaluation of a self-rating scale for depressive disorder in childhood (Depression Self-Rating Scale). J. Child Psychol. Psychiatry 1987; 28: 43–60. 19 Alfano CA, Zakem AH, Costa NM, Taylor LK, Weems CF. Sleep problems and their relation to cognitive factors, anxiety, and depressive symptoms in children and adolescents. Depress. Anxiety 2009; 26: 503–12. 20 Chervin RD, Dillon JE, Archbold KH, Ruzicka DL. Conduct problems and symptoms of sleep disorders in children. J. Am. Acad. Child Adolesc. Psychiatry 2003; 42: 201–8. 21 Aronen ET, Lampenius T, Fontell T, Simola P. Sleep in children with disruptive behavioral disorders. Behav. Sleep Med. 2014; 12: 373–88. 22 Shanahan L, Copeland WE, Angold A, Bondy CL, Costello EJ. Sleep problems predict and are predicted by generalized anxiety/ depression and oppositional defiant disorder. J. Am. Acad. Child Adolesc. Psychiatry 2014; 53: 550–58. 23 Alfano CA, Beidel DC, Turner SM, Lewin DS. Preliminary evidence for sleep complaints among children referred for anxiety. Sleep Med. 2006; 7: 467–73. 24 Kaneita Y, Yokoyama E, Harano S et al. Associations between sleep disturbance and mental health status: A longitudinal study of Japanese junior high school students. Sleep Med. 2009; 10: 780– 86. 25 Ivanenko A, McLaughlin Crabtree V, Gozal D. Sleep and depression in children and adolescents. Sleep Med. Rev. 2005; 9: 115–29. 26 Usami M, Oiji A, Saito¯ K. Sleep problems among junior high school students with major depressive disorder. Kitasato Med. J. 2012; 42: 91–7.
© 2015 Japan Pediatric Society
Pediatrics International (2015) 57, 690–693
doi: 10.1111/ped.12620
Original Article
Behavioral symptoms and sleep problems in children with anxiety disorder Yoshitaka Iwadare,1 Yuichi Kamei,2 Masahide Usami,1 Hirokage Ushijima,1 Tetsuya Tanaka,1 Kyota Watanabe,1 Masaki Kodaira3 and Kazuhiko Saito3 1 Department of Child and Adolescent Psychiatry, National Center for Global Health and Medicine, Kohnodai Hospital, Ichikawa, 2Department of Clinical Laboratory, National Center Hopsital, National Center of Neurology and Psychiatry, Kodaira and 3Department of Child and Adolescent Psychiatry, Aiiku Hospital, Minato, Japan Abstract
Background: Sleep disorders are frequently associated with childhood behavioral problems and mental illnesses such as anxiety disorder. To identify promising behavioral targets for pediatric anxiety disorder therapy, we investigated the associations between specific sleep and behavioral problems. Methods: We conducted retrospective reviews of 105 patients aged 4–12 years who met the DSM-IV criteria for primary diagnosis of generalized anxiety disorder (n = 33), separation anxiety disorder (n = 23), social phobia (n = 21), or obsessive compulsive disorder (n = 28). Sleep problems were evaluated using the Children’s Sleep Habits Questionnaire (CSHQ) and behavioral problems by the Spence Children’s Anxiety Scale, Oppositional Defiant Behavior Inventory (ODBI), and Depression Self-Rating Scale for Children. Results: Depressive behavior was weakly correlated with CSHQ subscores for sleep onset delay and night waking but not with total sleep disturbance. Anxiety was correlated with bedtime resistance, night waking, and total sleep disturbance score. Oppositional defiance was correlated with bedtime resistance, daytime sleepiness, sleep onset delay, and most strongly with total sleep disturbance. On multiple regression analysis ODBI score had the strongest positive association with total sleep disturbance and the strongest negative association with total sleep duration. Conclusions: Sleep problems in children with anxiety disorders are closely related to anxiety and oppositional defiant symptoms.
Key words anxiety disorder, child, Children’s Sleep Habits Questionnaire, oppositional defiance, sleep.
Sleep disruption in children is associated with a more severe form of anxiety illness and independently predicts impairment in daytime functioning beyond anxiety symptomatology.1,2 In addition, sleep deficiency and sleep problems interfere with cognitive function and induce several problematic daytime behaviors, including hyperkinesis, attention deficit, and emotional instability, in children.3–9 Sleep-related problems in early childhood predict later emotional and behavioral disturbances, including clinical anxiety.10,11 Sleep problems are highly prevalent among children with psychiatric disorders, including anxiety disorder, and sleep quality is an important consideration in pediatric psychiatry. Little research has focused, however, on sleep disturbance in children presenting clinically significant anxiety disorders1,2,12,13 or on the relationships between behavioral symptoms and sleeprelated problems. The aim of this study was to assess these
Correspondence: Yoshitaka Iwadare, MD PhD, Department of Child and Adolescent Psychiatry, National Center of Global Health and Medicine, Kohnodai Hospital, 1-7-1 Kohnodai, Ichikawa, Chiba 2728516, Japan. Email: [email protected] Received 3 September 2014; revised 24 December 2014; accepted 23 January 2015.
© 2015 Japan Pediatric Society
relationships by examining the correlation between sleep quality and behavioral problems in children with anxiety disorder.
Methods Participants
Retrospective chart reviews of children presenting to the National Center for Global Health and Medicine, Kohnodai Hospital, were conducted between September 2007 and February 2011. Participants were 105 children aged 4–12 years (mean ± SD: 9.1 ± 2.1 years; 54 girls) who were referred to Kohnodai Hospital, National Center for Global Health and Medicine, Child and Adolescent Psychiatry. All patients met the DSM-IV criteria for a primary diagnosis of generalized anxiety disorder (GAD; n = 33), separation anxiety disorder (SAD; n = 23), social phobia (SP; n = 21), or obsessive compulsive disorder (OCD; n = 28). Eighteen patients (17.1%) also met the criteria for at least one other disorder. The most common comorbid diagnoses were pervasive developmental disorder (n = 13) and Tourette syndrome (n = 2). The exclusion criteria included a history of psychotropic drugs, bipolar disorder, psychosis, suicidal ideation, and mental retardation. (Mental retardation was added to the exclusion criteria because this study included self-report questionnaire.) This study
Table 1 lists the correlations among CSHQ subscore, age, and behavioral symptom scores (SCAS, DSRS-C, and ODBI scores). Age was significantly negatively correlated with CSHQ subscore for bedtime resistance (r = −0.36, P < 0.01), sleep anxiety (r = −0.26, P < 0.01), parasomnias (r = −0.32, P < 0.01), and total
– −0.04 – 0.67** −0.10 – −0.12 0.12 −0.05 – 0.15 0.10 0.42** 0.04 – 0.15 −0.05 0.13 0.42** 0.02 – 0.23* 0.31** 0.19 0.10 0.13 0.18 0.04 0.29** 0.36** −0.09 – −0.01 0.27* 0.13 0.08 0.25* 0.34** 0.07 0.05 0.10 0.27* −0.18 – 0.30* 0.22 −0.02 0.23* 0.17 0.00 0.24* −0.02 −0.09 0.10 0.10 −0.22
3 2
1 – 0.15 −0.08 −0.21* −0.36** 0.09 0.19 −0.26** −0.01 −0.32** 0.00 0.11 −0.14 −0.30** 2.14 5.64 16.02 14.11 3.23 0.77 1.68 2.42 1.34 1.69 0.62 3.26 7.86 69.24
SD Mean
9.09 12.70 32.14 22.62 11.35 1.64 4.44 7.08 3.90 9.04 3.30 12.43 49.11 528.98 Age (years) DSRS-C SCAS ODBI Bedtime resistance Sleep onset delay Sleep duration Sleep anxiety Night waking Parasomnias Sleep-disordered breathing Daytime sleepiness Total sleep disturbance Total sleep duration (min)
Results
Table 1 Age, behavioral symptom scores and CSHQ subscores: Correlations
Spearman’s correlation coefficients were calculated to assess the relationship between specific sleep problems (CSHQ total and subscores) and individual behavioral trait scores (total SCAS, ODBI, and DSRS-C scores). The relationship between age and all psychometric/behavioral test scores was also assessed. Statistical analysis was performed using SPSS version 19 (SPSS Inc., Chicago, IL, USA). Full model multiple regression analysis was used for the following. First, it was performed to estimate the relative influence of behavioral trait and sleeping problems (CSHQ subscores) on anxiety problems (SCAS). The following variables were tested in the analysis for individual traits: (i) age; (ii) DSRS-C; (iii) ODBI; and (iv) CSHQ subscore. Second, it was performed to estimate the relative influence of each behavioral trait on specific sleeping problems (CSHQ subscore). The following variables were tested in the analysis for individual traits: (i) age’ (ii) DSRS-C; (iii) SCAS; and (iv) ODBI. Variables with P < 0.05 were considered statistically significant.
4
Statistical analysis
691
*P < 0.05, **P < 0.01. CSHQ, Children’s Sleep Habits Questionnaire; DSRS-C, Birleson Depression Self-Rating Scale For Children; ODBI, Oppositional Defiant Behavior Inventory; SCAS, Spence Children’s Anxiety Scale.
5
6
CSHQ items
The Spence Children’s Anxiety Scale (SCAS) is a 38-item selfreport questionnaire that assesses multiple symptoms of childhood anxiety disorders on the basis of the current diagnostic criteria.15 The Oppositional Defiant Behavior Inventory (ODBI) is composed of 18 items describing concrete oppositional behaviors that are graded on a 4-point scale ranging from 0 (rarely) to 3 (always).16,17 The Birleson Depression Self-Rating Scale for Children (DSRS-C) is an 18-item measure of depressive symptoms in children.18
7
8
Behavioral symptom scores
– 0.33** 0.14 0.04 0.24* 0.67** 0.00
9
10
11
The Children’s Sleep Habits Questionnaire (CSHQ) is a selfreport questionnaire for parents on the sleep habits and sleep status of children aged 4–12 years.14 The questionnaire includes 38 items that are designed to assess child sleep behavior over the past week and are rated on a 3-point scale. CSHQ yields a total sleep problem score and subscores corresponding to specific problem areas including bedtime resistance, sleep anxiety, sleep onset delay, parasomnias, night waking, sleep-disordered breathing, and daytime sleepiness.
– −0.04 0.06 0.10 0.03 0.29** 0.41** −0.21*
Children’s Sleep Habits Questionnaire
– 0.37** 0.17 0.34** 0.03 0.04 0.42** 0.55** 0.07
12
Measures
– 0.30** 0.04 0.84** 0.30** 0.21* 0.09 0.23* 0.74** 0.03
13
14
was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of the National Center for Global Health and Medicine.
–
Sleep problems and anxiety disorder
© 2015 Japan Pediatric Society
692 Y Iwadare et al. Discussion
Table 2 Significant indicators of CSHQ score Total sleep disturbance Age DSRS-C SCAS ODBI R = 0.433; F(4,58) = 3.334; P < 0.05
β 0.007 −0.068 0.251 0.389
P 0.953 0.605 0.054 0.003
Bedtime resistance Age DSRS-C SCAS ODBI R = 0.501; F(4,58) = 4.850; P < 0.01
β −0.314 −0.147 0.316 0.143
P 0.011 0.244 0.012 0.247
Night waking Age DSRS-C SCAS ODBI R = 0.433; F(4,58) = 3.417; P < 0.05
β 0.085 0.049 0.369 0.227
P 0.497 0.705 0.005 0.078
Daytime sleepiness Age DSRS-C SCAS ODBI R = 0.403; F(4,58) = 2.809; P < 0.05
β 0.193 −0.099 −0.004 0.413
P 0.132 0.455 0.976 0.002
Total sleep duration Age DSRS-C SCAS ODBI R = 0.418; F(4,58) = 2.907; P < 0.05
β −0.345 0.034 −0.171 −0.322
P 0.010 0.804 0.207 0.019
DSRS-C, Birleson Depression Self-Rating Scale For Children, ODBI, Oppositional Defiant Behavior Inventory, SCAS, Spence Children’s Anxiety Scale.
sleep duration (r = −0.30 P < 0.01). DSRS-C score was significantly positively correlated with sleep onset delay (r = 0.23, P < 0.05) and night waking (r = 0.24, P < 0.05). SCAS score was significantly positively correlated with bedtime resistance (r = 0.27, P < 0.05), sleep anxiety (r = 0.25, P < 0.05), night waking (r = 0.34, P < 0.01), and total sleep disturbance (r = 0.27, P < 0.05). ODBI score was significantly positively correlated with bedtime resistance (r = 0.23, P < 0.05), sleep onset delay (r = 0.31, P < 0.01), daytime sleepiness (r = 0.29, P < 0.01), and total sleep disturbance (r = 0.36, P < 0.01). On multiple regression analysis with SCAS as the dependent variable, there were no factors significantly associated with SCAS. Table 2 presents multiple regression analysis showing the relative strength of the associations between behavioral symptom tests and each CSHQ subscore (sleep problem). Total sleep disturbance was most strongly associated with ODBI. Bedtime resistance was mainly influenced by SCAS, followed by age. Night waking was influenced by SCAS and daytime sleepiness by ODBI. Total sleep duration (min) was influenced most strongly by age, followed by ODBI. © 2015 Japan Pediatric Society
CSHQ score, age, and behavioral symptom score
In this group of children with anxiety disorders (GAD, SAD, SP, or OCD), anxiety symptoms were associated with general sleep disturbance and with several more specific sleep-related problems. Depression as measured using DSRS-C was only weakly correlated with two CSHQ subscores but not with the total score, possibly because of the age limit of the study group (≤12 years). Alfano et al. reported that anxiety symptoms are associated with sleep problems in youth of all ages, whereas depressive symptoms are more strongly associated with sleep problems among adolescents.19 Parents of anxious young children have reported greater bedtime resistance, sleep anxiety, and parasomnias in children.1 Their findings are consistent with the present findings of significant negative correlations between age and bedtime resistance, sleep anxiety, parasomnias, and total sleep duration (Table 1). Influence of factors on SCAS and CSHQ score
There were no significant influencing factors on SCAS, indicating that there are other factors involved in anxiety, and illustrating the limitations of the present study. In contrast, the factor most strongly influencing CSHQ subscores for bedtime resistance and night waking was anxiety (SCAS), indicating that anxiety symptoms affect the capacity to fall and stay asleep. Total sleep disturbance, daytime sleepiness, and total sleep duration were most strongly influenced by oppositional defiance. Previous reports have also identified an association between sleep disturbance and oppositional defiant symptoms,20–22 and conduct problems have been linked to other sleep disorder symptoms such as sleep-disordered breathing, restless legs syndrome (RLS), and periodic limb movement syndrome (PLMS).20 It has also been reported that patients with conduct disorder/oppositional defiant disorder (CD/ODD) sleep fewer hours and their sleep is less restorative.21 Further, Shanahan et al. found that sleep problems predict an increased prevalence of ODD later in life and that ODD predicts an increase in sleep problems over time.22 Children with anxiety disorder and sleep problems are more likely to have daytime sleepiness, which in turn can lead to oppositional defiant behavior as younger children cannot verbalize their own sleep problems. Sleep complains are common in child anxiety disorders.23 Additionally, sleep problems induced a variety of cognitive function and problematic behaviors (hyperkinesis, attention deficit, and unstable emotions).3–7,9,24 Improving sleep problems with anxiety disorder in children may ease these cognitive and behavioral problems. Therefore medical treatment of anxiety disorders in children should focus on the symptoms of oppositional defiance. While sleep problems are related to depressive symptoms in adolescents,25,26 sleep problems in children with anxiety disorders are more closely related to anxiety and oppositional defiance symptoms. A limitation of this study is that CSHQ was completed by parents, who were asked whether they were aware of problems in their children’s sleep behavior. Therefore, unless parents are
Sleep problems and anxiety disorder aware of the problems, the CSHQ may not be reliable. In addition, there was no control group and no long-term follow-up assessment. To confirm the present findings, it will be necessary to objectively evaluate sleep status in children with anxiety disorders in a controlled environment (a sleep laboratory) using polysomnography. Because the relationship between sleep disturbance, anxiety, and defiant behaviors is complicated, more specific studies are needed.
Acknowledgments This work was supported by a grant from the National Center for Global Health and Medicine (22-120).
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