Sleep in Children with Chronic Illness, and the Relation to Emotional and Behavioral Problems A Population-Based Study

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1 Sleep in Children with Chronic Illness, and the Relation to Emotional and Behavioral Problems A Population-Based Study Mari Hysing, 1 PSYD, Børge Sivertsen, 2 PHD, Kjell Morten Stormark, 3 PHD, Irene Elgen, 4 MD PHD, and Astri J. Lundervold, 1,3 PHD 1 Department of Biological and Medical Psychology, University of Bergen, 2 Department of Clinical Psychology, University of Bergen, 3 Centre for Child and Adolescent Mental Health, University of Bergen, and 4 Department of Paediatrics, Haukeland University Hospital Objective To examine sleep and sleep problems in children with chronic illness, and the potential effect of emotional and behavioral problems. Methods The Bergen Child Study is a total population study. Based on data from the second wave, information about sleep was given by 5,781 children and their parents, of which 496 children (8.6%) had a chronic illness. Results There were no differences in time in bed between children with a chronic illness and their healthy peers. However, the chronic illness group reported more problems falling asleep and had more nighttime awakenings. The increased risk for sleep problems was reduced to a nonsignificant level when adjusting for emotional and behavioral problems. Conclusions The elevated rate of sleep problems and association with emotional and behavioral problems in children with chronic illness underline the importance of early detection and intervention in this group. Key words children; chronic illness; emotional and behavioral problems; sleep problems. Introduction Sleep problems are prevalent in childhood. While sleep quality and nighttime awakenings are relatively stable during childhood, there appears to be a gradual decrease in sleep duration and an increase in morning drowsiness in middle childhood (Sadeh, Raviv, & Gruber, 2000). Sleep problems are related to a range of negative consequences including reduced daytime functioning, academic and cognitive deficits, and increased risk of emotional and behavior problems (Chorney, Detweiler, Morris, & Kuhn, 2008; Curcio, Ferrara, & De Gennaro, 2006). Children with chronic illness are especially believed to be at increased risk for sleep problems. However, little is known about the rate of sleep problems in children with chronic illness as the research in this field has been scarce (Owens, 2005). To the best of our knowledge, no population-based studies are available examining the rate of parent- and childreported sleep problems and their relation to emotional and behavioral disorders. An increased rate of sleep problems has been reported in children with specific chronic illnesses, including cerebral palsy (Newman, O Regan, & Hensey, 2006), epilepsy (Becker, Fennell, & Carney, 2004), asthma (Sadeh, Horowitz, Wolach-Benodis, & Wolach, 1998), headaches (Bursztein, Steinberg, & Sadeh, 2006), and migraine (Heng & Wirrell, 2006). Chronic illness in children may affect sleep through various pathways. Some illnesses such as asthma and epilepsy may have worsening symptoms at night, and others (e.g., diabetes) may require nighttime medication. Pain, hospitalization, and effects of medications may all be possible risk factors for poor sleep (Valrie, Gil, Redding-Lallinger, & Daeschner, 2007). Symptoms of the chronic illness may disrupt sleep patterns, such as when children with migraine are prone to sleep during the day after headache, interrupting the normal sleep wake cycle. A direct impact on sleep physiology may be present in neurological disorders with central nervous system affection influencing sleep systems and All correspondence concerning this article should be addressed to Mari Hysing PsyD, Department of Biological and Medical Psychology, University of Bergen, Jonas Liesvei 91, 5009 Bergen, Norway. mari.hysing@psybp.uib.no. Journal of Pediatric Psychology 34(6) pp , 2009 doi: /jpepsy/jsn095 Advance Access publication September 11, 2008 Journal of Pediatric Psychology vol. 34 no. 6 ß The Author Published by Oxford University Press on behalf of the Society of Pediatric Psychology. All rights reserved. For permissions, please journals.permissions@oxfordjournals.org

2 666 Hysing et al. sleep physiology. Children with chronic illness are also prone to the effect of general factors known to affect sleep in the general population, such as overweight and low socioeconomic status (Beebe et al., 2007). Sleep and Emotional and Behavioral Problems Emotional and behavioral problems are associated with sleep problems in children in both clinical (Ivanenko, Crabtree, Obrien, & Gozal, 2006) and population-based studies (Paavonen et al., 2002). The first wave of the Bergen Child Study (BCS) showed that having a chronic illness was associated with increased risk of emotional and behavioral problems as assessed by the Strengths and Difficulties Questionnaire (SDQ), and with psychiatric disorders as assessed by a structured interview (development and well-being assessment) (Hysing, Elgen, Gillberg, Lie, & Lundervold, 2007). The relation between sleep and emotional and behavioral disorders has been less studied but is assessed in some chronic illness groups. In a clinical study of sleep disturbances in children with epilepsy in the age range 7 14, inattentiveness/hyperactivity, oppositional behaviors, and depression were directly related to sleep disturbances, while the severity of epilepsy was not an independent predictor (Becker et al., 2004). A study of children with migraine in middle childhood showed a high incidence of sleep problems, and that children with migraine and sleep problems had more externalizing and internalizing behavioral problems compared with sibling controls (Heng & Wirrell, 2006). The direction of the association between sleep and emotional and behavioral problems is unclear. Sleep problems may adversely affect daytime behavior and/or behavior and emotional problems may affect sleep patterns such as rumination at bedtime for anxious children or bedtime resistance in children with defiant behavior. A third possible hypothesis is that chronic illness is an independent risk factor for sleep problems. The present study is part of a total-population longitudinal study, with data stemming from the second wave of the BCS. It improves upon earlier studies by including multiple informants, assessing sleep and emotional and behavioral disorders by both parent and child reports. Most studies have relied on parent report only, even though a large discrepancy between parent and child reports of sleep problems has been identified (Paavonen et al., 2002). The aim of the present study was twofold. First, we examined if children with chronic illness had an increased rate of sleep problems compared to children without chronic illness. Second, we explored the effect of chronic illness on sleep problems, adjusting for the effects of emotional and behavioral problems. Methods Subjects Data stem from the second wave of the BCS carried out in The BCS is a population-based study of children in all public, private, and special schools in the city of Bergen, Norway. In 2002, a target population of 9,430 primary school children (7 9 years) was included in the first wave of the study. Informed consent was given by 7,007 parents (for more details about the first wave, see Heivervang et al., 2007; Hysing et al., 2007; Stormark et al., 2007). The second wave was conducted in 2006, and 5,781 parents and children, now in the fifth to seventh grades (11 13 years), participated. Ethnic diversity was minimal, and mean age was 11.8 (SD ¼ 0.8). In all, 52% of the total samples were girls, and 68% of the participating families reported that their economy was good, 29% reported their economy was moderate and 3% reported their economy was poor. The study was approved by the Regional Committee for Medical Research Ethics in Western Norway and the National Data Inspectorate. Instruments Chronic Illness Chronic illness was defined in the following way. All parents responded to a simple question regarding whether or not their children had a chronic illness or a disability. Parents who rated such illness/disability as present went on to categorize it as (a) asthma, (b) epilepsy, (c) diabetes, (d) mental retardation, or (e) other illnesses. Parents who endorsed other illness were asked to specify in their own words what that illness was. Of the 5,781 children, 496 were reported to have at least one chronic illness. An experienced pediatrician categorized the reported disorders into subgroups. Thus, chronic illness was defined as reported by parents, and only somatic disorders were included. Reported psychiatric disorders (n ¼ 25) and specific learning disabilities (n ¼ 6) were not considered a chronic illness in this context and were included in the nonchronically ill group for statistical analyses. The chronic ill group included (n) asthma (234), allergy (134), epilepsy (40), eczema (36), migraine (20), cerebral palsy (10), hydrocephalus and myelomelingocele (7), other neurological disorders (8), mental retardation and related syndromes (40), diabetes (18), gastrointestinal disorders (17), skeletal disorders (15), sensory impairments (7), cardiovascular disorders (3), hemophilia (3),

3 Sleep in Children with Chronic Illness 667 kidney disorders (4), endocrinological disorders (3), rheumatism (3), and muscle disorders (3). Note that children may have more than one diagnosis. Demographic Information Parents reported level of education in three categories (primary school, secondary school, and college/university) and rated their household economy as good, medium, or poor. Body mass index (BMI) was calculated as weight (kg) divided by squared height (cm) and entered as a continuous variable. Emotional and Behavioral Disorders The SDQ (Goodman, 1999, 2001) is a behavioral screening questionnaire for children aged 4 16 years. The 25 items describing positive and negative attributes of children are allocated to five subscales with five items each: (a) emotional symptoms, (b) conduct problems, (c) hyperactivity-inattention problems, (d) peer relationship problem, and (e) prosocial behavior. A total difficulty score is computed by combining the first four subscale scores. Each subscale is scored on a 3-point scale: not true, somewhat true, and certainly true, with total subscale scores each ranging from 0 to 10, and total difficulties score from 0 to 40. The Cronbach s alpha in the present sample was.72. The SDQ has been extensively validated in various countries (e.g., in population studies of children and adolescents in Nordic countries) (Heiervang et al., 2007; Muris, Meesters, & van den Berg, 2003; Smedje, Broman, Hetta, & von Knorring, 1999). In the first wave of the BCS, the sensitivity and specificity of the SDQ (total score and impact score) in predicting psychiatric diagnoses were high. In the present study, SDQ was used as a measure of emotional and behavioral disorders. Sleep and Sleep Problems Sleep problems were assessed by both parent and child reports. The parents rated if their child had difficulties initiating and/or maintaining sleep (DIMS) on a 5-point Likert scale. A dichotomous variable was used for the purposes of the present study, in which responding either agree or partly agree was coded positive. The parents and children reported time spent in bed, operationalized by subtracting the rising time from bedtime. In addition, the parents were asked if they felt their children had got sufficient sleep during the night. A positive response included too little and somewhat little. A similar operationalization of DIMS has been applied in previous studies in adult populations (Neckelmann, Mykletun, & Dahl, 2007). Statistics Pearson chi-square tests and Kruskal Wallis analysis of variance were used to examine differences on demographics, clinical characteristics, and sleep variables in children with and without chronic illness. Logistic regression analyses were used to further explore the association between chronic illness and sleep problems. We conducted both univariate analyses and separate multivariate analyses adjusting for (a) demographic variables and BMI, (b) conduct problems, (c) hyperactivity problems, (d) peer problems, and (e) emotional problems. Finally, we conducted a fully adjusted analysis adjusting for all the listed potential confounders. Results are presented as odds ratios (OR) with 95% confidence intervals (95% CI). Analyses were performed using SPSS for Mac 16, and the alpha level was set at a two-tailed 5%. Results Sample Characteristics In total, 496 parents reported chronic illness in their children (Table I). There were significantly more boys than girls in the chronic illness groups, their BMI was significantly higher, and they were more likely to have a lower family income. Sleep and Sleep Problems in Children with a Chronic Illness Children with a chronic illness reported similar time in bed as children without chronic illness, and there were no significant differences in child versus parent reported time spent in bed. Bedtimes were similar in children with chronic illness and their peers, while there was a small, but significantly earlier, wake time in children with chronic illness (p ¼.048). Children with chronic illness had a significant higher rate of reported problems with initiating and maintaining sleep than children with no reported chronic illness (p <.001). Emotional and Behavioral Disorders and Sleep Problems Children with a chronic illness had a higher level of both parent- and child-reported emotional and behavioral disorders. The mean level across all subscales of the SDQ was significantly elevated in the parent and child reports (p <.001; see Table II). In a logistic regression adjusting for gender, age, income, education, and BMI, children with chronic illness had a significantly elevated risk for DIMS (OR ¼ 1.41, 95% CI ¼ ). When adjusting for all emotional and behavioral disorders, there was no longer a

4 668 Hysing et al. Table I. Demographic and Clinical Characteristics in Children with and without Chronic Illness Table II. Chronic Illness as a Risk factor for Sleep Problems (DIMS a ), Adjusting for Emotional and Behavioral Problems Characteristics No chronic illness Chronic illness ES P-value OR 95% CI N 5, Girls, % (n) 53.2 (2,499) 43.0 (213) <.001 BMI a Boys 18.2 ( ) 18.9 ( ) Girls 18.0 ( ) 18.7 ( ) Economy, % (n) <.001 Good 68.5 (3,060) 63.5 (303) Medium 29.0 (1,294) 30.6 (146) Poor 2.5 (111) 5.9 (28) Education Mother, % (n).79 Primary 8.1 (361) 9.0 (43) Secondary 37.9 (1,679) 37.8 (180) College/University 54.0 (2,392) 53.2 (253) Education Father, % (n).32 Primary 8.3 (359) 10.3 (46) Secondary 39.5 (1,704) 39.6 (176) College/University 52.2 (2,254) 50.1 (223) SDQ Child-reported a Emotion 1.59 ( ) 2.11 ( ) 0.27 <.001 Conduct 1.05 ( ) 1.20 ( ) Hyperactivity 2.50 ( ) 3.03 ( ) 0.32 <.001 Peer 1.09 ( ) 1.57 ( ) 0.29 <.001 Total 6.23 ( ) 7.91 ( ) 0.32 <.001 SDQ Parent-reported a Emotion 1.13 ( ) 1.77 ( ) 0.35 <.001 Conduct 0.78 ( ) 1.00 ( ) Hyperactivity 2.21 ( ) 2.90 ( ) 0.32 <.001 Peer 0.96 ( ) 1.57 ( ) 0.33 <.001 Total 5.09 ( ) 7.23 ( ) 0.41 <.001 a Data presented as mean (95% CI). statistically increased risk (OR ¼ 0.93, 95% CI ¼ ). Also when each subscale was adjusted for separately, the risk of sleep problems was reduced to a nonsignificant level (see Table II for details). Discussion In the present population-based study, the time spent in bed by children with a chronic illness did not differ from that of their healthy peers. However, the chronic illness groups reported more problems with falling asleep and more frequent nighttime awakenings. The increased risk for sleep problems in the children with chronic illness was reduced to a nonsignificant level when adjusting for emotional and behavioral problems. The present study confirms that sleep problems are common in middle childhood (Sadeh et al., 2000), with Model A: Unadjusted Model B: Model A þ gender, age, income, education, and BMI Model C: Model B þ conduct problems Model D: Model B þ hyperactivity problems Model E: Model B þ peer problems Model F: Model B þ emotional problems Fully adjusted model (AþBþCþDþEþF) a Difficulties initiating or maintaining sleep. an even higher rate of sleep problems in children with chronic illness. There is a range of potential factors that could affect the increased rate of sleep problems in the chronic illness group, and only some were assessed in the present study. Both low socioeconomic status (Stein, Mendelsohn, Obermeyer, Amromin, & Benca, 2001) and high BMI (Lumeng et al., 2007) are known risk factors for sleep problems in the general population, and both were found to be more prevalent among children with chronic illness in the present study. However, these factors only slightly reduced the risk of sleep problems and could hence not account for the high rate of sleep problems in the group as a whole. Emotional and behavioral disorders were found to be more prevalent in children with chronic illness. In the present study, these factors attenuated the risk of sleep problems to a nonsignificant level, emphasizing the need for assessing emotional and behavioral problems in the management of sleep problems in this population. However, due to the cross-sectional nature of the study, the directionality of this relationship remains unclear, limiting our ability to make causal inferences. Understanding the pathways and mechanisms for disrupted sleep is important when planning interventions, and the nature of the relationship between the reported sleep problems and emotional and behavioral disorders is also of great interest in children with chronic illness. Although our knowledge in this field as of today remains limited, the longitudinal design of the BCS may allow further understanding of the nature of this relationship in future studies. Limitations Limitations of the present study include the assessment of chronic illness by parent report, without medical verification of the diagnosis. DIMS was assessed by a joint variable, which did not enable us to specifically examine each construct independently. In addition, other factors that might affect sleep and emotional and behavioral problems,

5 Sleep in Children with Chronic Illness 669 including severity and duration of diagnosis and treatment, were not assessed. Future waves of the BCS will allow for more detailed assessment of both chronic illness and sleep problems. Clinical Implications Heightened awareness of sleep problems in children with chronic illness is important as there are known and effective interventions, and improved sleep quality could have positive effects on psychological, academic, and possibly physiological variables (Wolfson & Carskadon, 1998). As disrupted sleep in children influence other members of the family and remains a primary concern for many parents (Meltzer & Moore, 2008), the quality of life for the children and their family as a whole may improve following treatment of sleep problems. Acknowledgments The study was supported by the City of Bergen, the Research Council of Norway, the Norwegian Directorate for Health and Social Affairs, Western Norway Regional Health Authority, Haukeland University Hospital, Unifob Health, and the Meltzer legacy. Conflict of interest: None declared. Received April 26, 2008; accepted August 19, 2008 References Becker, D. A., Fennell, E. B., & Carney, P. R. (2004). Daytime behavior and sleep disturbance in childhood epilepsy. Epilepsy & Behavior, 5(5), Beebe, D. W., Lewin, D., Zeller, M., McCabe, M., MacLeod, K., Daniels, S. R., et al. (2007). Sleep in overweight adolescents: Shorter sleep, poorer sleep quality, sleepiness, and sleep-disordered breathing. Journal of Pediatric Psychology, 32(1), Bursztein, C., Steinberg, T., & Sadeh, A. (2006). Sleep, sleepiness, and behavior problems in children with headache. Journal of Child Neurology, 21(12), Chorney, D. B., Detweiler, M. F., Morris, T. L., & Kuhn, B. R. (2008). The interplay of sleep disturbance, anxiety, and depression in children. Journal of Pediatric Psychology, 33(4), Curcio, G., Ferrara, M., & De Gennaro, L. (2006). Sleep loss, learning capacity and academic performance. Sleep Medicine Reviews, 10(5), Goodman, R. (1999). The extended version of the Strengths and Difficulties Questionnaire as a guide to child psychiatric caseness and consequent burden. Journal of Child Psychology and Psychiatry, 40(5), Goodman, R. (2001). Psychometric properties of the strengths and difficulties questionnaire. Journal of the American Academy of Child and Adolescent Psychiatry, 40(11), Heiervang, E., Stormark, K. M., Lundervold, A. J., Heimann, M., Goodman, R., Posserud, M. B., et al. (2007). Psychiatric disorders in Norwegian 8- to 10-year-olds: An epidemiological survey of prevalence, risk factors, and service use. Journal of the American Academy of Child and Adolescent Psychiatry, 46(4), Heng, K., & Wirrell, E. (2006). Sleep disturbance in children with migraine. Journal of Child Neurology, 21(9), Hysing, M., Elgen, I., Gillberg, C., Lie, S. A., & Lundervold, A. J. (2007). Chronic physical illness and mental health in children. Results from a largescale population study. Journal of Child Psychology and Psychiatry, 48(8), Ivanenko, A., Crabtree, V. M., Obrien, L. M., & Gozal, D. (2006). Sleep complaints and psychiatric symptoms in children evaluated at a pediatric mental health clinic. Journal of Clinical Sleep Medicine, 2(1), Lumeng, J. C., Somashekar, D., Appugliese, D., Kaciroti, N., Corwyn, R. F., & Bradley, R. H. (2007). Shorter sleep duration is associated with increased risk for being overweight at ages 9 to 12 years. Pediatrics, 120(5), Meltzer, L. J., & Moore, M. (2008). Sleep disruptions in parents of children and adolescents with chronic illnesses: Prevalence, causes, and consequences. Journal of Pediatric Psychology, 33(3), Muris, P., Meesters, C., & van den Berg, F. (2003). The Strengths and Difficulties Questionnaire (SDQ) further evidence for its reliability and validity in a community sample of Dutch children and adolescents. European Child & Adolescent Psychiatry, 12(1), 1 8. Neckelmann, D., Mykletun, A., & Dahl, A. A. (2007). Chronic insomnia as a risk factor for developing anxiety and depression. Sleep, 30(7), Newman, C. J., O Regan, M., & Hensey, O. (2006). Sleep disorders in children with cerebral palsy. Developmental Medicine and Child Neurology, 48(7),

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