Pediatric Sleep Disorders/Sleep in Children with Chronic Illness.

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 1Department of Biological and Medical Psychology, University of Bergen,2Department of Clinical Psychology,

University of Bergen,3Centre for Child and Adolescent Mental Health, University of Bergen, and4Department 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 cog-

nitive deficits, and increased risk of emotional and behav-

ior 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 child-

reported 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 cere-

bral 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 medica-

tions may all be possible risk factors for poor sleep

(Valrie, Gil, Redding-Lallinger, & Daeschner, 2007).

Symptoms of the chronic illness may disrupt sleep pat-

terns, 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 physiol-

ogy 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. E-mail: [email protected].

Journal of Pediatric Psychology 34(6) pp. 665–670, 2009 doi:10.1093/jpepsy/jsn095

Advance Access publication September 11, 2008 Journal of Pediatric Psychology vol. 34 no. 6 � The Author 2008. Published by Oxford University Press on behalf of the Society of Pediatric Psychology.

All rights reserved. For permissions, please e-mail: [email protected]

at U niversity of A

labam a at B

irm ingham

on A ugust 17, 2010

http://jpepsy.oxfordjournals.org D

ow nloaded from

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 dis-

orders as assessed by a structured interview (development

and well-being assessment) (Hysing, Elgen, Gillberg, Lie, &

Lundervold, 2007).

The relation between sleep and emotional and behav-

ioral disorders has been less studied but is assessed in some

chronic illness groups. In a clinical study of sleep distur-

bances 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 behav-

ioral 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 chil-

dren or bedtime resistance in children with defiant behav-

ior. 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 long-

itudinal 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

2006. 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 (SD¼ 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 par-

ents 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 dis-

orders into subgroups. Thus, chronic illness was defined

as reported by parents, and only somatic disorders were

included. Reported psychiatric disorders (n¼ 25) and specific learning disabilities (n¼ 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 impair-

ments (7), cardiovascular disorders (3), hemophilia (3),

666 Hysing et al.

at U niversity of A

labam a at B

irm ingham

on A ugust 17, 2010

http://jpepsy.oxfordjournals.org D

ow nloaded from

kidney disorders (4), endocrinological disorders (3), rheu-

matism (3), and muscle disorders (3). Note that children

may have more than one diagnosis.

Demographic Information

Parents reported level of education in three categories (pri-

mary 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 contin-

uous variable.

Emotional and Behavioral Disorders

The SDQ (Goodman, 1999, 2001) is a behavioral screen-

ing questionnaire for children aged 4–16 years. The 25

items describing positive and negative attributes of chil-

dren are allocated to five subscales with five items each:

(a) emotional symptoms, (b) conduct problems, (c) hyper-

activity-inattention problems, (d) peer relationship prob-

lem, 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, some-

what 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 coun-

tries (e.g., in population studies of children and adoles-

cents 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 mea-

sure 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 pur-

poses 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 demo-

graphics, clinical characteristics, and sleep variables in chil-

dren with and without chronic illness. Logistic regression

analyses were used to further explore the association

between chronic illness and sleep problems. We con-

ducted 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 con-

ducted 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 chil-

dren (Table I). There were significantly more boys than

girls in the chronic illness groups, their BMI was signifi-

cantly 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 dis-

orders. 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

(OR¼ 1.41, 95% CI¼ 1.04–1.90). When adjusting for all emotional and behavioral disorders, there was no longer a

Sleep in Children with Chronic Illness 667

at U niversity of A

labam a at B

irm ingham

on A ugust 17, 2010

http://jpepsy.oxfordjournals.org D

ow nloaded from

statistically increased risk (OR¼ 0.93, 95% CI¼ 0.66– 1.30). Also when each subscale was adjusted for separ-

ately, the risk of sleep problems was reduced to a nonsigni-

ficant 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

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, lim-

iting 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 under-

standing 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 verifica-

tion of the diagnosis. DIMS was assessed by a joint vari-

able, which did not enable us to specifically examine each

construct independently. In addition, other factors that

might affect sleep and emotional and behavioral problems,

Table I. Demographic and Clinical Characteristics in Children with and

without Chronic Illness

Characteristics No chronic illness Chronic illness ES P-value

N 5,285 496

Girls, % (n) 53.2 (2,499) 43.0 (213) <.001

BMIa

Boys 18.2 (18.1–18.4) 18.9 (18.5–19.3) 0.23 .013

Girls 18.0 (17.8–18.1) 18.7 (18.2–19.1) 0.23 .023

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-reporteda

Emotion 1.59 (1.54–1.64) 2.11 (1.93–2.30) 0.27 <.001

Conduct 1.05 (1.01–1.08) 1.20 (1.08–1.31) 0.12 .01

Hyperactivity 2.50 (2.44–2.56) 3.03 (2.84–3.23) 0.32 <.001

Peer 1.09 (1.05–1.13) 1.57 (1.40–1.74) 0.29 <.001

Total 6.23 (6.09–6.36) 7.91 (7.42–8.41) 0.32 <.001

SDQ—Parent-reporteda

Emotion 1.13 (1.09–1.18) 1.77 (1.59–1.95) 0.35 <.001

Conduct 0.78 (0.75–0.81) 1.00 (0.88–1.12) 0.18 .001

Hyperactivity 2.21 (2.16–2.27) 2.90 (2.69–3.11) 0.32 <.001

Peer 0.96 (0.92–1.01) 1.57 (1.38–1.75) 0.33 <.001

Total 5.09 (4.96–5.22) 7.23 (6.70–7.77) 0.41 <.001

aData presented as mean (95% CI).

Table II. Chronic Illness as a Risk factor for Sleep Problems (DIMSa),

Adjusting for Emotional and Behavioral Problems

OR 95% CI

Model A: Unadjusted 1.54 1.20–1.99

Model B: Model Aþ gender, age, income, education, and BMI

1.41 1.04–1.90

Model C: Model Bþ conduct problems 1.28 0.93–1.74 Model D: Model Bþ hyperactivity problems 1.22 0.89–1.67 Model E: Model Bþ peer problems 1.14 0.83–1.57 Model F: Model Bþ emotional problems 1.01 0.72–1.40 Fully adjusted model (AþBþCþDþEþF) 0.93 0.66–1.30 aDifficulties initiating or maintaining sleep.

668 Hysing et al.

at U niversity of A

labam a at B

irm ingham

on A ugust 17, 2010

http://jpepsy.oxfordjournals.org D

ow nloaded from

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 effec-

tive 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 chil-

dren 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), 708–715.

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), 69–79.

Bursztein, C., Steinberg, T., & Sadeh, A. (2006). Sleep,

sleepiness, and behavior problems in children with

headache. Journal of Child Neurology, 21(12),

1012–1019.

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), 339–348.

Curcio, G., Ferrara, M., & De Gennaro, L. (2006). Sleep

loss, learning capacity and academic performance.

Sleep Medicine Reviews, 10(5), 323–337.

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),

791–799.

Goodman, R. (2001). Psychometric properties of the

strengths and difficulties questionnaire. Journal of the

American Academy of Child and Adolescent Psychiatry,

40(11), 1337–1345.

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),

438–447.

Heng, K., & Wirrell, E. (2006). Sleep disturbance in

children with migraine. Journal of Child Neurology,

21(9), 761–766.

Hysing, M., Elgen, I., Gillberg, C., Lie, S. A.,

& Lundervold, A. J. (2007). Chronic physical illness

and mental health in children. Results from a large-

scale population study. Journal of Child Psychology and

Psychiatry, 48(8), 785–792.

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), 42–48.

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), 1020–1029.

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), 279–291.

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), 873–880.

Newman, C. J., O’Regan, M., & Hensey, O. (2006).

Sleep disorders in children with cerebral palsy.

Developmental Medicine and Child Neurology, 48(7),

564–568.

Sleep in Children with Chronic Illness 669

at U niversity of A

labam a at B

irm ingham

on A ugust 17, 2010

http://jpepsy.oxfordjournals.org D

ow nloaded from

Owens, J. (2005). Epidemiology of sleep disorders during

childhood. In S. Sheldon, R. Ferber, & M. Kryger

(Eds.), Principles and practice of pediatric sleep medicine.

Philadelphia: Elsevier Saunders.

Paavonen, E. J., Almqvist, F., Tamminen, T., Moilanen, I.,

Piha, J., Rasanen, E., et al. (2002). Poor sleep

and psychiatric symptoms at school: An epidemiolo-

gical study. European Child & Adolescent Psychiatry,

11(1), 10–17.

Sadeh, A., Horowitz, I., Wolach-Benodis, L., & Wolach, B.

(1998). Sleep and pulmonary function in children

with well-controlled, stable asthma. Sleep, 21(4),

379–384.

Sadeh, A., Raviv, A., & Gruber, R. (2000). Sleep patterns

and sleep disruptions in school-age children.

Developmental Psychology, 36(3), 291–301.

Smedje, H., Broman, J. E., Hetta, J., & von Knorring, A. L.

(1999). Psychometric properties of a Swedish

version of the ‘‘Strengths and Difficulties

Questionnaire’’. European Child & Adolescent

Psychiatry, 8(2), 63–70.

Stein, M. A., Mendelsohn, J., Obermeyer, W. H.,

Amromin, J., & Benca, R. (2001). Sleep and

behavior problems in school-aged children. Pediatrics,

107(4), E60.

Stormark, K. M., Heiervang, E., Heimann, M.,

Lundervold, A., & Gillberg, C. (2008). Predicting

nonresponse bias from teacher ratings of mental

health problems in primary school children. Journal

of Abnormal Child Psychology, 36(3), 411–419.

Valrie, C. R., Gil, K. M., Redding-Lallinger, R.,

& Daeschner, C. (2007). Brief report: Sleep in

children with sickle cell disease: An analysis of daily

diaries utilizing multilevel models. Journal of Pediatric

Psychology, 32(7), 857–861.

Wolfson, A. R., & Carskadon, M. A. (1998). Sleep sched-

ules and daytime functioning in adolescents. Child

Development, 69(4), 875–887.

670 Hysing et al.

at U niversity of A

labam a at B

irm ingham

on A ugust 17, 2010

http://jpepsy.oxfordjournals.org D

ow nloaded from