Sleep and Daytime Behavior in Children With Obstructive Sleep Apnea and Behavioral Sleep Disorders

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Sleep and Daytime Behavior in Children With Obstructive Sleep Apnea

and Behavioral Sleep Disorders

Judith Owens, MD, MPH*; Lisa Opipari, PhD‡; Chantelle Nobile, BA‡; and Anthony Spirito, PhD‡

ABSTRACT. Objective. The purpose of this study was: 1) to examine both bedtime sleep behaviors and daytime behaviors associated with daytime sleepiness in a group of children with a primary medical sleep disor-der (obstructive sleep apnea syndrome [OSAS]) com-pared with a group of children with a primary behavioral sleep disorder (BSD) (limit setting sleep disorder or sleep onset association disorder); and 2) to investigate the im-pact of a comorbid BSD on sleep and daytime behavioral consequences of OSAS.

Methods. Children referred to a pediatric sleep dis-orders clinic during a 3-year period with a primary diagnosis of either polysomnographically-confirmed OSAS (n5 100) or a BSD (n552) were compared on several parent report measures assessing the following domains: symptoms of sleep disordered breathing, other sleep behaviors (primarily parasomnias), bed-time behaviors, and externalizing daybed-time behavior problems. The OSAS sample was then divided into a pure OSAS group (n578) and an OSAS plus a behav-ioral sleep diagnosis group (n 5 22) based on the presence or absence of delayed sleep onset and/or pro-longed nightwakings and compared on the parent-re-port symptom domains.

Results. Almost one-quarter of the OSAS group had clinically significant behavioral sleep problems, primar-ily bedtime resistance, in addition to OSAS. Bedtime resistance was associated with a significantly shortened sleep duration in both the BSD and OSAS-BSD groups. Although the OSAS-BSD group had less severe disease, as defined by polysomnographic variables, than the pure OSAS group, they were rated by their parents as having more daytime externalizing behavior problems associ-ated with daytime sleepiness.

Conclusions. The results of this study suggest that evaluation for comorbid BSD should be done in all children presenting with symptoms of OSAS. The co-existence of such BSDs may contribute significantly to sleep deprivation, and thus to behavioral

manifesta-tions of daytime sleepiness in these children.

Pediatrics 1998;102:1178 –1184; obstructive sleep apnea syndrome, bedtime resistance, daytime behavior, day-time sleepiness.

ABBREVIATIONS. OSAS, obstructive sleep apnea syndrome; BSD, behavioral sleep disorder; CSBS, Children’s Sleep Behavior Scale; SHQ, Sleep Habits Questionnaire; ;OSASQ, Obstructive Sleep Apnea Screening Questionnaire; ECBI, Eyberg Child Behav-ior Inventory; MANOVA, multivariate analysis of variance; P, pure.

O

bstructive sleep apnea syndrome (OSAS), as part of the spectrum of sleep disordered breathing, has been relatively recently recog-nized as an important clinical phenomenon in chil-dren and adolescents. OSAS is estimated to affect 1% to 3% of children,1and has a peak prevalence in the

preschool and early elementary school-aged years.2

One of the first detailed clinical descriptions of OSAS in children, by Guilleminault et al3in 1976, suggested

that behavioral and learning problems and impaired school performance were among the potential se-quelae. The underlying pathophysiologic mecha-nisms for the described neurobehavioral conse-quences of OSAS in children have been proposed to be intermittent nocturnal hypoxia secondary to ap-nea/hypopneas, and frequent electroencephalogram arousals from sleep4 that result in significant sleep

fragmentation.5 Daytime sleepiness resulting from

fragmented or disturbed sleep is often manifested in young children by behaviors such as increased activ-ity, aggression, impulsivactiv-ity, acting out behavior, poor concentration, and inattention.6 – 8 The

associa-tion of OSAS with these types of externalizing be-havioral symptoms has subsequently been described in a number of other clinical studies.9 –11

Children with behaviorally-based sleep disorders also often have significant sleep disturbance, with irregular sleep-wake schedules, and/or fragmented or insufficient sleep. Thus, they may present with daytime behavioral problems related to daytime sleepiness that are similar to those described in chil-dren with OSAS. Behaviorally-based sleep problems, such as prolonged bedtime struggles and frequent and/or prolonged night awakenings, are among the most common behavioral problems presenting to pe-diatricians in preschool and school-aged children.12

However, no studies to date have compared the de-gree and intensity of daytime behavioral problems in children with a primary behavioral sleep disorder (BSD) to those found in children with OSAS. Further-more, no studies have addressed how the coexistence of a behavioral sleep problem, such as limit setting sleep disorder (characterized by significant bedtime resistance) or sleep onset association disorder (pre-senting with frequent or prolonged night wakings) From the Departments of *Pediatrics and ‡Child and Family Psychiatry,

Hasbro Children’s Hospital and Brown University School of Medicine, Providence, Rhode Island.

This article was presented at the Society of Behavioral and Developmental Pediatrics Annual Meeting, Boston, MA, in October 1997.

Received for publication Mar 6, 1998; accepted Jun 30, 1998.

Reprint requests to (J.O.) Department of Pediatrics, Division of Pediatric Ambulatory Medicine, Rhode Island Hospital, 593 Eddy St, Providence, RI 02903.

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might affect the neurobehavioral consequences of OSAS in children.

The objectives of this pilot study were as follows: 1) to compare bedtime and sleep-associated behav-iors in children with polysomnographically docu-mented OSAS to similar behaviors in children diag-nosed with a BSD (ie, limit-setting and sleep onset association disorder); 2) to compare daytime behav-iors associated with sleepiness in children with OSAS to children with a BSD; and 3) to examine these sleep and daytime behaviors in children with both OSAS and a comorbid BSD.

METHODS Participants

The study sample consisted of 52 girls and 100 boys who ranged in age between 2 years, 1 month and 12 years, 7 months (mean age55 years, 9 months). All children were referred to a pediatric sleep disorders subspecialty clinic during a 3-year pe-riod. The Pediatric Sleep Disorders Clinic is based in a tertiary care children’s hospital and consists of a multidisciplinary team of pediatricians and psychologists. Children are generally referred to this clinic by their primary care physician or consulting subspe-cialist (ie, otolaryngologist, neurologist).

Children were selected for participation in this study based on having received a primary diagnosis of either OSAS or a BSD after their evaluation in the Pediatric Sleep Disorders Clinic. Children with OSAS or BSD who also had significant developmental delays (ie, moderate or severe mental retardation) or serious chronic medical conditions (eg, congenital heart disease) were excluded from the group. Eight children were excluded based on these criteria resulting in a final sample of 152 children.

The participants in this study represented a broad range of socioeconomic classes: 36% of the families reported income levels

,$15 000 per year; 13% were between $15 000 to $25 000; 29% were between the $25 000 to $50 000 range; and 20% reported incomes.$50 000 per year. The study sample was approximately 6.2% African-American, 7.3% Hispanic, 0.5% Asian, and 86.0% White/Caucasian.

Procedures

Parents were asked to complete an extensive packet of sleep and behavior questionnaires, routinely used as part of the clinical evaluation, before their child’s appointment. The questionnaires included measures of child sleep and daytime behaviors. During the Pediatric Sleep Disorders Clinic appointment, all children received an extensive diagnostic evaluation including review of questionnaires, interviews with a pediatrician and psychologist, and physical exam. After the evaluation, diagnoses were reached by multidisciplinary team consensus using theInternational Clas-sification of Sleep Disorders Diagnostic and Coding Manual13criteria. All children identified with symptoms of sleep apnea during the initial evaluation (eg, loud snoring, breathing problems, snor-ing/gasping) were scheduled for a single overnight polysomno-graphic evaluation to confirm the preliminary clinical findings. The basis for diagnosis of OSAS was the widely accepted pediatric diagnostic criteria of apnea/hypopnea index (apnea/hypopnea index of.1 episode/hour, nadir O2desaturation,92).14 Electro-encephalogram arousals were also recorded, but a standard cutoff in terms of number of arousals per hour in children does not currently exist.

BSD was defined as either a diagnosis of limit setting sleep disorder or sleep onset association disorder. Diagnoses were based on theInternational Classification of Sleep Disorders Diagnosis and Coding Manual13criteria. Limit setting sleep disorder is defined as: a) difficulty initiating sleep; b) stalling or refusal to go to bed at an appropriate time; c) once the sleep period is initiated, sleep is of normal quality and duration; d) no evidence of significant underlying medical or psychiatric disorder to account for the complaint; and e) does not meet criteria for any other sleep dis-order causing difficulty initiating sleep. Sleep onset association disorder is defined as: a) insomnia; b) insomnia temporarily asso-ciated with absence of certain conditions; c) disorder present for at least 3 weeks; d) sleep with particular association present is

nor-mal in onset, duration, and quality; e) no underlying medical or psychiatric disorder to account for complaint; and f) does not meet criteria for any other sleep disorder causing difficulty initiating sleep.

Measures

The following measures were used to obtain information across the domains of sleep disordered breathing, other sleep behaviors, bedtime behavior problems, and daytime behavior problems.

Children’s Sleep Behavior Scale (CSBS)

The CSBS15 is a 22-item parent-report measure that assesses children’s sleep related behaviors during the previous 6-month period. Items are based on a 5-point Likert scale ranging from “never” to “quite often.” This measure covers a wide range of sleep behaviors including sleep onset, restless sleep, night wak-ings, behaviors that occur while sleeping (eg, smiling, bruxism), nightmares, and morning waking. The CSBS has demonstrated good 2-week test-retest reliability, with the majority of the items

.0.70 and only 2 items with a reliability,0.50.15,16

Children’s Sleep Habits Questionnaire (SHQ)

The SHQ17is a 52-item instrument that assesses domains of bedtime behavior, sleep behaviors such as parasomnias, other night wakings, morning waking, and daytime sleepiness. This parent report measure is rated on a 3-point scale ranging from “rarely” to “usually.” This measure also includes an open-ended question that asks parents to record their child’s usual amount of sleep per day including both sleep during the night and daytime naps. One-week test-retest reliability coefficients, the majority of which were.0.60, have been reported.18

Obstructive Sleep Apnea Screening Questionnaire (OSASQ) The OSASQ is a 13-item questionnaire designed for use in the Pediatric Sleep Disorders Clinic to screen for nighttime breathing problems. This measure was designed as a brief screen to evaluate the presence of sleep related symptoms of obstructive sleep apnea. Items on this screening questionnaire include: snorts/gasp, wheezes/whistles, snores, snores loudly, chokes, holds breath, stops breathing, breaths with an open mouth, breathing problems, tosses/turns, kicks/jerks, restless, and sweats. This parent report measure is rated on a 5-point scale ranging from “never” to “every night.” Interitem agreement for this measure based on the current study sample was 0.89.

Eyberg Child Behavior Inventory (ECBI)

The ECBI19is a 36-item measure that assesses conduct problem behaviors in children ranging from 2 to 17 years old. Parents are asked to rate the frequency of occurrence for each of 36 behaviors using a 5-point Likert scale ranging from “never” to “always.” They also rate whether they perceive the behavior to be a problem for their child on a “yes”/“no” scale. This measure yields two scales; a problem scale and a frequency scale. This measure has demonstrated good discriminant, convergent, and concurrent va-lidity.20

Variable Reduction

There were three domains of sleep behavior that we examined: sleep disordered breathing, bedtime behavior problems, and other sleep behaviors. There are currently no standard pediatric sleep questionnaires that include sufficient items to thoroughly assess these behaviors. Therefore, we chose to select individual items from the multiple measures (ie, CSBS, SHQ, OSASQ) that reflected each of the domains of interest. Items were selected based on the consensus decision of a behavioral pediatrician and two child psychologists.acoefficients were calculated for each of the three sleep-related domains to assess degree of interitem agreement.

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Inter-item agreement for this set of variables was 0.81. Items selected to represent the domain of other sleep behaviors included: restless, smiling, talks, walks, sits up while asleep, laughs, nightmares, and terrified at night. Interitem agreement for this set of variables was 0.78.

The fourth behavioral domain of interest in this study was daytime behavior problems. This variable was assessed using the well-established Eyberg Problem and Frequency Scales.20

RESULTS

Comparisons of Children With OSAS and BSD on Descriptive Characteristics

Analysis of age and gender revealed that children in the OSAS and BSD groups differed on age but not gender variables. Children in the OSAS group were significantly older at time of diagnosis (6.4 years) than children in the BSD group (4.9 years; t[150] 5 2.95; P , .01). (Because of age differences between groups, all analyses were run both with and without age as a covariate. No differences were found in the pattern of results when we controlled for age. To present straightforward statistics, and means and standard deviations consistent with analyses con-ducted, we are reporting on the results from analyses that did not control for age.) In both groups there were more males than females, but the two groups did not differ between each other in gender compo-sition. The OSAS group was 70% male and the BSD group was 58% male (x252.30;P 5NS).

Comparisons of Clinical Symptomatology of Children With OSAS Versus BSD

Children in OSAS and BSD groups were compared on parent reported symptoms across the following four domains of clinical symptomatology: 1) sleep disordered breathing, 2) other sleep behaviors, 3) bedtime behavior, and 4) daytime behavior. Multi-variate analysis of variance (MANOVA) procedures using group status as the independent variable were used to compare the groups across each of these domains. A significant main effect for group was found on the MANOVA for sleep disordered breath-ing (F[8,99] 5 18.64; P , .001; multivariate effect size 50.60). Follow-up univariate analysis revealed that the OSAS group had significantly more frequent symptoms of gasping, wheezing, holding breath, stopping breathing, breathing problems, choking, snoring, and breathing with an open mouth than the BSD group. In contrast, there was no group differ-ence between the OSAS and BSD groups found with the MANOVA for other sleep behaviors (F[8,115]5 1.32;P5 NS; Table 1).

Significant group differences were found on the MANOVAs for bedtime behavior problems (F[6,87]5 8.79; P , .001; multivariate effect size 5 0.38) and daytime behavior problems (F[2,119]5 7.22;P, .01; multivariate effect size 5 0.11). As seen in Table 2, follow-up analyses revealed that children in the BSD group had significantly more problems with being ready for bed at bedtime, going to bed willingly, strug-gling at bedtime, falling asleep easily, and getting out of bed at night. Similarly, in terms of daytime behav-iors, children in the BSD group had greater frequency and problem scores for externalizing behavior prob-lems than the children with OSAS.

The groups were also compared on average time spent sleeping per night. Children in the OSAS group were reported to sleep significantly more than children in the BSD group (t[122] 53.68;P ,.001). On average, children in the OSAS received 10.1 hours of sleep per night as compared with 8.4 hours for children in the BSD group.

Comparisons of Clinical Symptomatology in Children With Pure OSAS, OSAS With a Secondary Behavioral Diagnosis, BSD

Because a number of children in the OSAS group were found to have behavioral sleep problems, this sample was divided into a pure OSAS group (OSAS-P) (n 5 78) and an OSAS plus BSD group (OSAS-BSD) (n522). Assignment to the OSAS-BSD group was based on a coexisting limit setting sleep

TABLE 1. Mean Scores (SD) on Symptoms of Sleep Disor-dered Breathing and Other Sleep Behaviors for OSAS and BSD Groups

OSAS BSD Univariate F

Breathing problems

Gasps 2.87 (1.5) 0.65 (1.1) 62.6*

Wheezes 1.96 (1.5) 0.36 (0.9) 35.7*

Chokes 1.73 (1.5) 0.13 (0.4) 34.9*

Snores 4.68 (0.8) 2.60 (1.6) 104.9* Stops breathing 2.10 (1.5) 0.25 (0.8) 60.0* Holds breath 3.76 (1.6) 1.13 (0.5) 80.4* Breathes with open mouth 4.13 (1.5) 2.16 (1.5) 40.8* Breathing problems 1.99 (1.5) 0.47 (0.9) 33.1* Other problems

Restless 4.13 (1.0) 4.08 (1.1) 0.00

Talks 3.09 (1.4) 2.92 (1.6) 0.41

Walks 1.89 (1.4) 1.63 (1.1) 0.86

Nightmares 2.50 (1.4) 3.01 (1.5) 3.31 Terrified at night 1.95 (1.3) 1.93 (1.2) 0.02

Smiles 2.33 (1.3) 2.15 (1.2) 1.52

Laughs 1.86 (1.1) 1.48 (0.8) 3.45

Sits up in bed 2.45 (1.6) 2.10 (1.2) 1.16

Abbreviations: SD, standard deviation; OSAS, obstructive sleep apnea syndrome; BSD, behavioral sleep disorder.

*P,.001. Note: higher scores indicate the behavior occurs more frequently.

TABLE 2. Mean Scores (SD) on Daytime and Bedtime Sleep Behavior Problems for OSAS and BSD Groups

OSAS BSD Univariate F*

Daytime behavior ECBI behavior problem

score

8.69 (8.8) 15.41 (9.5) 14.3§

ECBI behavior frequency score

110 (37) 135 (44) 10.6§

Bedtime behavior

Ready at bedtime 1.76 (0.8) 2.13 (0.9) 5.6† Goes to bed willingly 2.24 (1.4) 2.98 (1.6) 4.5† Resists bed 1.87 (0.7) 2.26 (0.8) 3.4 Struggles at bedtime 1.60 (0.8) 2.37 (0.85) 15.8§ Falls asleep easily 2.10 (1.3) 3.59 (1.4) 35.5§ Gets out of bed 3.51 (1.3) 4.29 (1.0) 10.5‡

Abbreviations: SD, standard deviation; OSAS, obstructive sleep apnea syndrome; BSD, behavioral sleep disorder; ECBI, Eyberg Child Behavior Inventory.

* Note: Higher scores represent greater behavior problems. †P,.05.

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disorder and/or sleep onset association disorder. TheInternational Classification of Sleep Disorders Diag-nosis and Coding Manual13criteria defined previously

were used to make diagnostic decisions. There were no significant differences in the age or gender com-position of the two groups. Children in the OSAS-P group were on average 6.2 years old, whereas chil-dren in the OSAS-BSD group were 7.1 years old (t[98]5 1.42; P5 NS). Both groups were predomi-nantly male; the OSAS-P group was 68% male and the OSAS-BSD group was 77% male (x250.71;P5

NS). Children in the pure OSAS group were found to have significantly more severe apnea based on two of the three polysomnographic indicators (Respira-tory Distress Index, nadir O2, arousals per hour) than

children in the OSAS-BSD group. Mean standard deviation scores for the groups across these mea-sures were as follows: Respiratory Distress Index: OSAS-P-12.6 (11.2), OSAS-BSD 5 6.1 (4.8), t(96) 5 2.57,P , .05; nadir O2: OSAS-P5 90.6 (4.2),

OSAS-BSD5 92.4 (2.7),t(94)5 1.92,P5 .05; arousals per hour: OSAS-P514.2 (11.5), OSAS-BSD5 10.4 (4.4),

t(92)5 1.5,P5 NS.

To examine differences in parent reported symp-toms, comparisons were made between children in the OSAS-P, OSAS-BSD, and BSD groups across the domains of sleep disordered breathing, other sleep behaviors, bedtime behavior problems, and daytime behavior problems. MANOVA procedures using group status as the independent variable were used to compare the groups across each of the four do-mains. Significant group effects were further ana-lyzed using follow-up univariate analysis of variance procedures with Sheffe tests used for post hoc com-parisons.

A significant main effect for group was found on the MANOVA for sleep disordered breathing (F[16,198]58.37;P,.001; multivariate effect size5 0.41). Follow-up univariate tests revealed significant group differences across all eight indices of sleep disordered breathing. As shown in Table 3, the OSAS-P and OSAS-BSD groups had significantly worse symptoms of sleep disordered breathing than the BSD group. The OSAS-P and OSAS-BSD groups differed from each other only on holding breath dur-ing sleep, with the OSAS-P group havdur-ing more symptomatology. No overall group differences were found on the MANOVA for other sleep behaviors (F[16,230]5 1.55;P5 NS).

Overall group differences were also found for both bedtime behavior problems (F[12,174] 5 6.35; P ,

.001; effect size50.31) and daytime behavior prob-lems (F[4,238]55.03;P,.01; effect size5 0.08). In terms of bedtime behaviors, across indices, children in the OSAS-P group had significantly fewer prob-lems than children in either the OSAS-BSD or BSD groups. There was no difference in the bedtime be-havior problems between children in the OSAS-BSD and BSD groups (Table 4). As seen in Table 4, chil-dren in the OSAS-P group only, had less frequent and problematic daytime behavior problems than the BSD group.

Finally, the usual amount of sleep per day was compared across the three groups. Children in the

OSAS-P group slept significantly more than children in either of the other two groups (F[2,124]515.7;P,

.001). On average, children in the OSAS-P group received 10.5 hours per night whereas children in the OSAS-BSD and BSD groups received 8.2 and 8.4 hours, respectively.

DISCUSSION

The results of this study suggest that there are qualitative and quantitative differences in both sleep-associated and daytime behaviors in children, depending on the primary and comorbid sleep dis-order diagnoses. First, as expected, the OSAS group had a significantly greater frequency of symptoms of sleep disordered breathing than did the BSD group, although the BSD group did exhibit some degree of snoring. When the OSAS group was divided into pure (OSAS-P) and comorbid (OSAS-BSD) groups, these two groups were found to be clinically similar to one another in terms of sleep disordered breath-ing. However, when severity of OSAS was defined by polysomnographic variables (number of apneas and hypopneas/hour and the nadir O2 saturation),

the OSAS-P group had significantly more severe dis-ease than the OSAS-BSD group. In fact, the children in the OSAS-P group had more than twice the num-ber of apneas and hypopneas/hour on polysomnog-raphy than did the OSAS-BSD group (12.6 vs 6.1 hypopneas/h). Despite having less severe disease, the OSAS-BSD group was subsequently found to have more significant daytime behavior problems than the OSAS-P group. This suggests that variables other than the severity of sleep-disordered breathing have an important influence on daytime behavioral problems associated with OSAS.

The other sleep behaviors examined in this study, which were primarily parasomnias such as

sleep-TABLE 3. Mean Scores (SD) on Symptoms of Sleep Disor-dered Breathing for OSAS-P, OSAS-BSD and BSD Groups*

Symptom OSAS-P OSAS-BSD BSD Univariate F

Gasps 2.98A 2.38A 0.65B 33.74†

(1.4) (1.5) (1.1)

Wheezes 2.08A 1.50A 0.36B 20.62†

(1.5) (1.5) (0.9)

Chokes 1.89A 1.25A 0.13B 19.59†

(1.5) (1.4) (0.4)

Snores 4.69A 4.65A 2.60B 51.99†

(0.9) (0.5) (1.6)

Stops breathing 2.20A 1.69A 0.25B 30.99† (1.5) (1.3) (0.8)

Holds breath 3.94A 3.00B 1.13B 46.71† (1.5) (1.6) (0.5)

Breaths with open mouth

4.23A 3.76A 2.16B 22.43†

(1.5) (1.7) (1.5) Breathing

problems

2.08A 1.60A 0.47B 17.65†

(1.5) (1.5) (0.9)

Abbreviations: SD, standard deviation; OSAS-P, obstructive sleep apnea pure group; OSAS-BSD, obstructive sleep apnea-behavioral sleep disorder group; BSD, behavior sleep disorder.

* Higher score indicate the behavior occurs more frequently. Let-ters indicate significant differences between groups based on planned comparison using the Scheffe test with a significance level at 0.05.

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walking, sleep-talking, and nightmares, were not sig-nificantly different in the OSAS versus BSD groups. Several studies have suggested that children with OSAS have an increased incidence of parasomnias, especially the partial arousal parasomnias (such as sleep walking and night terrors) that occur during delta or slow-wave sleep.21 The mechanism for the

increased incidence of partial arousal parasomnias in OSAS has been postulated to be OSAS-associated intermittent hypoxia and/or a rebound increase in the percentage of delta sleep in OSAS. We recently reported that the incidence of parasomnias in a group of children with OSAS was higher when com-pared with a control group, but was similar to the incidence of parasomnias in children with a BSD.22

This suggests that factors common to both OSAS and BSDs, such as sleep fragmentation resulting in in-creased rebound delta sleep, may be more important than hypoxia in determining the occurrence of para-somnias in both of the sleep-disordered groups.

A particularly striking sleep behavior finding in this study was a significantly shorter sleep duration in the BSD groups compared with the OSAS group. This occurred despite the fact that the BSD group was younger and would thus be expected, on aver-age, to have a longer sleep duration. When compared with age-adjusted norms,23,24the average sleep

dura-tion for the BSD group of 8.4 hours (compared with 10.5 hours in the OSAS group) was significantly be-low even the be-lower limit of age norms. This was not accounted for by a concomitant increase in the BSD group in daytime sleep (napping), and suggests that the shortened sleep duration in these children is not being compensated for by daytime sleep periods. The average sleep duration of the OSAS-BSD group was also significantly shorter than either the OSAS-P group or age-appropriate norms and almost identical to the average sleep duration in the BSD group. The increased frequency of bedtime struggles in both the

BSD and OSAS-BSD groups presumably resulted in significantly delayed sleep onset and thus in the shortened sleep duration. It is interesting to specu-late that the ability to at least partially compensate for the sleep fragmentation resulting from OSAS arousals by an increased or at least normal sleep duration may play an important role in mitigating the neurobehavioral consequences of OSAS.

By definition, the OSAS-BSD group, which repre-sented a substantial proportion of children in the total OSAS group, had clinically significant bedtime behavior problems, which were comparable to those in a group of children whose degree of bedtime resistance had led to referral to a pediatric sleep disorders clinic. A few studies have anecdotally re-ported a relatively high incidence of behavioral sleep problems in childhood OSAS; Guilleminault et al3

describe significant bedtime refusal, behavioral “hy-peractivity” at bedtime, and significant anxiety re-lated to falling asleep in three of eight children diag-nosed with OSAS. Similarly, Miyazaki et al25 noted

that 60% (9 of 15) of children with a diagnosis of OSAS had “significant bedtime struggles” but did not define these in more detail. In contrast, Carroll and Loughlin26 state that, in their experience,

al-though bedtime problems exist, they “are not com-mon” in children with OSAS. Our finding that nearly one-fourth of the OSAS group met the criteria for a clinical diagnosis of either a limit setting sleep dis-order or a sleep onset association disdis-order is similar to the prevalence of these BSDs found in other stud-ies of corresponding age groups in the general pop-ulation.27–30However, failing to clinically screen

chil-dren with OSAS for a comorbid BSD may have more significant consequences than do unrecognized or untreated BSDs in a normal population because the resultant sleep deprivation or disruption could have an additive effect on any daytime behavioral se-quelae of the OSAS.

TABLE 4. Mean Scores (SD) on Daytime and Bedtime Sleep Behavior Problems for OSAS-P, OSAS-BSD, and BSD Groups*

OSAS-P OSAS-BSD BSD Univariate F

Bedtime behavior

Ready at bedtime 1.60A 2.42B 2.13B 8.61‡

(0.7) (0.9) (0.9)

Goes to bed willingly 1.90A 3.65B 2.98B 11.26‡

(1.2) (1.4) (1.6)

Resists bed 1.70A 2.50B 2.26B 9.72‡

(0.6) (0.8) (0.8)

Struggles at bedtime 1.42A 2.30B 2.37B 14.72‡

(0.7) (0.9) (0.85)

Falls asleep easily 1.79A 3.41B 3.59B 27.87‡

(1.0) (1.5) (1.4)

Gets out of bed 3.41A 3.93AB 4.29B 6.71‡

(1.3) (1.2) (1.0)

Daytime behavior

ECBI problem score 7.65A 12.88AB 15.41B 9.73‡

(8.1) (10.3) (9.5)

ECBI frequency score 105A 130AB 135B 8.34‡

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Abbreviations: SD, standard deviation; OSAS-P, obstructive sleep apnea pure group; OSAS-BSD, obstructive sleep apnea-behavioral sleep disorder group; BSD, behavioral sleep disorder; ECBI, Eyberg Child Behavior Inventory.

* Higher scores represent greater behavior problems. Letters indicate significant difference between groups based on planned comparison using the Scheffe test with a significance level at 0.05.

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Finally, the BSD group overall had a greater num-ber and severity of externalizing daytime behavior problems, as measured by the problem and intensity scores on the ECBI, than did children with OSAS. When the OSAS group was divided, the BSD group also had a greater frequency and intensity of daytime behavior problems than did the OSAS-P group. The OSAS-BSD group scored in between the OSAS-P and BSD groups on these scales, and was not significantly different from either group. Our conceptualization of an elevated problem and intensity score on the ECBI as potentially indicative of daytime sleepiness is sim-ilar to that of other studies7,31–33that have examined

the complex association among daytime externaliz-ing behavior problems, daytime sleepiness, and sleep deprivation or fragmentation in school-aged children.34 –37

To further address this issue of the relationship between externalizing daytime behavior problems and daytime sleepiness, we also examined the rela-tive frequencies among the various OSAS and behav-ioral groups of several daytime sleepiness items that had been included on the sleep questionnaires. Al-though most of these items (including falling asleep during various activities) were not significantly dif-ferent among the OSAS-P, OSAS-BSD, and the BSD groups, two daytime sleepiness variables were sig-nificantly more common in the same groups that also had more externalizing behavior problems: disrupt-ing family activities because of sleepiness (P, .05), and difficulty waking in the morning (P,.05). This finding lends some additional support to the hypoth-esis that these externalizing behaviors were at least partially reflective of daytime somnolence, and thus of underlying sleep disturbance.

The behavioral manifestations of daytime sleepi-ness in young children, such as hyperactivity, clearly overlap with problematic behaviors that do not re-sult from sleep deprivation/disruption. The rere-sults of a cross-sectional study, such as this one, do not allow us to draw direct conclusions about the nature of the relationship between sleep disturbance and daytime sleepiness-associated behavior. Alternative explanations for the finding of increased externaliz-ing behavior problems in the BSD groups include the possibility that children with oppositional or aggres-sive behavior during the day are also likely to man-ifest similar behavior at bedtime. Other factors, such as an overall negative parental perception of both their child’s bedtime and daytime behavior, may be operative. It would be important in future studies to correlate more objective sleepiness measures, such as the Multiple Sleep Latency Test,39 and multiple

ob-server ratings with parental behavioral observations. Several additional limitations of this study exist. First, the fact that the BSD group did not undergo polysomnographic evaluation to rule out OSAS is a limitation of the study; ie, there may have been chil-dren with undiagnosed OSAS or other forms of sleep disordered breathing in the BSD group. Previous studies have failed to show that any constellation of clinical symptoms in children who do snore reliably predicts which children will subsequently have poly-somnographically-confirmed OSA versus primary or

benign snoring (defined as snoring without respira-tory compromise).38 However, all children

present-ing to our pediatric sleep clinic are systemically clin-ically screened for risk factors and symptoms of OSAS, and an overnight sleep study is obtained on all children with habitual snoring. Second, the design of the study did not allow us to examine the role of other possible confounding factors in the association among OSAS, bedtime behavior, and daytime behav-ior. For example, parental anxiety about symptoms of sleep disordered breathing, a variable previously shown to correlate with polysomnographic severity of disease,40may have resulted in a reduced

willing-ness on the part of those parents to enforce bedtime rules, resulting in a limit setting sleep disorder. This study also relied on parental report to define sleep disturbances. Although several studies have shown a correlation between parent reports and more objec-tive measures of sleep disturbance, such as actigra-phy,18 some authors have suggested that parental

report data may actually underestimate the fre-quency of some sleep disturbances, such as night waking, especially in older children who are often not directly observed by parents during sleep. Fi-nally, our study population, because it consisted ex-clusively of children referred to a pediatric sleep disorders clinic in a children’s teaching hospital, may not have been comparable to a general pediatric population in terms of the severity of both OSAS symptoms and behavioral sleep problems; therefore, the generalizability of our results may be limited.

CONCLUSION

The results of this study suggest the need for in-creased awareness on the part of physicians screen-ing and treatscreen-ing children for obstructive sleep apnea, of the common comorbid occurrence of behaviorally-based sleep disorders in these children. Children with OSAS are often evaluated by medical subspe-cialists, such as otolaryngologists and pulmonolo-gists, who may not screen these children for BSDs. Alternatively, children with BSDs may present to nonmedical mental health professionals, who may not be familiar with the clinical consequences of OSAS and thus may fail to recognize its coexistence with a BSD. Although further confirmation is needed, our results suggest that these comorbid BSDs may have a significant impact on the daytime behavioral consequences of OSAS, and that all chil-dren with OSAS should be clinically screened for BSD. In addition, assessment of average sleep dura-tion in children with OSAS should be part of the clinical evaluation for risk factors for daytime sleep-iness and behavioral problems. Finally, future stud-ies examining the neurobehavioral consequences of childhood OSAS should include evaluation for co-morbid BSDs.

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WHERE ARE WE GOING?

Medicine has become the prisoner of its suffering, its mandate has become muddled. What are its aims? Where is it to stop? Is its prime duty to keep people alive as long as possible, willy-nilly, whatever the circumstances? Is its charge to

make people lead healthy lives? Or is it but a service industry, on tap to fulfill whatever fantasies its clients may frame for their bodies, be they cosmetic surgery and designer bodies or the longing of postmenopausal women to have babies?

Porter R.The Greatest Benefit To Mankind.New York, NY: WW Norton; 1997

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DOI: 10.1542/peds.102.5.1178

1998;102;1178

Pediatrics

Judith Owens, Lisa Opipari, Chantelle Nobile and Anthony Spirito

Behavioral Sleep Disorders

Sleep and Daytime Behavior in Children With Obstructive Sleep Apnea and

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DOI: 10.1542/peds.102.5.1178

1998;102;1178

Pediatrics

Judith Owens, Lisa Opipari, Chantelle Nobile and Anthony Spirito

Behavioral Sleep Disorders

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Figure

TABLE 1.Mean Scores (SD) on Symptoms of Sleep Disor-dered Breathing and Other Sleep Behaviors for OSAS and BSDGroups

TABLE 1.Mean

Scores (SD) on Symptoms of Sleep Disor-dered Breathing and Other Sleep Behaviors for OSAS and BSDGroups p.3
TABLE 2.Mean Scores (SD) on Daytime and Bedtime SleepBehavior Problems for OSAS and BSD Groups

TABLE 2.Mean

Scores (SD) on Daytime and Bedtime SleepBehavior Problems for OSAS and BSD Groups p.3
TABLE 3.Mean Scores (SD) on Symptoms of Sleep Disor-dered Breathing for OSAS-P, OSAS-BSD and BSD Groups*

TABLE 3.Mean

Scores (SD) on Symptoms of Sleep Disor-dered Breathing for OSAS-P, OSAS-BSD and BSD Groups* p.4
TABLE 4.Mean Scores (SD) on Daytime and Bedtime Sleep Behavior Problems for OSAS-P, OSAS-BSD, and BSD Groups*

TABLE 4.Mean

Scores (SD) on Daytime and Bedtime Sleep Behavior Problems for OSAS-P, OSAS-BSD, and BSD Groups* p.5

References