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 Behavior Inventory; MANOVA, multivariate analysis of variance; P, pure.
Obstructive sleep apnea syndrome (OSAS), as part of the spectrum of sleep disordered breathing, has been relatively recently recognized as an important clinical phenomenon in children and adolescents. OSAS is estimated to affect 1% to 3% of children, and has a peak prevalence in the preschool and early elementary school-aged years. One of the first detailed clinical descriptions of OSAS in children, by Guilleminault et al in 1976, suggested that behavioral and learning problems and impaired school performance were among the potential sequelae. The underlying pathophysiologic mechanisms for the described neurobehavioral consequences of OSAS in children have been proposed to be intermittent nocturnal hypoxia secondary to apnea/hypopneas, and frequent electroencephalogram arousals from sleep that result in significant sleep fragmentation. Daytime sleepiness resulting from fragmented or disturbed sleep is often manifested in young children by behaviors such as increased activity, aggression, impulsivity, acting out behavior, poor concentration, and inattention. The association of OSAS with these types of externalizing behavioral symptoms has subsequently been described in a number of other clinical studies. 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 children 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 pediatricians in preschool and school-aged children. However, no studies to date have compared the degree and intensity of daytime behavioral problems in children with a primary behavioral sleep disorder (BSD) to those found in children with OSAS. Furthermore, 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 (presenting with frequent or prolonged night wakings) 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 behaviors in children with polysomnographically documented OSAS to similar behaviors in children diagnosed with a BSD (ie, limit-setting and sleep onset association disorder); 2) to compare daytime behaviors 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.
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 disorder 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 breathing. However, when severity of OSAS was defined by polysomnographic variables (number of apneas and hypopneas/hour and the nadir O[SUB 2] saturation), the OSAS-P group had significantly more severe disease than the OSAS-BSD group. In fact, the children in the OSAS-P group had more than twice the number of apneas and hypopneas/hour on polysomnography 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-walking, sleep-talking, and nightmares, were not significantly 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. 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 compared with a control group, but was similar to the incidence of parasomnias in children with a BSD.( This suggests that factors common to both OSAS and BSDs, such as sleep fragmentation resulting in increased rebound delta sleep, may be more important than hypoxia in determining the occurrence of parasomnias 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 average, to have a longer sleep duration. When compared with age-adjusted norms, the average sleep duration for the BSD group of 8.4 hours (compared with 10.5 hours in the OSAS group) was significantly below even the 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 speculate 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 represented 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 reported a relatively high incidence of behavioral sleep problems in childhood OSAS; Guilleminault et al describe significant bedtime refusal, behavioral "hyperactivity" at bedtime, and significant anxiety related to falling asleep in three of eight children diagnosed with OSAS. Similarly, Miyazaki et al 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 Loughlin state that, in their experience, although bedtime problems exist, they "are not common" 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 disorder or a sleep onset association disorder is similar to the prevalence of these BSDs found in other studies of corresponding age groups in the general population. However, failing to clinically screen children 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 sequelae of the OSAS.
Finally, the BSD group overall had a greater number 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 similar to that of other studies that have examined the complex association among daytime externalizing behavior problems, daytime sleepiness, and sleep deprivation or fragmentation in school-aged children.
To further address this issue of the relationship between externalizing daytime behavior problems and daytime sleepiness, we also examined the relative frequencies among the various OSAS and behavioral groups of several daytime sleepiness items that had been included on the sleep questionnaires. Although most of these items (including falling asleep during various activities) were not significantly different among the OSAS-P, OSAS-BSD, and the BSD groups, two daytime sleepiness variables were significantly more common in the same groups that also had more externalizing behavior problems: disrupting family activities because of sleepiness (P < .05), and difficulty waking in the morning (P < .05). This finding lends some additional support to the hypothesis that these externalizing behaviors were at least partially reflective of daytime somnolence, and thus of underlying sleep disturbance.
The behavioral manifestations of daytime sleepiness in young children, such as hyperactivity, clearly overlap with problematic behaviors that do not result from sleep deprivation/disruption. The results 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 externalizing behavior problems in the BSD groups include the possibility that children with oppositional or aggressive behavior during the day are also likely to manifest 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, and multiple observer ratings with parental behavioral observations. - Owens, Judith; Opipari, Lisa; Sleep and Daytime Behavior in Children With Obstructive Sleep Apnea and Behavioral Sleep Disorders; Pediatrics, Nov98, Vol. 102 Issue 5
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QUESTION 18 According to Owens, what are three differences in children with behavioral sleep disorders, as compared to children with obstructive sleep apnea? Record the letter of the correct answer the Answer Booklet .
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