Presentation and course
Pediatric obstructive sleep apnea is now recognized to be part of a spectrum of disorders characterized by repeated events of partial or complete upper airway obstruction during sleep. The phenotype of sleep-disordered breathing in children is variable, but the most prominent symptom is snoring (37). Although primary snoring is not usually associated with apnea, it is usually an indication of obstructive sleep apnea when it is accompanied by gasps, pauses in breathing, or arousals from sleep. Obstructive sleep apnea is caused by upper airway resistance or obstruction during sleep, typically associated with enlarged adenoids and/or tonsils. Though adenoids and tonsils have a typical developmental trajectory with decreasing size over time, children with obstructive sleep apnea have disproportionately larger adenoids and tonsils than their typically developing peers (24). Other factors can also contribute to obstructive sleep apnea in children such as abnormalities in craniofacial features, including retrognathia, and micrognathia, as well as the presence of underlying genetic syndromes such as Down syndrome, Prader-Willi syndrome, or Marfan syndrome. The International Classification of Sleep Disorders, 3rd edition, classifies sleep disorders into seven major categories: insomnia, sleep-related breathing disorder, hypersomnia of central origin, circadian rhythm sleep-wake disorders, parasomnias, sleep-related movement disorders, and “other” sleep disorders. Within this system, obstructive sleep apnea falls in the sleep-related breathing disorders category, and it applies to both adults and child populations (02).
Neuropsychological correlates of obstructive sleep apnea. Results of investigations examining neuropsychological correlates of obstructive sleep apnea in children have been quite variable, most likely related to differences in study design. For example, studies have differed in their definition and quantification of the sleep disorder, with some depending on parents’ report of sleep disturbance, whereas others employed objective assessment of obstructive sleep apnea through polysomnography (04; 27). Outcome measures have also differed, with some reports relying primarily on parental report of behavior or cognitive performance. Within cognitive domains, as well, some studies have emphasized general intellectual functioning, whereas others have included more specific areas of cognitive performance.
Intellectual functioning has a long history of study in the psychological sciences and was originally hypothesized as a construct using a single overall score from intelligence tests. The concept of intelligence has evolved over time to include several skill areas, most notably verbal and nonverbal domains (03). Some investigations of obstructive sleep apnea in children included measures of intellectual functioning and reported that children with obstructive sleep apnea tend to have lower scores than healthy, normal control children; however, the obtained scores of those with obstructive sleep apnea fall within normal limits (07; 39; 16). Kohler and colleagues found a range of deficits in children with documented sleep-disordered breathing, including poorer performance on measures of intellectual functioning as well as language and executive functioning, in comparison to controls (32). Hunter and colleagues found that children who snore performed less efficiently and with less capability across verbal and nonverbal cognitive demands (28). Lee and colleagues found that children with Down syndrome and obstructive sleep apnea, defined as greater than 1 on the apnea-hypopnea index, were associated with lower subtest scores of language domain and lower scores of expressive communications (35). However, other studies have failed to find this association. For example, Giordani and colleagues examined baseline neuropsychological performance in children (aged 5 to 12 years) referred for adenotonsillectomy versus surgical controls and did not find differences in intellectual functioning (16). The discrepancy across studies may be due to differences in the tests that were used, as those that found an association used comprehensive batteries of intellectual functioning (07; 39; 16), whereas those that did not used abbreviated batteries that estimate general intellect (20; 11; 33; 32).
Executive functioning is a complex concept but is generally thought to comprise skills such as planning ability, behavioral inhibition, and concept formation and is hypothesized to be a key domain affected by obstructive sleep apnea (04). Several studies have been published examining the impact of obstructive sleep apnea on executive functioning, though again, with variable results. For example, Beebe and colleagues found an association between executive functioning and obstructive sleep apnea (05). Specifically, they compared the neuropsychological performances of children referred to a sleep center due to concerns related to obstructive sleep apnea versus community controls. The groups were characterized as “primary snorers,” “mild obstructive sleep apnea,” “moderate obstructive sleep apnea,” and “controls.” He reported that obstructive sleep apnea was related to behavioral regulation and executive functioning, though no other differences were observed on other cognitive domains. However, Giordani and colleagues did not find significant differences on measures of executive functioning, although working memory differences were observed (16). The Pre-School OSA Tonsillectomy Adenoidectomy Study (POSTA) assessed executive functioning between children with primary snoring (AHI < 1) and obstructive sleep apnea (AHI > 1) (09). No statistical difference was observed between the two groups, but high median subscores were noted. This suggests that there is a high proportion of behavioral problems in preschool children with primary snoring or obstructive sleep apnea. The Tucson Children’s Assessment of Sleep Apnea study identified a negative correlation between the apnea-hypopnea index (AHI) and immediate recall, full scale intelligence quotient, performance IQ, and math achievement (30). Five-year follow-up results demonstrated that youth with untreated obstructive sleep apnea demonstrated hyperactivity, attention problems, aggressive behaviors, lower social competencies, poorer communication, and/or diminished adaptive skills (41). The discrepancies between these findings could be due to differences in the executive functioning measures used, or it is also possible that when executive measures include working memory, the associations with obstructive sleep apnea may account for the significant impairment in executive-related functioning.
Memory refers to the ability to take in and retain information over an extended period of time. Explicit memory includes both episodic (conscious memory for events) and semantic memory (fact knowledge) (03). The research evidence linking obstructive sleep apnea and memory has been mixed. For example, Blunden and colleagues found that children with obstructive sleep apnea showed poorer performance on memory screen (07), and Kaemingk found a similar association on a verbal learning task (30). However, O’Brien and colleagues failed to find an association between memory performance and obstructive sleep apnea in their group (39). Giordani and colleagues found delayed visual memory differences between children referred for adenotonsillectomy and control groups, although the difference between the adenotonsillectomy group with obstructive sleep apnea and the adenotonsillectomy group without obstructive sleep apnea was not significant, suggesting that obstructive sleep apnea was not necessarily the key contributing factor (16).
Visual perception and visuoconstruction refers to the ability to accurately perceive visual stimuli, copy a complex figure, or construct block designs under timed conditions. Researchers have failed to find any differences between children with obstructive sleep apnea and controls on these measures, except for one study that involved copying a complex figure (03; 05).
In summary, the neuropsychological associations with obstructive sleep apnea are inconsistent across studies. The reasons for this lack of consistency are puzzling and suggest that some perhaps more subtle, yet clinically significant disorder, other than obstructive sleep apnea underlies most cognitive deficits that have been tied to sleep disturbance in children. It is also possible that the alterations in brain functioning due to obstructive sleep apnea occur earlier in child development, and by the time children with obstructive sleep apnea reach school age, the issues resolve or are fixed and no longer variable with respect to severity of obstructive sleep apnea. It is also important to note that most studies do show that parent ratings appear to be sensitive to behavioral aspects associated with obstructive sleep apnea, as most studies that include parent ratings show that children with obstructive sleep apnea are generally more symptomatic than control groups included (04). It is possible that parents are detecting symptoms that objective neuropsychological measures do not. It also is possible that the generally more robust relationship between parental behavior ratings and polysomnography findings as compared to objective neuropsychological test results may be related to parents’ expectations of these behavioral problems and parents’ obvious awareness of sleep symptoms. Finally, other symptoms associated with obstructive sleep apnea may be the primary factors leading to disruption in cognitive functioning, such as elevated body mass index, presence of allergic rhinitis or repeated throat infections, and use of steroid inhalers.