Introduction. Clinical manifestations. Overview
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1 Neuropsychologic correlates in pediatric sleep apnea Elise K Hodges PhD ( Dr. Hodges of the University of Michigan received fees from Psychological Assessment Resources, Inc as a consultant. ) Lisa A Harker PsyD ( Dr. Harker of the University of Michigan has no relevant financial relationships to disclose. ) Kimberly P Heinrich PhD ( Dr. Heinrich of the University of Michigan has no relevant financial relationships to disclose. ) Bruno Giordani PhD ( Dr. Giordani of the University of Michigan has no relevant financial relationships to disclose. ) Antonio Culebras MD, editor. ( Dr. Culebras of SUNY Upstate Medical University at Syracuse received an honorarium from Jazz Pharmaceuticals for a speaking engagement.) Originally released January 16, 2012; expires January 16, 2015 Notice: This article has expired and is therefore not available for CME credit. Introduction Overview The association between obstructive sleep apnea (OSA) and neuropsychological functioning has been documented in adults, and although studies show a similar association in children, the findings across studies have been mixed. Previous investigations have shown that children with OSA demonstrate poorer performance on neuropsychological measures of intellectual functioning, attention, executive functioning, visual spatial abilities, and memory in comparison to children without OSA. However, the evidence of a causal role of OSA in the development of these neuropsychological inefficiencies has yet to be identified, and research into possible mechanisms is ongoing. Key points Pediatric obstructive sleep apnea (OSA) is typically associated with adenotonsillar hypertrophy. Neuropsychological investigations of the impact of OSA in children have been mixed. The relationship between OSA and cognitive or behavioral disturbance is complex and without clear predictive findings. The most common treatment for children with OSA is adenotonsillectomy. In those cases in which OSA is not successfully treated by adenotonsillectomy, other treatment options, such as continuous positive airway pressure (CPAP), should be considered. Historical note and terminology Early writings on the relationship between sleep and cognitive functioning go back to the beginning of the 20th century, when William Osler reported on Pickwickian syndrome to describe patients who exhibited both obesity and hypersomnolence (Osler 1918). It wasn't until 1970 that Carolo Tassinari, Elio Lugaresi, and others, who specialized in neurophysiology and electroencephalography, conducted clinical sleep studies and provided a complete description of sleep apnea syndrome, including the first characterization of non-obese adults to exhibit obstructive sleep apnea (OSA). These physicians also observed that clear diagnostic markers for OSA included cardiovascular correlates, snoring, and daytime sleepiness (Dement 2005). At the same time, Guilleminault and colleagues reported on the association between adenotonsillar hypertrophy and OSA in children and suggested that adenotonsillectomy might ameliorate associated symptoms (Guilleminault et al 1976; 1981; 1982). Guilleminault was also the first to describe the impact on daytime functioning in children, reporting that poor performance of math problems improved after adenotonsillectomy (Guilleminault et al 1976). Following this landmark paper, numerous studies have been undertaken to explore and characterize features of pediatric OSA, as well as the impact on neuropsychological performances. Clinical manifestations Presentation and course Pediatric OSA is now recognized to be part of a spectrum of disorders characterized by repeated events of partial or complete upper airway obstruction during sleep (Katz and Marcus 2005). The phenotype of sleep-disordered breathing in children is variable, but the most prominent symptom is snoring (O'Brien and Gozal 2005). Although primary snoring is not usually associated with apnea, it is usually an indication of OSA when it is accompanied by gasps, pauses in
2 breathing, or arousals from sleep. OSA 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 OSA have disproportionately larger adenoids and tonsils than their typically developing peers (Arens et al 2003; Pashayan and Passannante 2005; Gozal 2008; Lumeng and Chervin 2008). Other factors can also contribute to OSA 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, second edition, classifies sleep disorders into 8 major categories: insomnia, sleep-related breathing disorder, hypersomnia of central origin, circadian rhythm sleep disorders, parasomnias, sleep-related movement disorders, isolated symptoms and normal variants, and other sleep disorders. Within this system, OSA falls in the sleep-related breathing disorders category, and it applies to both adults and child populations (American Academy of Sleep Medicine 2005). Neuropsychological correlates of OSA. Results of investigations examining neuropsychological correlates of OSA in children have been quite variable, most likely related to differences in study design. For example, studies have differed in their quantification of sleep disorder, with some depending on parents' report of sleep disturbance, whereas others employed objective assessment of OSA through polysomnography (Beebe 2006; Hodges et al 2008). 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 (Baron 2004). Some investigations of OSA in children included measures of intellectual functioning and reported that children with OSA tend to have lower scores than healthy, normal control children; however, the obtained scores of those with OSA fall within normal limits (Blunden et al 2000; O'Brien et al 2004; Giordani et al 2008). A recent study by 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 (Kohler et al 2010). 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 (Giordani et al 2008). 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 (Blunden et al 2000; O'Brien et al 2004; Giordani et al 2008), whereas those that did not used abbreviated batteries that estimate general intellect (Gozal et al 2001; Chervin et al 2006; Kohler et al 2009; 2010). 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 OSA (Beebe 2006). Several studies have been published examining the impact of OSA on executive functioning, though again, with variable results. For example, Beebe and colleagues found an association between executive functioning and OSA (Beebe et al 2004). Specifically, they compared the neuropsychological performances of children referred to a sleep center due to concerns related to OSA versus community controls. The groups were characterized as primary snorers, mild OSA, moderate OSA, and controls. He reported that OSA 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 (Giordani et al 2008). 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 OSA 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) (Baron 2004). The research evidence linking OSA and memory has been mixed. For example, Blunden and colleagues found that children with OSA showed poorer performance on memory screen (Blunden et al 2000), and Kaemingk found a similar association on a verbal learning task (Kaemingk et al 2003). However, O'Brien and colleagues failed to find an association between memory performance and OSA in their group (O'Brien et al 2004). Giordani and colleagues found delayed visual memory differences between children referred for adenotonsillectomy and control groups, although the
3 difference between the adenotonsillectomy group with OSA and the adenotonsillectomy group without OSA was not significant, suggesting that OSA was not necessarily the key contributing factor (Giordani et al 2008). 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 OSA and controls on these measures, except for one study that involved copying a complex figure (Baron 2004; Beebe et al 2004). In summary, the neuropsychological association with OSA is 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 OSA underlies the majority of cognitive deficits that have been tied to sleep disturbance in children. It is also possible that the alterations in brain functioning due to OSA occur earlier in child development, and by the time children with OSA reach school age, the issues resolve or are fixed and no longer variable with respect to severity of OSA. It is also important to note that most studies do show that parent ratings appear to be sensitive to behavioral aspects associated with OSA, as most studies that include parent ratings show that children with OSA are generally more symptomatic than control groups included (Beebe 2006). 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 OSA may be the primary factors leading to disruption in cognitive functioning, such as body mass index, presence of allergic rhinitis or repeated throat infections, and use of steroid inhalers. Biological basis Etiology and pathogenesis The etiology of neuropsychological deficits in children with OSA is unknown, though possible associated factors include the cumulative effect of hypoxemia over time, cumulative effects of sleep fragmentation, or obesity-related issues (Arens et al 2003; American Academy of Sleep Medicine 2005; Katz and Marcus 2005; Pashayan and Passannante 2005; Beebe 2006; Gozal 2008; Lumeng and Chervin 2008). The underlying mechanisms that contribute to the neuropsychological difficulties in OSA are likely variable and multifactorial, involving multiple brain regions, neurotransmitter substances, and other factors. For example, the chronic and cumulative effect of hypoxemia over time or repeated episodes of sleep fragmentation may cause disruption in the normal development of the prefrontal cortex and related structures (Beebe 2006; Giordani et al 2008). Although the prefrontal cortex has been shown to be particularly susceptible to disruption associated with hypoxemia in adults and animals, a clearly established link has not been documented in children (Beebe et al 2004). In addition, other structures such as the hippocampus have also been implicated. For example, mouse models have shown associations between OSA and oxidative stress that contribute to cell death within the hippocampus. These structural alternations further cause a reduction in hippocampal long-term potentiation as well as functional deficits in spatial learning (Kaemingk et al 2003). Although these specific pathophysiological findings have not been documented in children, Giordani's findings related to delayed visual memory suggest that such associations are possible. Research has also begun to establish the association of elevations in proinflammatory markers in children with OSA as well as symptoms of daytime sleepiness and difficulties in school (Gozal et al 2008). Although some may argue that proinflammatory markers may be a consequence of obesity, which is known to be associated with OSA, Gozal recently reported on a group of non-obese children who exhibited elevated proinflammatory markers in the presence of OSA (Gozal et al 2008). Thus, evidence is accumulating that sleep-disordered breathing in children is associated with neurophysiologic and neuroanatomic compromise that contributes to neurobehavioral morbidity. Epidemiology" Large-scale epidemiologic studies of OSA and neuropsychological deficits in children with OSA have not been completed. However, given that lab-based studies of OSA report prevalence estimates of 1% to 4%, the percentage of children within this group who also demonstrate deficient neuropsychological functioning is probably less than the estimates of prevalence of OSA (Lumeng and Chervin 2008).
4 Prevention Because there is no single underlying mechanism that causes neuropsychological deficits related to OSA, prevention recommendations are difficult. Nevertheless, in cases of OSA where obesity is a substantial factor, weight loss programs are recommended. In cases where OSA is caused by adenotonsillar hypertrophy, adenotonsillectomy is the treatment of choice (Rosen 2004). Differential diagnosis Patients who present with the more common neuropsychological symptoms associated with OSA, including inattention, hyperactivity, or learning problems, should also be screened for symptoms of OSA as the percentage of children with attention deficit hyperactivity disorder who may also suffer from sleep-disordered breathing has been estimated in the range of 15% to 25% (O'Brien et al 2004; American Academy of Sleep Medicine 2005; Katz and Marcus 2005; Chervin et al 2006). Although it is unknown if surgical treatment for OSA provides relief or remission of neurobehavioral problems in children with OSA, accumulating evidence suggests that parents and physicians need to consider this possibility, along with medication or other alternative approaches used to control these conditions (Hoban and Chervin 2007). Diagnostic workup Evaluation of the symptoms of sleep-disordered breathing using parent rating scales may be helpful as an initial screen of possible sleep-disordered breathing symptoms. The Pediatric Sleep Questionnaire (PSQ) (Chervin et al 2000) and the Obstructive Sleep Apnea Quality of Life Survery-18 (OSA-18) (Franco et al 2000) are examples. Overnight polysomnography continues to be the gold standard in evaluation of OSA in children. This method measures and quantifies ventilatory symptoms and sleep abnormalities associated with sleep-disordered breathing, but involves overnight stays in sleep laboratories so that respiratory functions, sleep-wake cycles, cardiac function, oxygen saturation, and carbon dioxide tension and behavior can be monitored. Management Treatment of OSA in children can involve several modalities. However, because the most common cause of OSA in children is adenotonsillar hypertrophy, the most common treatment is adenotonsillectomy. Because adenotonsillectomy may not provide complete remission of OSA-related neuropsychological inefficiencies, a work-up by a neuropsychologist when issues arise may be helpful (Hoban and Chervin 2007). Outcomes In cases where adenotonsillectomy is performed, rates of remission from OSA have been reported as high as 85% (Rosen 2004). However, in cases where surgery cannot be performed or in cases where surgery has not provided remission, the use of continuous positive airway pressure (CPAP) and bilevel positive airway pressure BiPAP can be considered postoperatively in order to improve the airway. It is important to note that compliance with these devices can be quite poor, and they are not typically recommended for children with adenotonsillar hypertrophy. In addition, studies examining the impact of adenotonsillectomy on OSA outcomes have not been supportive (Hoban and Chervin 2007). For example, in a longitudinal study of children with OSA referred for adenotonsillectomy, Giordani and colleagues found that children exhibited declines in learning and memory measures, as well as verbal abstraction, suggesting the need for ongoing monitoring following surgery (Giordani et al 2012). References cited American Academy of Sleep Medicine. International classification of sleep disorders: Diagnostic and coding manual. 2nd edition. Westchester, IL: American Academy of Sleep Medicine, Arens R, McDonough JM, Corbin AM, et al. Upper airway size analysis by magnetic resonance imaging of children with obstructive sleep apnea syndrome. Am J Respir Crit Care Med 2003;167(1): PMID Baron IS. Intelligence testing: General considerations. In: Neuropsychological Evaluation of the Child. New York, NY: Oxford, 2004:
5 Beebe DW. Neurobehavioral morbidity associated with disordered breathing during sleep in children: a comprehensive review. Sleep 2006;29(9): PMID Beebe DW, Wells CT, Jeffries J, Chini B, Kalra M, Amin R. Neuropsychological effects of pediatric obstructive sleep apnea. J Int Neuropsychol Soc 2004;10(7): PMID Blunden S, Lushington K, Kennedy D, Martin J, Dawson D. Behavior and neurocognitive performance in children aged 5-10 years who snore compared to controls. J Clin Exp Neuropsychol 2000;22(5): PMID Chervin RD, Hedger K, Dillon JE, Pituch KJ. Pediatric sleep questionnaire (PSQ): validity and reliability of scales for sleep-disordered breathing, snoring, sleepiness, and behavioral problems. Sleep Med 2000;1(1): PMID Chervin RD, Weatherly RA, Ruzicka DL, et al. Subjective sleepiness and polysomnographic correlates in children scheduled for adenotonsillectomy vs other surgical care. Sleep 2006;29(4): PMID Dement WC. History of sleep medicine. Neurol Clin 2005;23(4): PMID Franco R, Rosenfeld R, Rao M. First place resident clinical science award Quality of life for children with obstructive sleep apnea. Otolaryngol Head Neck Surg 2000;123(1 Pt 1):9-16. PMID Giordani B, Hodges EK, Guire KE, et al. Neuropsychological and behavioral functioning in children with and without obstructive sleep apnea referred for tonsillectomy. J Int Neuropsychol Soc 2008;14(4): PMID Giordani B, Hodges EK, Guire KE, et al. Changes in neuropsychological and behavioral functioning in children with and without obstructive sleep apnea following tonsillectomy. J Int Neuropsychol Soc 2012;18(2): PMID Gozal D. Matters of the heart: the brain in pediatric sleep apnea. Am J Respir Crit Care Med 2008:178(8): PMID Gozal D, Serpero LD, Sans Capdevila O, Kheirandish-Gozal L. Systemic inflammation in non-obese children with obstructive sleep apnea. Sleep Medicine 2008;9(3): PMID Gozal D, Wang M, Pope DW Jr. Objective sleepiness measures in pediatric obstructive sleep apnea. Pediatrics 2001;108(3): PMID Guilleminault C, Eldridge FL, Simmons FB, Dement WC. Sleep apnea in eight children. Pediatrics 1976;58(1): PMID Guilleminault C, Korobkin R, Winkle R. A review of 50 children with obstructive sleep apnea syndrome. Lung 1981;159(5): PMID Guilleminault C, Winkle R, Korobkin R, Simmons B. Children and nocturnal snoring: evaluation of the effects of sleep related respiratory resistive load and daytime functioning. Eur J Pediatr 1982;139(3): PMID Hoban TF, Chervin RD. Sleep-related breathing disorders of childhood: description and clinical picture, diagnosis, and treatment approaches. Sleep Med Clin 2007;2(3): Hodges EK, Bloomfield E, Coulas T, Giordani B. Cognitive and behavioral change after adenotonsillectomy in children with sleep-disordered breathing. A review. Minerva Psychiatrica 2008;49(4): Kaemingk KL, Pasvogel AE, Goodwin JL, et al. Learning in children and sleep disordered breathing: findings of the Tucson Children's Assessment of Sleep Apnea (tucasa) prospective cohort study. J Int Neuropsychol Soc 2003;9(7): PMID Katz ES, Marcus CL. Diagnosis of obstructive sleep apnea in infants and children. In: Sheldon SH, Ferber R, Kryger MH, editors. Principles and Practice of Pediatric Sleep Medicine. Elsevier Saunders, 2005: Kohler MJ, Lushington K, Kennedy JD. Neurocognitive performance and behavior before and after treatment for sleepdisordered breathing. Nat Sci Sleep 2010;2: PMID
6 Kohler MJ, Lushington K, van den Heuvel CJ, Martin J, Pamula Y, Kennedy D. Adenotonsillectomy and neurocognitive deficits in children with sleep disordered breathing. PLoS One 2009;4(10):e7343. PMID Lumeng JC, Chervin RD. Epidemiology of pediatric obstructive sleep apnea. Proc Am Thorac Soc 2008;5(2): PMID O'Brien LM, Gozal D. Consequences of obstructive sleep apnea syndrome. In: Sheldon SH, Ferber R, Kryger MH, editors. Principles and Practice of Pediatric Sleep Medicine. Elsevier Saunders, 2005: O'Brien LM, Mervis CB, Holbrook CR, et al. Neurobehavioral correlates of sleep-disordered breathing in children. J Sleep Res 2004;13(2): PMID Osler W. The principle and practice of medicine. Eighth ed Rosen CL. Obstructive sleep apnea syndrome in children: controversies in diagnosis and treatment. Pediatr Clin N Am 2004;51(1): **References especially recommended by the author or editor for general reading. ICD and OMIM codes ICD codes ICD-9: Obstructive sleep apnea: Profile Age range of presentation years years Sex preponderance male=female Family history family history may be obtained Heredity None Differential diagnosis list Attention deficit hyperactivity disorder Associated disorders Down syndrome Marfan syndrome Prader-Willi syndrome Other topics to consider Intellectual disability Sleep and medical disorders Sleep disorders
7 Obstructive sleep apnea Copyright MedLink Corporation. All rights reserved.
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