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Neurocognitive and behavioral functioning in adolescents with sleep-disordered breathing: a population-based, dual-energy X-ray absorptiometry study

Abstract

Background/Objectives:

Sleep-disordered breathing (SDB) has been associated with neurocognitive and behavioral problems in young children; however, this association is less studied in adolescents. Evidence suggests that obesity plays a key role in the development of SDB, although its relative association with neurobehavioral functioning remains unclear. We examined whether SDB and obesity are associated with neurocognitive and behavioral problems in adolescents.

Subjects/Methods:

A total of 421 adolescents (17.0±2.2y, 53.9% male) from the Penn State Child Cohort, a general population sample, underwent a 9-h polysomnography, clinical history, physical examination, neurocognitive evaluation and Dual-energy X-ray Absorptiometry (DXA) scan, and completed the Child or Adult Behavior Checklist. Obstructive sleep apnea (OSA) was defined as an apnea–hypopnea index (AHI)2, primary snoring (PS) as AHI<2+snoring and no-SDB as AHI<2 without snoring. Body weight measures included body mass index (BMI) percentile, waist circumference (WC) and DXA-measured total adipose tissue (TAT).

Results:

WC and TAT were significantly associated with impaired vigilance, processing speed, working memory, and control interference and greater internalizing and externalizing behaviors, while BMI percentile was marginally associated. SDB per se (PS, AHI or OSA) was not significantly associated with impaired neurocognitive outcomes or greater behavioral problems. However, TAT was significantly associated with impaired vigilance and greater internalizing and externalizing behaviors and, to a lesser extent, slower processing speed and greater control interference, only in adolescents with OSA.

Conclusions:

Central obesity, an etiopathogenic mechanism of OSA, is more strongly associated with neurocognitive and behavioral problems in adolescents than SDB alone. Deficits in low-order (vigilance) and high-order (executive) functions and behavioral problems observed in adolescents with OSA are primarily associated with increased central adiposity, a finding not entirely captured with less precise measures of obesity. These data support that OSA and its associated neurocognitive and behavioral morbidity are related to underlying metabolic dysfunction as early as adolescence.

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References

  1. Friedman BC, Hendeles-Amitai A, Kozminsky E, Leiberman A, Friger M, Tarasiuk A et al. Adenotonsillectomy improves neurocognitive functioning in children with obstructive sleep apnea syndrome. Sleep 2003; 26: 999–1005.

    Article  Google Scholar 

  2. Kennedy JD, Blunden S, Hirte C, Parsons DW, Martin AJ, Crowe E et al. Reduced neurocognition in children who snore. Pediatr Pulmonol 2004; 37: 330–337.

    Article  CAS  Google Scholar 

  3. Halbower AC, Deganokar M, Barker PB et al. Childhood obstructive sleep apnea associates with neuropsychological deficits and neuronal brain injury. PLoS Med 2006; 3: 1391–1402.

    Article  Google Scholar 

  4. 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: 1–8.

    Article  Google Scholar 

  5. Bourke R, Anderson V, Yang JS, Jackman AR, Killedar A, Nixon GM et al. Cognitive and academic functions are impaired in children with all severities of sleep-disordered breathing. Sleep Med 2011; 12: 489–496.

    Article  Google Scholar 

  6. O’Brien L, Mervis CB, Holbrook CR et al. Neurobehavioral correlates of sleep disordered breathing in children. J Sleep Res 2004; 13: 165–172.

    Article  Google Scholar 

  7. O'Brien LM, Mervis CB, Holbrook CR, Bruner JL, Klaus CJ, Rutherford J et al. Neurobehavioral implications of habitual snoring in children. Pediatrics 2004; 114: 44–49.

    Article  Google Scholar 

  8. Beebe DW, Wells C, Jeffries J, Chini B, Kalra M, Raouf A . Neuropsychological effects of pediatric obstructive sleep apnea. J Int Neuropsychol Soc 2004; 10: 962–975.

    Article  Google Scholar 

  9. Gozal D, Crabtree VM, Sans Capdevila O, Witcher LA, Kheirandish-Gozal L . C-reactive protein, obstructive sleep apnea, and cognitive dysfunction in school-aged children. Am J Respir Crit Care Med 2007; 176: 188–193.

    Article  CAS  Google Scholar 

  10. Honaker SM, Gozal D, Bennett J, Capdevila OS, Spruyt K . Sleep-disordered breathing and verbal skills in school-aged community children. Dev Neuropsychol 2009; 34: 588–600.

    Article  Google Scholar 

  11. Lewin DS, Rosen RC, England SJ, Dahl RE . Prelimary evidence of behavioral and cognitive sequelae of obstructive sleep apnea in children. Sleep Med 2002; 3: 5–13.

    Article  Google Scholar 

  12. Chervin RD, Ruzicka DL, Giordani BJ, Weatherly RA, Dillon JE, Hodges EK et al. Sleep disordered breathing, behavior, and cognition in children before and after adenotonsillectomy. Pediatrics 2006; 117: e769–e778.

    Article  Google Scholar 

  13. Hamasaki Uema SF, Nagata Pignatari SS, Fujita RR, Moreira GA, Pradella-Hallinan M, Weckx L . Assessment of cognitive learning function in children with obstructive sleep breathing disorders. Braz J Otorhinolaryngol 2007; 73: 315–320.

    Article  Google Scholar 

  14. Gozal D, Kheirandish-Gozal L, Bhattacharjee R, Spruyt K . Neurocognitive and endothelial dysfunction in children with obstructive sleep apnea. Pediatrics 2010; 126: e1161–e1167.

    Article  Google Scholar 

  15. Kheirandish-Gozal L, de Jong MR, Spruyt K, Chamuleau SAJ, Gozal D . Obstructive sleep apnoea is associated with impaired pictorial memory task acquisition and retention in children. Euro Respir J 2010; 36: 164–169.

    Article  CAS  Google Scholar 

  16. Biggs SN, Bourke R, Anderson V, Jackman AR, Killedar A, Nixon GM et al. Working memory in children with sleep disordered breathing: objective versus subjective measures. Sleep Med 2011; 12: 887–891.

    Article  Google Scholar 

  17. Kohyama J, Furushima W, Hasegawa T . Behavioral problems in children evaluated for sleep disordered breathing. Sleep Hypn 2003; 5: 89–94.

    Google Scholar 

  18. Tran KD, Nguyen CD, Weedon J, Goldstein NA . Child behavior and quality of life in pediatric obstructive sleep apnea. Arch Otolaryngol Head Neck Surg 2005; 131: 52–57.

    Article  Google Scholar 

  19. Bourke RS, Anderson V, Yang JS, Jackman AR, Killedar A, Nixon GM et al. Neurobehavioral function is impaired in children with all severities of sleep disordered breathing. Sleep Med 2011b; 12: 222–229.

    Article  Google Scholar 

  20. Rosen CL, Storfer-Isser A, Taylor HG, Kirchner L, Emancipator JL, Redline S . Increased behavioral morbidity in school aged children with sleep disordered breathing. Pediatrics 2004; 114: 1640–1648.

    Article  Google Scholar 

  21. Ting H, Wong RH, Yang HJ, Lee SP, Lee SD, Wang L . Sleep disordered breathing, behavior, and academic performance in Taiwan schoolchildren. Sleep Breath 2011; 15: 91–98.

    Article  Google Scholar 

  22. Mulvaney SA, Goodwin JL, Morgan WJ, Rosen GR, Quan SF . Behavior problems associated with sleep disordered breathing in school aged children-the Tucson Children’s Assessment of Sleep Apnea Study. J Ped Psych 2006; 31: 1–7.

    Article  Google Scholar 

  23. Zhao Q, Sherrill DL, Goodwin JL, Quan SF . Association between sleep disordered breathing and behavior in school aged children: The Tucson Children’s Assessment of Sleep Apnea Study. Open Epidemiol J 2008; 1: 1–9.

    Article  Google Scholar 

  24. Marcus CL, Moore RH, Rosen CL, Giordani B, Garetz SL, Taylor HG et al. Childhood Adenotonsillectomy Trial (CHAT). A randomized trial of adenotonsillectomy for childhood sleep apnea. N Engl J Med 2013; 368: 2366–2376.

    Article  CAS  Google Scholar 

  25. Bixler EO, Fernandez-Mendoza J, Liao D, Calhoun S, Rodriguez-Colon SM, Gaines J et al. Natural history of sleep disordered breathing in prepubertal children transitioning to adolescence. Eur Respir J 2016; 47: 1402–1409.

    Article  Google Scholar 

  26. Perfect MM, Archbold K, Goodwin JL, Levine-Donnerstein D, Quan SF . Risk of behavioral and adaptive functioning difficulties in youth with previous and current sleep disordered breathing. Sleep 2013; 36: 517–525B.

    PubMed  PubMed Central  Google Scholar 

  27. Xanthopoulos MS, Gallagher PR, Berkowitz RI, Radcliffe J, Bradford R, Marcus CL . Neurobehavioral functioning in adolescents with and without obesity and obstructive sleep apnea. Sleep 2015; 38: 401–410.

    Article  Google Scholar 

  28. Tan E, Healey D, Schaughency E, Dawes P, Galland B . Neurobehavioral correlates in older children and adolescents with obesity and obstructive sleep apnoea. J Paediatr Child Health 2014; 50: 16–23.

    Article  Google Scholar 

  29. Beebe DW, Ris MD, Kramer ME, Long E, Amin R . The association between sleep disordered breathing, academic grades, and cognitive and behavioral functioning among overweight subjects during middle to late childhood. Sleep 2010; 33: 1447–1456.

    Article  Google Scholar 

  30. Hannon TS, Rofey DL, Ryan CM, Clapper DA, Chakravorty S, Arslanian SA . Relationships among obstructive sleep apnea, anthropometric measures, and neurocognitive functioning in adolescents with severe obesity. J Pediatr. 2012; 160: 732–735.

    Article  Google Scholar 

  31. Rhodes SK, Shimoda KC, Waid LR, O'Neil PM, Oexmann MJ, Collop NA et al. Neurocognitive deficits in morbidly obese children with obstructive sleep apnea. J Pediatr 1995; 127: 741–744.

    Article  CAS  Google Scholar 

  32. Bixler EO, Vgontzas AN, Lin HM, Liao D, Calhoun S, Vela-Bueno A et al. Sleep disordered breathing in children in a general population sample: prevalence and risk factors. Sleep 2009; 32: 731–736.

    Article  Google Scholar 

  33. Rechtschaffen A, Kales AA . Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. US Government Printing Office: Washington, DC, USA, 1968.

    Google Scholar 

  34. Iber C, Ancoli-Israel S, Chesson AL, Quan SF . The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. American Academy of Sleep Medicine: Westchester, IL, USA, 2007.

    Google Scholar 

  35. Gaines J, Vgontzas AN, Fernandez-Mendoza J, Calhoun SL, He F, Liao D et al. Inflammation mediates the association between visceral adiposity and obstructive sleep apnea in adolescents. Am J Physiol Endocrinol Metab 2016; 311: E851–E858.

    Article  Google Scholar 

  36. Carskadon MA, Acebo C . A self-administered rating scale for pubertal development. J Adoles Health 1993; 14: 190–195.

    Article  CAS  Google Scholar 

  37. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z et al. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 2002; 246: 1–190.

    Google Scholar 

  38. Hologic Inc. Body Composition User Guide. Hologic Inc.: Bedford, 2010. Document No. MAN-02354 Revision 001.

  39. Kelly TL, Wilson KE, Ruth CR . Estimating visceral fat by dual-energy X-ray absorptiometry. US Patent Application Number US2010-0234719 (Hologic, Inc., 2010).

  40. Gordon M . The Gordon Diagnostic System. Gordon Systems: DeWitt, NY, 1983.

    Google Scholar 

  41. Wechsler D . Wechsler Intelligence Scale for Children, 4th edn. Psychological Corporation: San Antonio, TX, USA, 2003.

    Google Scholar 

  42. Wechsler D . Wechsler Adult Intelligence Scale, 3rd edn. Psychological Corporation: San Antonio, TX, USA, 1997.

  43. Golden CJ, Freshwater SM, Golden GL . Stroop Color and Word Test Children’s Version. Stoelting: Wood Dale, IL, USA, 2003.

    Google Scholar 

  44. Golden CJ, Freshwater SM . The Stroop Color and Word Test: A Manual for Clinical and Experimental Uses. Stoelting: Chicago, IL, 2002.

    Google Scholar 

  45. Wechsler D . Wechsler Abbreviated Scale of Intelligence. Psychological Corporation: San Antonio, TX, USA, 1999.

    Google Scholar 

  46. Wilkinson GS . Wide Range Achievement Test–Revision 3. Jastak Association: Wilmington, DE, USA, 1993.

    Google Scholar 

  47. Delis DC, Kramer JH, Kaplan E, Ober BA . The California Verbal Learning Test-Children’s Version. Psychological Corporation: San Antonio, TX, USA, 1994.

    Google Scholar 

  48. Delis DC, Kramer JH, Kaplan E, Ober BA . The California Verbal Learning Test-II, 2nd edn. Psychological Corporation: San Antonio, TX, USA, 2000.

  49. Achenbach Tm Rescorla LA . Manual for the ASEBA School-Age Forms and Profiles. ASEBA: Burlington, VT, USA, 2001.

    Google Scholar 

  50. Achenbach TM, Rescorla LA . Manual for the ASEBA Adult Forms & Profiles. ASEBA: Burlington, VT, USA, 2003.

    Google Scholar 

  51. Bixler EO, Vgontzas AN, Lin HM, Calhoun SL, Vela-Bueno A, Kales A . Excessive daytime sleepiness in a general population sample: the role of sleep apnea, age, obesity, diabetes, and depression. J Clin Endocrinol Metab 2005; 90: 4510–4515.

    Article  CAS  Google Scholar 

  52. Fernandez-Mendoza J, Vgontzas AN, Kritikou I, Calhoun SL, Liao D, Bixler EO . Natural history of excessive daytime sleepiness: role of obesity, weight loss, depression, and sleep propensity. Sleep 2015; 28: 351–360.

    Article  Google Scholar 

  53. Tsaoussoglou M, Bixler EO, Calhoun S, Chrousos GP, Sauder K, Vgontzas AN . Sleep-disordered breathing in obese children is associated with prevalent excessive daytime sleepiness, inflammation, and metabolic abnormalities. J Clin Endocrinol Metab 2010; 95: 143–150.

    Article  CAS  Google Scholar 

  54. Youssef NA, Ege M, Angly SS, Strauss JL, Marx CE . Is obstructive sleep apnea associated with ADHD? Ann Clin Psychiatry 2011; 23: 213–224.

    PubMed  Google Scholar 

  55. Tauman R, Gozal D . Obesity and obstructive sleep apnea in children. Paediatr Respir Rev. 2006; 7: 247–259.

    Article  Google Scholar 

  56. Dreber H, Reynisdottir S, Angelin B, Tynelius P, Rasmussen F, Hemmingson E . Mental distress in treatment seeking young adults (18-25 years) with severe obesity compared with population controls of different body mass index levels: Cohort Study. Clin Obes 2017; 7: 1–10.

    Article  CAS  Google Scholar 

  57. Gall K, van Zutven K, Lindstrom J, Bentley C, Gratwick-Sarnil K, Harrison C et al. Obesity and emotional well-being in adolescents: Roles of body dissatisfaction, loss of control eating, and self-rated health. Obesity 2016; 24: 837–842.

    Article  Google Scholar 

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Acknowledgements

This study was partially supported by US National Institutes of Health grants R01 HL63772, R01 HL97165, UL1 RR033184, C06 RR16499.

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Correspondence to J Fernandez-Mendoza.

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Frye, S., Fernandez-Mendoza, J., Calhoun, S. et al. Neurocognitive and behavioral functioning in adolescents with sleep-disordered breathing: a population-based, dual-energy X-ray absorptiometry study. Int J Obes 42, 95–101 (2018). https://doi.org/10.1038/ijo.2017.229

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