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Cognition and nocturnal disturbance in OSA: the importance of accounting for age and premorbid intelligence

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Abstract

Introduction

Obstructive sleep apnea (OSA) is a common disorder that is associated with impaired attention, memory and executive function. However, the mechanisms underlying such dysfunction are unclear. To determine the influence of sleep fragmentation and hypoxia, this study examined the effect of sleep fragmentation and hypoxia on cognition in OSA, while controlling for potentially confounding variables including sleepiness, age and premorbid intelligence.

Method

Participants with and without OSA (N = 150) were recruited from the general community and a tertiary hospital sleep clinic. All underwent comprehensive, laboratory-based polysomnography (PSG) and completed assessments of cognition including attention, short- and long-term memory and executive function. Structural equation modelling (SEM) was used to construct a theoretically-driven model to examine the relationships between hypoxia and sleep fragmentation, and cognitive function.

Results

Although after controlling for IQ, increased sleep disturbance was a significant predictor of decreased attention (p = 0.04) and decreased executive function (p = 0.05), controlling for age removes these significant relationships. No significant predictors of memory function were found.

Conclusions

The mechanisms underlying the effects of OSA on cognition remain to be defined. Implications are discussed in light of these findings.

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Notes

  1. Other indices of sleep fragmentation (e.g. TST, ArI during REM) and the following measures of hypoxia: CT90, Lowest SaO2 during REM, Mean SaO2 during REM, were considered and tested. None accounted for sufficient variance in cognitive performance to be included.

  2. All supplementary tables are available from Research Gate: https://www.researchgate.net/publication/261676388_Cognition_and_nocturnal_disturbance_in_OSA_the_importance_of_accounting_for_age_and_premorbid_intelligence#share

References

  1. Young T, Peppard PE, Gottlieb DJ (2002) Epidemiology of obstructive sleep apnea. Am J Respir Crit Care Med 165(9):1217–1239

  2. Kryger MH (2010) Atlas of clinical sleep medicine. Saunders Elsevier, Philadelphia

    Google Scholar 

  3. Beebe DW, Groesz L, Wells C, Nichols A, McGee K (2003) The neuropsychological effects of obstructive sleep apnea: a meta-analysis of norm-referenced and case-controlled data. Sleep 26:298–307

    PubMed  Google Scholar 

  4. Bucks R, Olaithe M, Eastwood P (2012) Neurocognitive function in obstructive sleep apnoea: A meta-review. Respirology 18(1):61–70

  5. Fulda S, Schulz H (2003) Cognitive dysfunction in sleep-related breathing disorders: a meta-analysis. Sleep Res Online 5:19–51

    Google Scholar 

  6. Aloia MS, Arnedt T, Davis JD, Riggs RL, Byrd D (2004) Neuropsychological sequelae of obstructive sleep apnea-hypopnea syndrome: a critical review. J Int Neuropsychol Soc 10:772–785

    Article  PubMed  Google Scholar 

  7. Wallace A, Bucks RS (2012) Memory and Obstructive Sleep Apnoea: A Meta-Analysis. Sleep 36(2):203–220

  8. Olaithe M, Bucks R (2013) Executive dysfunction in OSA before and after treatment: a meta-analysis. Sleep 36:1297–1305

    PubMed Central  PubMed  Google Scholar 

  9. Saunamäki T, Jehkonen M (2007) A review of executive functions in obstructive sleep apnea syndrome. Acta Neurol Scand 115:1–11

    Article  PubMed  Google Scholar 

  10. Beebe DW, Gozal D (2002) Obstructive sleep apnea and the prefrontal cortex: Towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. J Sleep Res 11:1–16

    Article  PubMed  Google Scholar 

  11. Poe G, Walsh CM, Bjorness TE (2010) Cognitive neuroscience of sleep. Prog Brain Res 185:1–19

    Article  PubMed Central  PubMed  Google Scholar 

  12. Everson CA (1995) Functional consequences of sustained sleep deprivation in the rat. Behav Brain Res 69:43–54

    Article  CAS  PubMed  Google Scholar 

  13. Alhola P, Polo-Kantola P (2007) Sleep deprivation: Impact on cognitive performance. Neuropsychiatr Dis Treat 3:553–567

    PubMed Central  PubMed  Google Scholar 

  14. Durmer JS, Dinges DF (2005) Neurocognitive Consequences of Sleep Deprivation. Seminars in Neurology 25(1):117–129

  15. Verstraeten E, Cluydts R, Pevemagie D, Hoffman G (2004) Executive function in sleep apnea: controlling for attentional capacity in assessing executive attention. Sleep 27:685–693

    PubMed  Google Scholar 

  16. Stepanski EJ (2002) The effect of sleep fragmentation on daytime function. Sleep 25:268–276

    PubMed  Google Scholar 

  17. Verstraeten E, Cluydts R (2004) Executive control of attention in sleep apnea patients: Theoretical concepts and methodological considerations. Sleep Med Rev 8:257–267

    Article  PubMed  Google Scholar 

  18. Ayalon L, Ancoli-lsrael S, Aka AA, McKenna BS, Drummond SP (2009) Relationship between obstructive sleep apnea severity and brain activation during a sustained attention task. Sleep: J Sleep Sleep Disord Res 32:373–381

    Google Scholar 

  19. Bartlett D, Rae C, Thompson C, Byth K, Joffe D et al (2004) Hippocampal area metabolites relate to severity and cognitive function in obstructive sleep apnea. Sleep Med 5:593–596

    Article  PubMed  Google Scholar 

  20. Chiang AA (2006) Obstructive sleep apnea and chronic intermittent hypoxia: a review. Chin J Physiol 49:234–243

    CAS  PubMed  Google Scholar 

  21. Hopkins RO, Kesner RP, Goldstein M (1995) Memory for novel and familiar spatial and linguistic temporal distance information in hypoxic subjects. J Int Neuropsychol Soc 1:454–468

    Article  CAS  PubMed  Google Scholar 

  22. Naismith S, Winter V, Gotsopoulos H, Hickie I, Cistulli P (2011) Neurobehavioral functioning in obstructive sleep apnea: Differential effects of sleep quality, hypoxemia and subjective sleepiness. J Clin Exp Neuropsychol 26:43–54

    Article  Google Scholar 

  23. Gale SD, Hopkins RO (2004) Neuroimaging and neuropsychological findings following carbon monoxide poisoning and obstructive sleep apnea. J Int Neuropsychol Soc 10:60–71

    Article  PubMed  Google Scholar 

  24. Saunamäki T, Himanen S-L, Polo O, Jehkonen M (2010) Executive dysfunction and learning effect after continuous positive airway pressure treatment in patients with obstructive sleep apnea syndrome. Eur Neurol 63:215–220

    Article  PubMed  Google Scholar 

  25. Naismith S, Winter V, Gotsopoulos H, Hickie I, Cistulli P (2004) Neurobehavioral functioning in obstructive sleep apnea: Differential effects of sleep quality, hypoxemia and subjective sleepiness. J Clin Exp Neuropsychol 26:43–54

    Article  CAS  PubMed  Google Scholar 

  26. Alchanatis ZN, Deligiorgis N, Amfilochiou A, Dionellis G et al (2005) Sleep apnea-related cognitive deficits and intelligence: an implication of cognitive reserve theory. J Sleep Res 14:69–75

    Article  PubMed  Google Scholar 

  27. Alchanatis ZN, Deligiorgis N, Chroneou A, Soldatos C et al (2008) Comparison of cognitive performance among different age groups in patients with obstructive sleep apnea. Sleep Breathing 12:17–24

    Article  PubMed  Google Scholar 

  28. Durmer JS, Dinges DF (2005) Neurocognitive consequences of sleep deprivation. Semin Neurol 25:117–129

    Article  PubMed  Google Scholar 

  29. Guilleminault C, Brooks SN (2001) Excessive daytime sleepiness; a challenge for the practising neurologist. Brain 124:1482–1491

    Article  CAS  PubMed  Google Scholar 

  30. AASM (2007) The AASM manual for the scoring of sleep and associated events; rules, terminology and technical specifications. Iber C, Ancoli-Israeli S, Chesson AL, Quan SF (ed) American Academy of Sleep Medicine, Illinois

  31. Wesnes KA (2000) Predicting, assessing, differentiating and treating the dementias: experience in MCI and various dementias using the CDR computerised cognitive assessment system. In: Vellas B, Fitten LI (eds) Research and practice in Alzheimer’s disease. Serdi, Paris, pp 59–65

    Google Scholar 

  32. Van Den Goor JM, Saxby BK, Tijssen TG, Wesnes KA, de Mol BA et al (2008) Improvement of cognitive test performance in patients undergoing primary CABG and other CPB-assisted cardiac procedures. Perfusion 23:267–273

    Article  PubMed  Google Scholar 

  33. Royall DR, Cordes JA, Polk M (1998) CLOX: an executive clock drawing task. J Neurol Neurosurg Psychiatry 64:588–594

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Partington JE, Leiter RG (1949) Partington's pathway test. Psychol Serv Center Bull 1:9–20

    Google Scholar 

  35. Reitan RM (1958) Validity of the trail making test as an indicator of organic brain damage. Percept Mot Skills 8:271–276

    Article  Google Scholar 

  36. AASM (1999) Sleep-related breathing disorders in adults: Recommendations for Syndrome Definition and Measurement Techniques in Clinical Research. Sleep 22:667–689

    Google Scholar 

  37. Nelson HE, Willison J (1991) National Adult Reading Test Manual. NFER-Nelson, Wilson

    Google Scholar 

  38. McGurn B, Starr JM, Topfer JA, Pattie A, Whiteman MC et al (2004) Pronunciation of irregular words is preserved in dementia, validating premorbid IQ estimation. Neurology 62:1184–1186

    Article  CAS  PubMed  Google Scholar 

  39. Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14:540–545

    CAS  PubMed  Google Scholar 

  40. Olaithe M, Skinner TC, Clarke J, Eastwood P, Bucks RS (2012) Can we get more from the Epworth Sleepiness Scale than just one score? a confirmatory factor analysis of the ESS. Sleep Breathing 17:763–769

    Article  PubMed  Google Scholar 

  41. IBM (2012) IBM SPSS Statistics for Windows. 21.0 ed. IBM Corporation, Armonk

  42. Sulit L, Siorfer-Isser A, Kirchner L, Redline S (2006) Differences in polysomnography predictors for hypertension and impaired glucose tolerance. Sleep 29:777–783

    PubMed  Google Scholar 

  43. Cohen J, Cohen P (1983) Applied multiple regression/correlation analysis for the behavioral sciences Hillsdale. Erlbaum, NJ

    Google Scholar 

  44. Lei M, Lomax RG (2005) The Effect of Varying Degrees of Nonnormality in Structural Equation Modeling. Struct Equ Model 12:1–27

    Article  Google Scholar 

  45. Ullman JB, Bentler PM (2012) Structural equation modeling. In: Weiner IB (ed) Handbook of psychology, 2nd edn. John Wiley & Sons, Wiley Online Library

    Google Scholar 

  46. Iaccobucci D (2010) Structural equation modelling: Fit indices, sample size, and advanced topics. J Consum Psychol 20:90–98

    Article  Google Scholar 

  47. Byrne BM (2010) Structural Equation Modelling with AMOS: Basic concepts, application and programming (2nd Ed.). Structural Equation Modelling with AMOS: Basic concepts, application and programming. Taylor & Francis Group, New York

    Google Scholar 

  48. MacCallum RC, Austin JT (2010) Applications of structural equation modelling in psychology research. Annu Rev Psychol 51:201–226

    Article  Google Scholar 

  49. Schreiber JB, Stage FK, King J, Nora A, Barlow EA (2006) Reporting structural equation modeling and confirmatory factor analysis results: a review. J Educ Res 99:323–337

    Article  Google Scholar 

  50. Hu L, Bentler PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Struct Equ Model 6:1–55

    Article  Google Scholar 

  51. IBM (2012) IBM AMOS Statistics for Windows 21.0 ed. IBM Corporation, Armonk

    Google Scholar 

  52. Kribbs NB, Pack AI, Kline LR, Getsy JE, Schuett JS et al (1993) Effects of one night without nasal CPAP Treatment on sleep and sleepiness in patients with obstructive sleep apnea. Am Rev Respir Disord 147:1162–1168

    Article  CAS  Google Scholar 

  53. Tsai JCG (2010) Neurological and neurobehavioural sequelae of obstructive sleep apnea. Neurorehabilitation 26:85–94

    PubMed  Google Scholar 

  54. Deegan JJ (1978) On the occurrence of standardized regression coefficients greater than one. Educ Psychol Meas 38:873–888

    Article  Google Scholar 

  55. Joreskog KG (1999) How large can a standardized coefficient be. Unpublished report: SSI Central, Inc. pp. http://www.ssicentral.com/lisrel/techdocs/HowLargeCanaStandardizedCoefficientbe.pdf. June 2013

  56. Alchanatis ZN, Deligiorgis N, Liappas I, Chroneou A et al (2008) Comparison of cognitive performance among different age groups in patients with obstructive sleep apnea. Sleep Breathing 12:17–24

    Article  PubMed  Google Scholar 

  57. Regard M, Oelz O, Brugger P, Landis M (1989) Persistent cognitive impairment in climbers after repeated exposure to extreme altitude. Neurology 39:210–213

    Article  CAS  PubMed  Google Scholar 

  58. Hopkins RO, Woon FLM (2006) Neuroimaging, cognitive, and neurobehavioral outcomes following carbon monoxide poisoning. Behav Cognitive Neurosci Rev 5:141–155

    Article  Google Scholar 

  59. Kaw R, Hernandez AV, Walker E, Aboussouan L, Mohlesi B (2009) Determinants of hypercapnia in obese patients with obstructive sleep apnea: a systematic review and meta-analysis of cohort studies. CHEST 136:787–796

    PubMed  Google Scholar 

  60. Findley LJ, Barth JT, Powers DC, Wilhoit SC, Boyd DG et al (1986) Cognitive impairment in patients with obstructive sleep apnea and associated hypoxemia. Chest 90:686

    Article  CAS  PubMed  Google Scholar 

  61. Asano K, Takata Y, Usui Y, Shiina K, Hashimura Y et al (2009) New index for analysis of polysomnography, 'integrated area of desaturation', is associated with high cardiovascular risk in patients with mild to moderate obstructive sleep apnea. Respiration 78:278–284

    Article  PubMed  Google Scholar 

  62. Pepin JL, Delavie N, Pin I, Deschaux C, Argod J et al (2005) Pulse transit time improves detection of sleep respiratory events and microarousals in children. CHEST 127:722–730

    Article  PubMed  Google Scholar 

  63. Hultsch DF, Hertzog C, Small BJ, Dixon RA (1999) Use it or lose it: Engaged lifestyle as a buffer of cognitive decline in aging? Psychol Ageing 14:245–263

    Article  CAS  Google Scholar 

  64. Kramar AF, Erikson KI, Colcombe J (2006) Exercise, cognition, and the aging brain. J Appl Physiol 101:1237–1242

    Article  Google Scholar 

  65. Norbury R, Craig M, Cutter WJ, Whitehead M, Murphy D (2004) Oestrogen: brain ageing, cognition and neuropsychiatric disorder. Menopause Int 10

  66. Ayalon L, Ancoli-Israel S, Klemfuss Z, Shalauta MD, Drummond SPA (2006) Increased brain activation during verbal learning in obstructive sleep apnea. Neuroimage 31:1817–1825

    Article  PubMed  Google Scholar 

  67. Castronovo V, Canessa N, Ferini-Strambi L, Aloia MS, Consonni M et al (2009) Brain activation changes before and after PAP treatment in obstructive sleep apnea. Sleep 32:1161–1172

    PubMed Central  PubMed  Google Scholar 

  68. Incalzi RA, Marra C, Salvigni BL, Petrone A, Gemma A et al (2004) Does cognitive dysfunction conform to a distinctive pattern in obstructive sleep apnea syndrome? J Sleep Res 13:79–86

    Article  Google Scholar 

  69. Verstraeten E (2007) Neurocognitive effects of obstructive sleep apnea syndrome. Curr Neurol Neurosci Rep 7:161–166

    Article  PubMed  Google Scholar 

  70. Beebe DW (2006) Neurobehavioral effects of obstructive sleep apnea: an overview and heuristic model. Curr Opin Pulm Med 11:494–500

    Article  Google Scholar 

  71. Zimmerman ME, Aloia MS (2012) Sleep-disordered breathing and cognition in older adults. Curr Neurol Neurosci Rep 12:537–546

    Article  PubMed Central  PubMed  Google Scholar 

  72. Casseli RJ (2008) Obstructive sleep apnea, apolipoprotein E e4, and mild cognitive impairment. Sleep Med 9:816–817

    Article  Google Scholar 

  73. Lim DC, Pack AI (2013) Obstructive sleep apnea and cognitive impairment: Addressing the blood-brain barrier. Sleep Med Rev 18(1):35–48

  74. Kiralti PO, Demir AU, Volkan-Salanci B, Demir B, Sahin A (2010) Cerebral blood flow and cognitive function in obstructive sleep apnea syndrome. Hell J Nucl Med 13:138–143

    Google Scholar 

  75. Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A (2000) The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis. Cogn Psychol 41:49–100

    Article  CAS  PubMed  Google Scholar 

  76. Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment. Oxford University Press, New York

    Google Scholar 

  77. Fisk JE, Sharp CA (2004) Age-related impairment in executive functioning: Updating, inhibition, shifting, and access. J Clin Exp Neuropsychol 26:874–890

    Article  PubMed  Google Scholar 

  78. Nair D, Dayyat EA, Zhang SX, Wang Y, Gozal D (2011) Intermittent Hypoxia-Induced Cognitive Deficits Are Mediated by NADPH Oxidase Activity in a Murine Model of Sleep Apnea. PLoS One 6: Epub Ahead of Publication

  79. Guo Q, Yan W, Qing L, Min L, Huan W (2013) Levels of thioredoxin are related to the severity of obstructive sleep apnea: Based on oxidative stress concept. Sleep Breathing 17:311–316

    Article  PubMed  Google Scholar 

  80. Razi E, Akbari H (2006) A comparison of arterial oxygen saturation measured both by pulse oximeter and arterial blood gas analyzer in hypoxemic and non-hypoxemic pulmonary diseases. Turkish Repir J 7:43–47

    Google Scholar 

  81. Xie H, Yung W (2012) Chronic intermittent hypoxia-induced deficits in synaptic plasticity and neurocognitive functions: a role for brain-derived neurotrophic factor. Acta Pharmacol Sin 33:5–10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Disclosures

The authors were not provided with any financial support for this research.

Conflicts of interest

PE is a consultant and a member of the Medical Advisory Board for Apnex Medical Inc., and a member of the Medical and Industry Advisory Board, Sleep for Health and Safety Inc. DH is a consultant and a member of the Medical Advisory Board of Apnex Medical Inc., and conducts paid speaking engagements for Philips Respironics.

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Authors and Affiliations

  1. School of Psychology, University of Western Australia (M304), 35 Stirling Hwy Crawley, WA, 6009, Perth, Australia

    Michelle Olaithe & Romola S. Bucks

  2. School of Psychological and Clinical Sciences, Charles Darwin University, Darwin, Australia

    Timothy C. Skinner

  3. Centre for Sleep Science, School of Anatomy, Physiology & Human Biology, University of Western Australia, Perth, WA, Australia

    Peter E. Eastwood

  4. Western Australian Sleep Disorders Research Institute, Department of Pulmonary Physiology and Sleep Medicine, Queen Elizabeth II Medical Centre, Perth, WA, Australia

    David Hillman & Peter E. Eastwood

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  1. Michelle Olaithe
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  2. Timothy C. Skinner
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  3. David Hillman
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  4. Peter E. Eastwood
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  5. Romola S. Bucks
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Correspondence to Romola S. Bucks.

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Olaithe, M., Skinner, T.C., Hillman, D. et al. Cognition and nocturnal disturbance in OSA: the importance of accounting for age and premorbid intelligence. Sleep Breath 19, 221–230 (2015). https://doi.org/10.1007/s11325-014-1000-2

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  • DOI: https://doi.org/10.1007/s11325-014-1000-2

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