Abstract
Introduction
Sleep spindles play a key role in sleep-mediated cognitive processes. Cognitive functions are well-known to be affected in obstructive sleep apnea (OSA). Here, we analyzed attention and executive functions in patients with OSA and investigated the relationship between sleep spindles and cognitive abilities.
Methods
Sixty patients with OSA (18–65 years, 19 females and 41 males) and a control group (n = 41) including age-and sex-matched healthy individuals were consecutively and prospectively enrolled. All participants had a full-night polysomnography, and sleep spindles were analyzed using a semi-automated program. For the evaluation of short-term memory, attention and executive functions, Stroop test, forward and backward digit span tests were applied to all participants upon awakening following polysomnography.
Results
Scores of forward and backward digit span and Stroop tests were worse in OSA patients in compared to those in controls. Mean density of sleep spindles was decreased in OSA patients than those in controls (p = 0.044). A positive correlation was found between fast sleep spindle frequency and forward digit span (r = 2.222; p = 0.038) and backward digit span test scores (r = 2,157; p = 0.042) in OSA patients. In patients with moderate to severe OSA, sleep spindle density was positively correlated with forward (r = 2.323, p = 0.029) and backward (r = 2.500, p = 0.016) DSTs, and the duration of sleep spindles had positive correlation with backward DST (r = 2.452, p = 0.010).
Conclusion
Our findings demonstrated that the disturbances in sleep spindle characteristics in OSA are associated with the cognitive impairments in attention, short-term memory, and executive functions, especially in patients with moderate to severe OSA.
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Data availability
The data supporting this study's findings are available from the corresponding author upon reasonable request.
References
American Academy of Sleep Medicine (2014) The international classification of sleep disorders ({ICSD}-3). American Academy of Sleep Medicine
Carvalho DZ, Gerhardt GJ, Dellagustin G, de Santa-Helena EL, Lemke N, Segal AZ, Schönwald SV (2014) Loss of sleep spindle frequency deceleration in Obstructive Sleep Apnea. Clin Neurophysiol 125(2):306–312. https://doi.org/10.1016/j.clinph.2013.07.005
Lanfranco F, Gianotti L, Maccario M (2003) Endocrine and metabolic alterations in obstructive sleep apnea syndrome. J Endocrinol Invest 26(6):491–492. https://doi.org/10.1007/BF03345208
Hopps E, Caimi G (2015) Obstructive sleep apnea syndrome: links betwen pathophysiology and cardiovascular complications. Clin Invest Med 38(6):E362–E370. https://doi.org/10.25011/cim.v38i6.26199
Leng Y, McEvoy CT, Allen IE, Yaffe K (2017) Association of sleep-disordered breathing with cognitive function and risk of cognitive impairment: a systematic review and meta-analysis. JAMA Neurol 74(10):1237–1245. https://doi.org/10.1001/jamaneurol.2017.2180
Seda G, Han TS (2020) Effect of obstructive sleep apnea on neurocognitive performance. Sleep Med Clin 15(1):77–85. https://doi.org/10.1016/j.jsmc.2019.10.001
De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7(5):423–440. https://doi.org/10.1053/smrv.2002.0252
Guadagni V, Byles H, Tyndall AV, Parboosingh J, Longman RS, Hogan DB, Hanly PJ, Younes M, Poulin MJ (2021) Association of sleep spindle characteristics with executive functioning in healthy sedentary middle-aged and older adults. J Sleep Res 30(2):e13037. https://doi.org/10.1111/jsr.13037
Schabus M, Hödlmoser K, Gruber G, Sauter C, Anderer P, Klösch G, Parapatics S, Saletu B, Klimesch W, Zeitlhofer J (2006) Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur J Neurosci 23(7):1738–1746. https://doi.org/10.1111/j.1460-9568.2006.04694.x
Mohammadi H, Aarabi A, Rezaei M, Khazaie H, Brand S (2021) Sleep spindle characteristics in obstructive sleep apnea syndrome (OSAS). Front Neurol 12:598632. https://doi.org/10.3389/fneur.2021.598632
Schönwald SV, Carvalho DZ, de Santa-Helena EL, Lemke N, Gerhardt GJ (2012) Topography-specific spindle frequency changes in obstructive sleep apnea. BMC Neurosci 13:89. https://doi.org/10.1186/1471-2202-13-89
Li W, Duan Y, Yan J, Gao H, Li X (2020) Association between loss of sleep-specific waves and age, sleep efficiency, body mass index, and apnea-hypopnea index in human N3 sleep. Aging Dis 11(1):73–81. https://doi.org/10.14336/AD.2019.0420
Mullins AE, Kim JW, Wong KKH, Bartlett DJ, Vakulin A, Dijk DJ, Marshall NS, Grunstein RR, D’Rozario AL (2021) Sleep EEG microstructure is associated with neurobehavioural impairment after extended wakefulness in obstructive sleep apnea. Sleep Breath 25(1):347–354. https://doi.org/10.1007/s11325-020-02066-5
Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–662
Ryan JJ, Lopez SJ, Paolo AM (1996) Digit span performance of persons 75–96 years of age: base rates and associations with selected demographic variables. Psychol Assess 8(3):324–327
Berry RB, Quan SF, Abreu AR (2020) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications version 2.6. American Academy of Sleep Medicine, Darien
D’Rozario AL, Hoyos CM, Wong K, Unger G, Kim JW, Vakulin A, Kao CH, Naismith SL, Bartlett DJ, Grunstein RR (2022) Improvements in cognitive function and quantitative sleep electroencephalogram in obstructive sleep apnea after six months of continuous positive airway pressure treatment. Sleep 45(6):zsac013. https://doi.org/10.1093/sleep/zsac013
Lustenberger C, Wehrle F, Tüshaus L, Achermann P, Huber R (2015) The multidimensional aspects of sleep spindles and their relationship to word-pair memory consolidation. Sleep 38(7):1093–1103. https://doi.org/10.5665/sleep.4820
Attier-Zmudka J, Sérot JM, Valluy J, Saffarini M, Douadi Y, Malinowski KP, Balédent O (2020) Sleep apnea syndrome in an elderly population admitted to a geriatric unit: prevalence and effect on cognitive function. Front Aging Neurosci 11:361. https://doi.org/10.3389/fnagi.2019.00361
D’Rozario AL, Field CJ, Hoyos CM, Naismith SL, Dungan GC, Wong K, Grunstein RR, Bartlett DJ (2018) Impaired neurobehavioural performance in untreated obstructive sleep apnea patients using a novel standardised test battery. Front Surg 5:35. https://doi.org/10.3389/fsurg.2018.00035
Li Q, Li NZ, Li TT, Sun YQ, Wang J, Chen R (2019) Zhonghua jie he he hu xi za zhi = Zhonghua jiehe he huxi zazhi. Chin J Tuberc Respir Dis 42(6):419–425. https://doi.org/10.3760/cma.j.issn.1001-0939.2019.06.004
Bawden FC, Oliveira CA, Caramelli P (2011) Impact of obstructive sleep apnea on cognitive performance. Arq Neuropsiquiatr 69(4):585–589. https://doi.org/10.1590/s0004-282x2011000500003
Van der Elst W, Van Boxtel MP, Van Breukelen GJ, Jolles J (2006) The Stroop color-word test: influence of age, sex, and education; and normative data for a large sample across the adult age range. Assessment 13(1):62–79. https://doi.org/10.1177/1073191105283427
Chen HD, Wang J, Wang XS, Yao XB, Wu XF, Wu JL, Huang GP (2020) Relationship between cognitive impairment and sleep-related respiratory indexes in patients with obstructive sleep apnea. Zhonghua Yi Xue Za Zhi 100(37):2929–2933. https://doi.org/10.3760/cma.j.cn112137-20200224-00435
Djonlagic I, Mariani S, Fitzpatrick AL, Van Der Klei VMGTH, Johnson DA, Wood AC, Seeman T, Nguyen HT, Prerau MJ, Luchsinger JA, Dzierzewski JM, Rapp SR, Tranah GJ, Yaffe K, Burdick KE, Stone KL, Redline S, Purcell SM (2021) Macro and micro sleep architecture and cognitive performance in older adults. Nat Hum Behav 5(1):123–145. https://doi.org/10.1038/s41562-020-00964-y
Gildner TE, Liebert MA, Kowal P, Chatterji S, Snodgrass JJ (2014) Associations between sleep duration, sleep quality, and cognitive test performance among older adults from six middle income countries: results from the Study on Global Ageing and Adult Health (SAGE). J Clin Sleep Med 10(6):613–621. https://doi.org/10.5664/jcsm.3782
Parker JL, Appleton SL, Melaku YA, Stevens D, Wittert GA, Martin S, Adams RJ, Vakulin A (2021) Sleep macroarchitecture but not obstructive sleep apnea is independently associated with cognitive function in only older men of a population-based cohort. J Sleep Res 30(6):e13370. https://doi.org/10.1111/jsr.13370
Ondze B, Espa F, Dauvilliers Y, Billiard M, Besset A (2003) Sleep architecture, slow wave activity and sleep spindles in mild sleep disordered breathing. Clin Neurophysiol 114(5):867–874. https://doi.org/10.1016/s1388-2457(02)00389-9
Purcell SM, Manoach DS, Demanuele C, Cade BE, Mariani S, Cox R, Panagiotaropoulou G, Saxena R, Pan JQ, Smoller JW, Redline S, Stickgold R (2017) Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat Commun 8:15930. https://doi.org/10.1038/ncomms15930
Himanen SL, Virkkala J, Huhtala H, Hasan J (2002) Spindle frequencies in sleep EEG show U-shape within first four NREM sleep episodes. J Sleep Res 11(1):35–42. https://doi.org/10.1046/j.1365-2869.2002.00273.x
Himanen SL, Virkkala J, Huupponen E, Hasan J (2003) Spindle frequency remains slow in sleep apnea patients throughout the night. Sleep Med 4(3):229–234. https://doi.org/10.1016/s1389-9457(02)00239-3
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All authors contributed to the conception and design of the study. Data preparation: E.K.K.; Statistical analysis: G.B.S; Article writing: E.K.K., G.B.S., D.K.; Editing and revising: G.B.S. All authors contributed to and approved the final manuscript.
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Kizilkilic, E.K., Karadeniz, D. & Senel, G.B. Attention and executive function impairments in obstructive sleep apnea are associated with decreased sleep spindles. Acta Neurol Belg (2024). https://doi.org/10.1007/s13760-024-02534-9
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DOI: https://doi.org/10.1007/s13760-024-02534-9