Cyclic alternating pattern in obstructive sleep apnea: A preliminary study.
arousals
cyclic alternating pattern
obstructive sleep apnea
sleep
Journal
Journal of sleep research
ISSN: 1365-2869
Titre abrégé: J Sleep Res
Pays: England
ID NLM: 9214441
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
revised:
10
03
2021
received:
07
01
2021
accepted:
18
03
2021
pubmed:
4
5
2021
medline:
15
12
2021
entrez:
3
5
2021
Statut:
ppublish
Résumé
Obstructive sleep apnea is linked to cardiovascular disease, metabolic disorders and dementia. The precise nature of the association between respiratory events in obstructive sleep apnea, cortical or subcortical arousals, and cognitive, autonomic and oxidative stress consequences remains incompletely elucidated. Previous studies have aimed to understand the relationship between obstructive sleep apnea and arousal patterns, as defined by the cyclic alternating pattern, but results have been inconsistent, in part likely due to the presence of associated comorbidities. To better define this relationship, we analysed cyclic alternating patterns in patients with obstructive sleep apnea without any additional comorbidities. We identified 18 adult male, non-obese subjects with obstructive sleep apnea and no other comorbidities or medication history, who underwent whole-night electroencephalography and polysomnography. Cyclic alternating pattern analysis was performed and verified by certified somnologists. Pairwise linear regression analysis demonstrated an inverse relationship between obstructive sleep apnea severity and cyclic alternating pattern subtype A1, and a direct correlation with cyclic alternating pattern subtype A3. Cyclic alternating pattern subtypes A1 prevail in milder obstructive sleep apnea phenotype, whilst cyclic alternating pattern subtypes A2 and A3 overcome among moderate-to-severe obstructive sleep apnea patients. The milder obstructive sleep apnea group also presented higher sleep efficiency, and increased percentages of non-rapid eye movement stage 3 and rapid eye movement sleep, as well as longer cyclic alternating pattern sequences in N3, while severe obstructive sleep apnea patients spent more time in lighter sleep stages. These results imply/suggest a balance between cyclic alternating pattern's adaptive and maladaptive arousal processes in obstructive sleep apnea of differing severities. In milder obstructive sleep apnea (apnea-hypopnea index < 20), sleep continuity may be reinforced by cyclic alternating pattern subtype A1, whereas in more severe obstructive sleep apnea, decompensation of these sleep-stabilizing mechanisms may occur and more intrusive cyclic alternating pattern fluctuations disrupt sleep circuitry.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13350Subventions
Organisme : Wellcome Trust
ID : 103952/Z/14/Z
Pays : United Kingdom
Informations de copyright
© 2021 The Authors. Journal of Sleep Research published by John Wiley & Sons Ltd on behalf of European Sleep Research Society.
Références
American Academy of Sleep Medicine. The International Classification of Sleep Disorders - Third Edition (ICSD-3). : American Academy of Sleep Medicine, 2014.
Anaclet, C., Ferrari, L., Arrigoni, E., Bass, C. E., Saper, C. B., Lu, J., & Fuller, P. M. (2014). The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nature Neuroscience, 17, 1217-1224. https://doi.org/10.1038/nn.3789
Berry, R. B., Brooks, R., Gamaldo, C., Harding, S. M., Lloyd, R. M., Quan, S. F., … Vaughn, B. V. (2017). AASM Scoring Manual Updates for 2017 (Version 2.4). Journal of Clinical Sleep Medicine, 13, 665-666. https://doi.org/10.5664/jcsm.6576
Bosi, M., Milioli, G., Riccardi, S., Melpignano, A., Vaudano, A. E., Cortelli, P., … Parrino, L. (2018). Arousal responses to respiratory events during sleep: The role of pulse wave amplitude. Journal of Sleep Research, 27, 259-267. https://doi.org/10.1111/jsr.12593
Boutin, R. C., Alsahafi, Z., & Pagliardini, S. (2017). Cholinergic modulation of the parafacial respiratory group. Journal of Physiology, 595, 1377-1392. https://doi.org/10.1113/JP273012
Bucks, R. S., Olaithe, M., Rosenzweig, I., & Morrell, M. J. (2017). Reviewing the relationship between OSA and cognition: Where do we go from here? Respirology, 22, 1253-1261. https://doi.org/10.1111/resp.13140
Clinical.Trials.Gov. (2020). Investigating the Neuropathology of Obstructive Sleep Apnoea (INcOSA). In. NCT02967536
Emamian, F., Khazaie, H., Tahmasian, M., Leschziner, G. D., Morrell, M. J., Hsiung, G.-Y., … Sepehry, A. A. (2016). The association between obstructive sleep apnea and alzheimer's disease: a meta-analysis perspective. Frontiers in Aging Neuroscience, 8, 78. https://doi.org/10.3389/fnagi.2016.00078
Gleeson, K., Zwillich, C. W., & White, D. P. (1990). The influence of increasing ventilatory effort on arousal from sleep. American Review of Respiratory Disease, 142, 295-300. https://doi.org/10.1164/ajrccm/142.2.295
Grady, F., Peltekian, L., Iverson, G., & Geerling, J. C. (2020). Direct Parabrachial-Cortical Connectivity. Cerebral Cortex, 30, 4811-4833. https://doi.org/10.1093/cercor/bhaa072
Jackson, M. L., Cavuoto, M., Schembri, R., Doré, V., Villemagne, V. L., Barnes, M., … Robinson, S. R. (2020). Severe obstructive sleep apnea is associated with higher brain amyloid burden: A preliminary PET imaging study. Journal of Alzheimer's Disease, 78, 611-617. https://doi.org/10.3233/JAD-200571
Kaur, S., Pedersen, N. P., Yokota, S., Hur, E. E., Fuller, P. M., Lazarus, M., … Saper, C. B. (2013). Glutamatergic signaling from the parabrachial nucleus plays a critical role in hypercapnic arousal. Journal of Neuroscience, 33, 7627-7640. https://doi.org/10.1523/JNEUROSCI.0173-13.2013
Kaur, S., & Saper, C. B. (2019). Neural circuitry underlying waking up to hypercapnia. Front Neurosci, 13, 401. https://doi.org/10.3389/fnins.2019.00401
Korkmaz, S., Bilecenoglu, N. T., Aksu, M., & Yoldas, T. K. (2018). Cyclic alternating pattern in obstructive sleep apnea patients with versus without excessive sleepiness. Sleep Disord, 2018, 8713409. https://doi.org/10.1155/2018/8713409
Malhotra, A., Mesarwi, O., Pepin, J. L., & Owens, R. L. (2020). Endotypes and phenotypes in obstructive sleep apnea. Current Opinion in Pulmonary Medicine, 26, 609-614. https://doi.org/10.1097/MCP.0000000000000724
Milioli, G., Bosi, M., Grassi, A., Riccardi, S., Terzano, M. G., Cortelli, P., … Parrino, L. (2015). Can sleep microstructure improve diagnosis of OSAS? Integrative information from CAP parameters. Archives Italiennes De Biologie, 153, 194-203.
Parrino, L., Ferri, R., Bruni, O., & Terzano, M. G. (2012). Cyclic alternating pattern (CAP): The marker of sleep instability. Sleep Medicine Reviews, 16, 27-45. https://doi.org/10.1016/j.smrv.2011.02.003
Polsek, D., Cash, D., Veronese, M., Ilic, K., Wood, T. C., Milosevic, M., … Rosenzweig, I. (2020). The innate immune toll-like-receptor-2 modulates the depressogenic and anorexiolytic neuroinflammatory response in obstructive sleep apnoea. Scientific Reports, 10, 11475. https://doi.org/10.1038/s41598-020-68299-2
Rosenzweig, I., Glasser, M., Crum, W. R., Kempton, M. J., Milosevic, M., McMillan, A., … Morrell, M. J. (2016). Changes in neurocognitive architecture in patients with obstructive sleep apnea treated with continuous positive airway pressure. EBioMedicine, 7, 221-229. https://doi.org/10.1016/j.ebiom.2016.03.020
Rosenzweig, I., Glasser, M., Polsek, D., Leschziner, G. D., Williams, S. C., & Morrell, M. J. (2015). Sleep apnoea and the brain: A complex relationship. The Lancet Respiratory Medicine, 3, 404-414. https://doi.org/10.1016/S2213-2600(15)00090-9
Rosenzweig, I., Williams, S. C., & Morrell, M. J. (2014). The impact of sleep and hypoxia on the brain: Potential mechanisms for the effects of obstructive sleep apnea. Current Opinion in Pulmonary Medicine, 20, 565-571. https://doi.org/10.1097/MCP.0000000000000099
Satpute, A. B., Kragel, P. A., Barrett, L. F., Wager, T. D., & Bianciardi, M. (2019). Deconstructing arousal into wakeful, autonomic and affective varieties. Neuroscience Letters, 693, 19-28. https://doi.org/10.1016/j.neulet.2018.01.042
Terzano, M. G., Parrino, L., Boselli, M., Spaggiari, M. C., & Di Giovanni, G. (1996). Polysomnographic analysis of arousal responses in obstructive sleep apnea syndrome by means of the cyclic alternating pattern. Journal of Clinical Neurophysiology, 13, 145-155. https://doi.org/10.1097/00004691-199603000-00005
Terzano, M. G., Parrino, L., Smerieri, A., Carli, F., Nobili, L., Donadio, S., & Ferrillo, F. (2005). CAP and arousals are involved in the homeostatic and ultradian sleep processes. Journal of Sleep Research, 14, 359-368. https://doi.org/10.1111/j.1365-2869.2005.00479.x
Terzano, M. G., Parrino, L., Smerieri, A., Chervin, R., Chokroverty, S., Guilleminault, C., … Walters, A. (2002). Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. Sleep Medicine, 3, 187-199. https://doi.org/10.1016/S1389-9457(02)00003-5
Thomas, R. J. (2003). Arousals in sleep-disordered breathing: Patterns and implications. Sleep, 26, 1042-1047. https://doi.org/10.1093/sleep/26.8.1042
White, D. P. (2017). Advanced concepts in the pathophysiology of obstructive sleep apnea. Advances in Oto-Rhino-Laryngology, 80, 7-16.
Yokota, S., Kaur, S., Vanderhorst, V. G., Saper, C. B., & Chamberlin, N. L. (2015). Respiratory-related outputs of glutamatergic, hypercapnia-responsive parabrachial neurons in mice. The Journal of Comparative Neurology, 523, 907-920. https://doi.org/10.1002/cne.23720