Effect of sleep-disordered breathing on stable electroencephalographic characteristics during night sleep in patients with arterial hypertension

Introduction. Obstructive sleep apnea (OSA) is the most common sleep-disordered breathing condition. A significant number of OSA patients often present with cardiovascular comorbidities, particularly arterial hypertension. OSA is associated with changes in bioelectrical activity of the brain, such as slowing of electroencephalographic activity in the cortex and reduced interhemispheric synchronization. These changes can become pathophysiological markers of sleep-disordered breathing.
Aim. To investigate the effect of sleep-disordered breathing on a range of quantitative electroencephalogram (EEG) characteristics during nighttime sleep in patients with arterial hypertension and clinically significant OSA.
Materials and methods. The material for this retrospective study consisted of 84 polysomnographic records of patients predominantly diagnosed with arterial hypertension. Patients were divided into three groups based on the apneahypopnea index (AHI). Polysomnographic records were used to assess the synchronization measure of brain electrical activity between occipital EEG leads. The synchronization measure was evaluated using a method based on wavelet bicoherence calculation.
Results. Statistically significant differences were observed in the low-frequency ranges Δf1-Δf4: 0.2-1.0 Hz, 0.8-1.6 Hz, 1.0-2.0 Hz, 1.0-4.0 Hz. In these frequencies, the interhemispheric synchronization measure significantly decreased with increasing severity of apnea.
Conclusion. To determine the severity of obstructive sleep apnea, a parameter based on the synchronization measure evaluated from symmetrical occipital EEG signals in the frequency ranges 0.2-1.0 Hz, 0.8-1.6 Hz, 1.0-2.0 Hz, and 1.0-4.0 Hz can be considered. This may serve as the basis for developing and implementing new diagnostic tools for assessing the severity of sleep-disordered breathing in practice.

1. Muromtseva G.A., Kontsevaya A.V., Konstantinov V.V., Artamonova G.V., Gatagonova T.M., Duplyakov D.V., Efanov A.Yu., Zhernakova Yu.V., Il’in V.A., Konradi A.O., Libis R.A., Minakov E.V., Nedogoda S.V., Oschepkova E.V., Romanchuk S.V., Rotar O.P., Trubacheva I.A., Deev A.D., Shalnova S.A., Chazova I.E., Shlyakhto E.V., Boytsov S.A., Balanova Yu.A., Gomyranova N.V., Evstifeeva S.E., Kapustina A.V., Litinskaya O.A., Mamedov M.N., Metelskaya V.A., Oganov R.G., Suvorova E.I., Khudyakov M.B., Baranova E.I., Kasimov R.A., Shabunova A.A., Ledyaeva A.A., Chumachek E.V., Azarin O.G., Babenko N.I., Bondartsov L.V., Furmenko G.I., Khvostikova A.E., Belova O.A., Nazarova O.A., Shutemova E.A., Barbarash O.L., Danilchenko Ya.V., Indukaeva E.V., Maksimov S.A., Mulerova T.A., Skripchenko A.E., Cherkass N.V., Basyrova I.R., Isaeva E.N., Kondratenko V.Yu., Lopina E.A., Safonova D.V., Gudkova S.A., Cherepanova N.A., Kaveshnikov V.S., Karpov R.S., Serebryakova V.N., Medvedeva I.V., Storozhok M.A., Shava V.P., Shalaev S.V., Gutnova S.K., Tolparov G.V. [The prevalence of non-infectious diseases risk factors in Russian population in 2012-2013 years. The results of ECVD-RF]. Cardiovascular Therapy and Prevention 2014; 13(6):4-11 (in Russian). https://doi.org/10.15829/1728-8800-2014-6-4-11

2. Pinto J.A., Ribeiro D.K., Cavallini A.F., Duarte C., Freitas G.S. Comorbidities associated with obstructive sleep apnea: a retrospective study. Int. Arch. Otorhinolaryngol. 2016; 20(2):145–150. https://doi.org/10.1055/s-0036-1579546

3. Muxfeldt E.S., Margallo V.S., Guimarães G.M., Salles G.F. Prevalence and associated factors of obstructive sleep apnea in patients with resistant hypertension. Am. J. Hypertens. 2014; 27(8):1069–1078. https://doi.org/10.1093/ajh/hpu023

4. Kobalava Zh.D., Konradi A.O., Nedogoda S.V., Shlyakhto E.V., Arutyunov G.P., Baranova E.I., Barbarash O.L., Boitsov S.A., Vavilova T.V., Villevalde S.V., Galyavich A.S., Glezer M.G., Grineva E.N., Grinstein Yu.I., Drapkina O.M., Zhernakova Yu.V., Zvartau N.E., Kislyak O.A., Koziolova N.A., Kosmacheva E.D., Kotovskaya Yu.V., Libis R.A., Lopatin Yu.M., Nebiridze D.V., Nedoshivin A.O., Ostroumova O.D., Oschepkova E.V., Ratova L.G., Skibitsky V.V., Tkacheva O.N., Chazova I.E., Chesnikova A.I., Chumakova G.A., Shalnova S.A., Shestakova M.V., Yakushin S.S., Yanishevsky S.N. [Arterial hypertension in adults. Clinical guidelines 2020]. Russian Journal of Cardiology 2020; 25(3): 149–218 (in Russian). https://doi.org/10.15829/1560-4071-2020-3-3786

5. Morisson F., Lavigne G., Petit D., Nielsen T., Malo J., Montplaisir J. Spectral analysis of wakefulness and REM sleep EEG in patients with sleep apnoea syndrome. Eur. Respir. J. 1998; 11(5):1135–1140. https://doi.org/10.1183/09031936.98.11051135

6. Morisson F., Décary A., Petit D., Lavigne G., Malo J., Montplaisir J. Daytime sleepiness and EEG Spectral analysis in apneic patients before and after treatment with continuous positive airway pressure. Chest 2001; 119(1):45–52. https://doi.org/10.1378/chest.119.1.45

7. Mathieu A., Mazza S., Petit D., Décary A., Massicotte-Marquez J., Malo J., Montplaisir J. Does age worsen EEG slowing and attention deficits in obstructive sleep apnea syndrome? Clin. Neurophysiol. 2007; 118(7):1538–1544. https://doi.org/10.1016/j.clinph.2007.04.009

8. Makarov V.V., Zhuravlev M.O., Runnova A.E., Protasov P., Maksimenko V.A., Frolov N.S., Pisarchik A.N., Hramov A.E. Betweenness centrality in multiplex brain network during mental task evaluation. Phys. Rev. E 2018; 98(6):062413. https://doi.org/10.1103/physreve.98.062413

9. Selskii A., Drapkina O., Agaltsov M., Posnenkova O., Simonyan M., Zhuravlev M. Runnova A. Adaptation of recurrence plot method to study a polysomnography: changes in EEG activity in obstructive sleep apnea syndrome. Eur. Phys. J. Spec. Top. 2023; 232:703–714. https://doi.org/10.1140/epjs/s11734-023-00814-8

10. Hu Q., Li M., Li Y. Single-channel EEG signal extraction based on DWT, CEEMDAN, and ICA method. Front. Hum. Neurosci. 2022; 16:1010760. https://doi.org/10.3389/fnhum.2022.1010760

11. Runnova A., Zhuravlev M., Orlova A., Agaltsov M., Drapkina O., Kiselev A. Structural abnormalities of brain electrical activity during night sleep in patients with obstructive apnoea syndrome. Eur. Phys. J. Spec. Top. 2023; 233:531– 542. https://doi.org/10.1140/epjs/s11734-023-01056-4

12. Selskii A.O., Egorov E.N., Ukolov R.V., Orlova A.A., Drozhdeva E.E., Mironov S.A., Doludin Yu.V., Agaltsov M.V., Drapkina O.M. Sleep-disordered breathing: statistical characteristics of joint recurrent indicators in ЕЕG activity. Russian Open Medical Journal 2023; 12(4):e0401. https://doi.org/10.15275/rusomj.2023.0401

13. Jalili M., Barzegaran E., Knyazeva M.G. Synchronization of EEG: Bivariate and Multivariate Measures. IEEE Trans. Neural Syst. Rehabil. Eng. 2014; 22(2):212–221. https://doi.org/10.1109/tnsre.2013.2289899

14. Knyazeva M.G., Carmeli C., Khadivi A., Ghika J., Meuli R., Frackowiak R.S. Evolution of source EEG synchronization in early Alzheimer's disease. Neurobiol. Aging 2013; 34(3):694–705. https://doi.org/10.1016/j.neurobiolaging.2012.07.012

15. Sakkalis V., Doru Giurcaneanu C., Xanthopoulos P., Zervakis M. E., Tsiaras V., Yang Y., Karakonstantaki E., Micheloyannis S. Assessment of linear and nonlinear synchronization measures for analysing EEG in a mild epileptic paradigm. IEEE Trans. Inf. Technol. Biomed. 2009; 13(4):433–441. https://doi.org/10.1109/titb.2008.923141

16. Moazami-Goudarzi M., Sarnthein J., Michels L., Moukhtieva R., Jeanmonod D. Enhanced frontal low and high frequency power and synchronization in the resting EEG of parkinsonian patients. NeuroImage 2008; 41(3):985–997. https://doi.org/10.1016/j.neuroimage.2008.03.032S

17. Khan S., Gramfort A., Shetty N.R., Kitzbichler M.G., Ganesan S., Moran J.M., Lee S.M., Gabrieli J.D.E., Tager- Flusberg H.B., Joseph R.M., Herbert M.R., Hämäläinen M.S., Kenet T. Local and long-range functional connectivity is reduced in concert in autism spectrum disorders. Proc. Nat. Acad. Sci. 2013; 110(8):3107–3112. https://doi.org/10.1073/pnas.1214533110

18. Zhuravlev M., Agaltsov M., Kiselev A., Simonyan M., Novikov M., Selskii A., Ukolov R., Drapkina O., Orlova A., Penzel T., Runnova A. Compensatory mechanisms of reduced interhemispheric EEG connectivity during sleep in patients with apnea. Sci. Rep. 2023;13(1):8444. https://doi.org/10.1038/s41598-023-35376-1

19. Rosenzweig I., Glasser M., Polsek D., Leschziner G.D., Williams S.C., Morrell M.J. Sleep apnoea and the brain: a complex relationship. Lancet Respir. Med. 2015; 3(5):404–414. https://doi.org/10.1016/S2213-2600(15)00090-9

20. Rostampour M., Noori K., Heidari M., Fadaei R., Tahmasian M., Khazaie H., Zarei M. White matter alterations in patients with obstructive sleep apnea: a systematic review of diffusion MRI studies. Sleep Med. 2020; 75:236–245. https://doi.org/10.1016/j.sleep.2020.06.024

21. Macey P.M., Kumar R., Woo M.A., Valladares E.M., Yan-Go F.L., Harper R.M. Brain structural changes in obstructive sleep apnea. Sleep 2008; 31(7):967–977. PMID: 18652092; PMCID: PMC2491498.