Molecular circadian markers in acute ischemic stroke (preliminary results)
https://doi.org/10.18705/1607-419X-2024-2442
EDN: QEKFWO
Abstract
Background. Ischemic stroke is the leading cause of mortality and loss of working ability. Sleep disorders and sleep-wake rhythm disorders are considered to be a potential modifiable risk factor of acute stroke. Objective. To determine the peculiarities of circadian rhythms in acute stroke by assessing the daily variation of urinary excretion of cortisol and 6-sulfatoxymelatonin. Materials and methods. We examined 27 patients with acute ischemic stroke and 9 patients admitted to the hospital with suspected but not confirmed stroke. All examinations in both groups were performed in similar settings. All patients underwent neurological assessment in acute phase and before discharge including evaluation by National Institute of Health Stroke Scale, modified Rankin scale (mRs), Barthel index and Rivermead index. Within 48–72 hours after admission, urine samples were collected at 7 a. m., 3 p. m. and 11 p. m. for cortisol and 6-sulfatoxymelatonin assessment (enzyme-linked immunosorbent assay analysis). Results. Daily urinary cortisol excretion did not differ in stroke and control subjects. However, stroke patients demonstrated the highest values in the evening while control subjects had higher levels in the morning. The rhythm of urinary 6-sulfatoxymelatonin excretion is preserved in both groups with the highest level in the morning. However, stroke patients show lower levels at all time points (by 45 %, 33 % and 72 % in the morning, afternoon and evening, respectively). There were no changes in either cortisol or 6-sulfatoxymelatonin excretion depending on stroke severity. Afternoon excretion of 6-sulfatoxymelatonin correlates with Barthel index at discharge (ρ = 0,63; p = 0,004), mRs score at discharge (ρ = –0,65; p = 0,003) and Rivermead index at admission (ρ = 0,52; p = 0,024) and at discharge (ρ = 0,49; p = 0,032). Conclusion. Patients with acute mild-moderate stroke show abnormal daily rhythm of urinary cortisol excretion with the maximum in the evening. The daily rhythm of 6-sulfatoxymelatonin excretion is preserved with the maximum excretion at night, but stroke patients have lower levels compared to control subjects.
Keywords
About the Authors
L. S. KorostovtsevaRussian Federation
Lyudmila S. Korostovtseva, MD, PhD, Senior Researcher, Somnology Group, Research Department of Arterial Hypertension
2 Akkuratov street, St Petersburg, 197341
Phone: 8(812)702–37–33
E. N. Zabroda
Russian Federation
Ekaterina N. Zabroda, Laboratory Assistant, Somnology Group, Research Department of Arterial Hypertension; Student
St Petersburg
S. N. Kolomeychuk
Russian Federation
Sergey N. Kolomeichuk, PhD, Senior Research Associate, Laboratory of Genetics Institute of Biology; Researcher, Sleep Laboratory, Research Department for Hypertension
Petrozavodsk
St Petersburg
A. D. Gordeev
Russian Federation
Alexey L. Gordeev, Laboratory Assistant, Somnology Group, Research Department of Arterial Hypertension; Student
St Petersburg
V. V. Amelina
Russian Federation
Valeria V. Amelina, PhD in Psychology, Senior lecturer; Junior Researcher, Somnology Group, Research Department of Arterial Hypertension
St Petersburg
E. A. Stabrova
Russian Federation
Elena A. Stabrova, MD, Clinical Laboratory Diagnostics Doctor, Central Clinical and Diagnostic Laboratory
St Petersburg
E. Y. Vasilieva
Russian Federation
Elena Y. Vasilieva, MD, PhD, Clinical Laboratory Diagnostics Doctor, Head, Central Clinical and Diagnostic Laboratory
St Petersburg
M. V. Bochkarev
Russian Federation
Mikhail V. Bochkarev, MD, PhD, Researcher, Research Group of Hypersomnias and Sleep-Disordered Breathing Group, World Class Research Centre for Personalized Medicine
St Petersburg
Y. V. Sviryaev
Russian Federation
Yurii V. Sviryaev, MD, PhD, DSc, Head, Research Group of Hypersomnias and Sleep-Disordered Breathing Group, World Class Research Centre for Personalized Medicine; Leading Researcher, Head, Somnology Group, Research Department of Arterial Hypertension
St Petersburg
References
1. Lloyd-Jones DM, Allen NB, Anderson CAM, Black T, Brewer LC, Foraker RE et al. Life’s Essential 8: updating and enhancing the American Heart Association’s construct of cardiovascular health: a presidential advisory from the American Heart Association. Circulation. 2022;146(5):e18–43. doi:10.1161/CIR.0000000000001078
2. 2021 ESC Guidelines on cardiovascular disease prevention in clinical practice Developed by the Task Force for cardiovascular disease prevention in clinical practice with representatives of the European Society of. Eur Heart J. 2021;42(34):3227–337. doi:10.1093/eurheartj/ehab484
3. Charchar FJ, Prestes PR, Mills C, Mooi S, Neupane D, Marques FZ et al. Lifestyle management of hypertension: International the World Hypertension League and European Society of Hypertension Table of Contents. J Hypertens. 2024;42(1):23–49. doi:10.1097/HJH.0000000000003563
4. Mancia G, Kreutz R, Burnier M, Grassi G, Januszewicz A, Lorenza M et al. 2023 ESH Guidelines for the management of arterial hypertension. The Task Force for the management of arterial hypertension of the European Society of Hypertension Endorsed by the International Society of Hypertension (ISH) and the European Renal Association. J Hypertens. 2023;41(12):1874–2071. doi:10.1097/HJH.0000000000003563
5. Bassetti CLA, Randerath W, Vignatelli L, Ferini-Stpambi L, Brill A, Bonsignore MR. EAN / ERS / ESO / ESRS statement on the impact of sleep disorders on risk and outcome of stroke. Eur Respir J. 2020;55(4):1901104. doi:10.1183/13993003.01104-2019
6. Yoshizaki T, Ishihara J, Kotemori A, Kokubo Y, Saito I. Association between irregular daily routine and risk of incident stroke and coronary heart disease in a large Japanese population. Sci Rep. 2022;12:1–10. doi:10.1038/s41598-022-20019-8
7. Korostovtseva LS, Kolomeichuk SN. Circadian factors in stroke: a clinician’s perspective. Cardiol Ther. 2023;12(2):275–95. doi:10.1007/s40119-023-00313-w
8. Gottlieb E, Churilov L, Werden E, Churchward T, Pase MP, Egorova N et al. Sleep-wake parameters can be detected in patients with chronic stroke using a multisensor accelerometer: A validation study. Journal of Clinical Sleep Medicine. 2021;17(2):167–75.
9. Gebruers N, Truijen S, Engelborghs S, Nagels G, Brouns R, De Deyn P. Actigraphic measurement of motor deficits in acute ischemic stroke. Cerebrovascular Diseases. 2008;26:533–40.
10. Takekawa H, Miyamoto M, Miyamoto T, Yokota N, Hirata K. Alteration of circadian periodicity in core body temperatures of patients with acute stroke. Psychiatry and Clinical Neurosciences. 2002;56(3):221–2.
11. Ischemic stroke and transient ischemic attack in adults. Clinical guidelines. 2022;1–215. In Russian
12. Kwah L, Diong J. National Institutes of Health Stroke Scale (NIHSS). J Physiother. 2014;60(1):61.
13. Mahoney R, Barthel D. Functional evaluation: the Barthel Index. Md Sate Mod J. 1965;14:61–5.
14. Rankin J. Cerebral vascular accidents in patients over te age of 60. Scott Med J. 1957;2:200–15.
15. Collen FM, Wade DT, Robb GF, Bradshaw CM. The Rivermead Mobility index: A further development of the rivermead motor assessment. Disability and rehabilitation. 1991;13(2):50–4.
16. Adams H, Bendixen B, Kappelle L, Biller J, Love B, Gordon D et al. Classification of subtype of acute ischemic stroke definitions for use in a multicenter clinical trial. Stroke. 1993;24(1):35–41.
17. Kovalzon VM. Neurobiology of wakefulness and sleep. M.: LENAND, 2024. 416 p. In Russian
18. Kryger M, Roth T, Dement WC. Principles and Practice of Sleep Medicine. In: Kryger M, Roth T, editors. 6th ed. 2017. 1778 р.
19. Moon C, Benson CJ, Albashayreh A, Perkhounkova Y, Burgess HJ. Sleep, circadian rhythm characteristics, and melatonin levels in later life adults with and without coronary artery disease. J Clin Sleep Med. 2023;19(2):283–92. doi:10.5664/jcsm.10308
20. Zhanina MY, Druzhkova TA, Yakovlev AA, Vladimirova EE, Freiman S V, Eremina NN et al. Development of poststroke cognitive and depressive disturbances: associations with neurohumoral indices. Curr Issues Mol Biol. 2022;44:6290–305. doi:10.3390/cimb44120429
21. Murros K, Fogelholm R, Kettunen S, Vuorela AL. Serum cortisol and outcome of ischemic brain infarction. Journal of the Neurological Sciences. 1993;116(1):12–7.
22. Barugh AJ, Gray P, Shenkin SD, MacLullich AMJ, Mead GE. Cortisol levels and the severity and outcomes of acute stroke: A systematic review. J Neurol. 2014;261(3):533–45. doi:10.1007/s00415-013-7231-5
23. Olsson T, Marklund N, Gustafson Y, Nasman B. Abnormalities at different levels of the hypothalamic-pituitary-adrenocortical axis early after stroke. Stroke. 1992;23(11):1573–6.
24. Anne M, Juha K, Makikallio T, Mikko T, Olli V, Kyosti S et al. Neurohormonal activation in ischemic stroke: effects of acute phase disturbances on long-term mortality. Curr Neurovasc Resh. 2007;4(3):170–5.
25. Kario K, Pickering TG, Matsuo T, Hoshide S, Schwartz JE, Shimada K. Stroke prognosis and abnormal nocturnal blood pressure falls in older hypertensives. Hypertension. 2001;38(4):852–7.
26. Schwarz S, Schwab S, Klinga K, Bettendorf M. Neuroendocrine changes in patients with acute space occupying ischaemic stroke. J Neurol Neurosurg Psychiatry. 2003;74:725–7.
27. Johansson Ê, Ahren B, Nasman B, Carlstrom K, Olsson T. Cortisol axis abnormalities early after stroke — relationships to cytokines and leptin. J Intern Med. 2000;247(2):179–87.
28. Szczudlik A, Dziedzic T, Bartus S, Slowik A, Kieltyka A. Serum interleukin-6 predicts cortisol release in acute stroke patients. J Endocrinol Invest. 2004;27(1):37–41.
29. Atanassova PA, Terzieva DD, Dimitrov BD. Impaired nocturnal melatonin in acute phase of ischaemic stroke: Cross-sectional matched case-control analysis. J Neuroendocrinol. 2009;21(7):657–63.
30. Ritzenthaler T, Nighoghossian N, Berthiller J, Schott AM, Cho TH, Derex L et al. Nocturnal urine melatonin and 6-sulphatoxymelatonin excretion at the acute stage of ischaemic stroke. J Pineal Res. 2009;46(3):349–52. doi: 10.1111/j.1600-079X.2009.00670.x
31. Kulesh AA, Lapaeva TV, Shestakov VV. Chronobiological characteristics of stroke and poststroke cognitive impairment. S. S. Korsakov Journal of Neurology and Psychiatry. 2014;114(11):32–35. In Russian.
32. Beloosesky Y, Grinblat J, Laudon M, Grosman B, Streifler JY, Zisapel N. Melatonin rhythms in stroke patients. Neurosci Letters. 2002;319(2):103–6.
33. Yu S-Y, Sun Q, Chen S, Wang F, Chen R, Chen J et al. Circadian rhythm disturbance in acute ischemic stroke patients and its effect on prognosis. Cerebrovasc Dis. 2024;53(1):14–27. doi:10.1159/000528724
34. Meng H, Liu T, Borjigin J, Wang MM. Ischemic stroke destabilizes circadian rhythms. J Circ Rhythms. 2008;6:1–13. doi:10.1186/1740-3391-6-9
35. Adamczak-Ratajczak A, Kupsz J, Owecki M, Zielonka D, Sowinska A, Checinska-Maciejewska Z et al. Circadian rhythms of melatonin and cortisol in manifest huntington’s disease and in acute cortical ischemic stroke. J Physiol Pharmacol. 2017;68(4):539–46.
36. Lorente L, Martín MM, Abreu-González P, Pérez-Cejas A, Ramos L, Argueso M et al. Serum melatonin levels are associated with mortality in patients with malignant middle cerebral artery infarction. J Intern Med Res. 2018;46(8):3268–77. doi:10.1177/0300060518775008
Supplementary files
Review
For citations:
Korostovtseva L.S., Zabroda E.N., Kolomeychuk S.N., Gordeev A.D., Amelina V.V., Stabrova E.A., Vasilieva E.Y., Bochkarev M.V., Sviryaev Y.V. Molecular circadian markers in acute ischemic stroke (preliminary results). "Arterial’naya Gipertenziya" ("Arterial Hypertension"). 2024;30(3):282-291. (In Russ.) https://doi.org/10.18705/1607-419X-2024-2442. EDN: QEKFWO