medsovetМедицинский СоветMeditsinskiy sovet = Medical Council2079-701X2658-5790REMEDIUM GROUP Ltd.10.21518/2079-701X-2022-16-23-50-59medsovet-7294Research ArticleНЕВРОЛОГИЯNEUROLOGYЗакономерности и особенности течения раннего и позднего этапов восстановительного периода после ишемического инсульта, развившегося на фоне COVID-19Patterns and features of the course of the early and late stages recovery period after ischemic stroke associated with COVID-19https://orcid.org/0000-0002-7941-2010КабаеваЕ. Н.KabaevaE. N.

Кабаева Екатерина Николаевна – кандидат медицинских наук, доцент кафедры нервных болезней и нейрохирургии имени проф. Ю.С. Мартынова.

117198, Москва, ул. Миклухо-Маклая, д. 6

Ekaterina N. Kabaeva - Cand. Sci. (Med.), Associate Professor of the Department of Nervous Diseases and Neurosurgery named after Prof. Yu.S. Martynov, Peoples’ Friendship University of Russia.

6, Miklukho-Maklai St., Moscow, 117198

katkab@list.ruhttps://orcid.org/0000-0001-5758-8552ЕршовА. В.ErshovA. V.

Ершов Антон Валерьевич - доктор медицинских наук, профессор кафедры патофизиологии Института биодизайна и моделирования сложных систем, ПМГМУ им. И.М. Сеченова (Сеченовский Университет); ведущий научный сотрудник, Научно-исследовательский институт общей реаниматологии имени В.А. Неговского ФНКЦ РР.

119991, Москва, ул. Большая Пироговская, д. 2, стр. 4; 107031, Москва, ул. Петровка, д. 25, стр. 2

Anton V. Ershov - Dr. Sci. (Med.), Professor, Department of Pathophysiology, Institute of Biodesign and Complex Systems Modeling, Sechenov First Moscow State Medical University (Sechenov University); Leading Researcher, Negovsky Research Institute of General Resuscitation of the Federal Scientific and Clinical Center for Resuscitation and Rehabilitology.

2, Bldg. 4, Bolshaya Pirogovskaya St., Moscow, 119991; 2, Bldg. 25, Petrovka St., Moscow, 107031

salavatprof@mail.ruhttps://orcid.org/0000-0003-0151-9114ЛитвицкийП. Ф.LitvitskiyP. F.

Литвицкий Петр Францевич - доктор медицинских наук, профессор, член-корр. РАН, заведующий кафедрой патофизиологии Института биодизайна и моделирования сложных систем.

119991, Москва, ул. Большая Пироговская, д. 2, стр. 4

Peter F. Litvitskiy - Dr. Sci. (Med.), Professor, Corr. Member RAS, Head of the Department of Pathophysiology, Institute of Biodesign and Complex Systems Modeling, Sechenov First Moscow State Medical University (Sechenov University).

2, Bldg. 4, Bolshaya Pirogovskaya St., Moscow, 119991

litvicki@mma.ruhttps://orcid.org/0000-0003-3203-6676РеджеповД. T.RejepovD. T.

Реджепов Довлет Таганович - ассистент Института биохимической технологии и нанотехнологии.

117198, Москва, ул. Миклухо-Маклая, д. 6

Dovlet T. Rejepov - Assistant of the Institute of Biochemical Technology and Nanotechnology, Peoples’ Friendship University of Russia.

6, Miklukho-Maklai St., Moscow, 117198

redjepov_dt@pfur.ruhttps://orcid.org/0000-0003-0032-9917ПоздняковА. А.PozdnyakovA. A.

Поздняков Артем Александрович - старший преподаватель кафедры эпидемиологии и доказательной медицины.

119991, Москва, ул. Большая Пироговская, д. 2, стр. 4

Artem A. Pozdnyakov - Senior Lecturer, Department of Epidemiology and Evidence-Based Medicine, Sechenov First Moscow State Medical University (Sechenov University).

2, Bldg. 4, Bolshaya Pirogovskaya St., Moscow, 119991

artem.a.pozdniakov@gmail.comРоссийский университет дружбы народовРоссияPeoples’ Friendship University of RussiaRussian FederationПервый Московский государственный медицинский университет имени И.М. Сеченова (Сеченовский Университет); Научно-исследовательский институт общей реаниматологии имени В.А. Неговского Федерального научно-клинического центра реаниматологии и реабилитологииРоссияSechenov First Moscow State Medical University (Sechenov University); Negovsky Research Institute of General Resuscitation of the Federal Scientific and Clinical Center for Resuscitation and RehabilitologyRussian FederationПервый Московский государственный медицинский университет имени И.М. Сеченова (Сеченовский Университет)РоссияSechenov First Moscow State Medical University (Sechenov University)Russian Federation2022180120230235059Copyright © Кабаева Е.Н., Ершов А.В., Литвицкий П.Ф., Реджепов Д.T., Поздняков А.А., 20232023Кабаева Е.Н., Ершов А.В., Литвицкий П.Ф., Реджепов Д.T., Поздняков А.А.Kabaeva E.N., Ershov A.V., Litvitskiy P.F., Rejepov D.T., Pozdnyakov A.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.med-sovet.pro/jour/article/view/7294Введение

Введение. COVID-19 повышает риск развития ишемического инсульта (ИИ), однако при этом мало изученным остается влияние COVID-19 на течение восстановительного периода после ИИ.

Цель

Цель. Выявить закономерности и особенности течения и проявлений раннего и позднего этапов восстановительного периода после ИИ, развившегося у пациентов на фоне COVID-19.

Материалы и методы

Материалы и методы. Обследован 81 пациент, разделенный на 3 группы: 1) с ИИ на фоне COVID-19 (n = 21); 2) с инфицированием COVID-19 без ИИ (n = 40); 3) с ИИ без COVID-19 (n = 20). У пациентов с инсультом исследовали степень тяжести инсульта (шкала NIHSS), функциональный статус (шкала Рэнкина), уровень повседневной активности (шкала Бартел). У всех обследуемых оценивали жалобы, общее состояние, уровень активности, способность к самообслуживанию, эмоциональный статус. Анализировали тяжесть течения инсульта, функциональный статус, объем поражений легких по МСКТ, наличие сердечно-сосудистых заболеваний, показатели общего и биохимического анализа крови, динамику уровня цитокинов IL-6, IL-8, IL-10, TNF-α в крови. Со всеми обследуемыми проводили телефонное интервьюирование в течение 12 мес. после выписки из стационара.

Результаты

Результаты. Наибольшая смертность на постгоспитальном этапе (67%) была у пациентов, перенесших ИИ на фоне COVID-19, при этом половина зарегистрирована в первые 3 мес., к концу 6-го месяца этот показатель составил 79%. Летальные исходы у пациентов с ИИ, развившиеся на фоне COVID-19, наступали на 6 мес. раньше, чем в группе пациентов с ИИ без COVID-19. Основными причинами фатальных исходов у пациентов с ИИ на фоне COVID-19 в первые 3 мес. были острый инфаркт миокарда и повторные инсульты. Высокая частота неблагоприятных реабилитационных прогнозов и летальных исходов как в остром периоде заболевания, так и на постгоспитальном этапе отмечалась у пациентов с высокой коморбидностью.

Заключение

Заключение. Пациенты, перенесшие ИИ на фоне COVID-19, в первые 3 мес. постгоспитального периода входят в группу повышенного риска развития тромботических и тромбоэмболических осложнений и летального исхода.

Introduction

Introduction. COVID-19 increases the risk of ischemic stroke (IS), but the impact of COVID-19 on the recovery period of IS remains poorly understood.

The aim of the study – to identify patterns and features of the course and manifestations of the early and late stages of the recovery period after ischemic stroke associated with COVID-19.

Materials and methods

Materials and methods. The combined retro-prospective study included 81 patients. Patients were divided into three groups: 1) development of stroke followed by outcome in ischemic stroke (IS) associated with COVID-19 (n = 21); 2) COVID-19 infection without stroke (n = 40); 3) development of stroke without COVID-19 (n = 20). All subjects were interviewed by telephone within 12 months from the date of discharge from the hospital. In patients with stroke, the severity of stroke (NIHSS scale), functional status (Rankine scale), and daily activity level (Bartel scale) were studied. All subjects were interviewed by telephone within 12 months from the moment of discharge from the hospital, the following were assessed: complaints, general condition of patients, the patient’s level of activity and ability to self-care, emotional status and the presence of anxiety and depressive disorders. The following were retrospectively assessed: stroke severity, functional status, volume of lung lesions according to MSCT, the presence of cardiovascular diseases, indicators of general and biochemical blood tests, changes in blood levels of cytokines IL-6, IL-8, IL-10, TNF-α.

Results

Results. The highest mortality at the post-hospital stage (only 67 and 47% of the total number of deaths) was in patients who had an ischemic stroke associated with COVID-19; half of them were registered in the first 3 months; by the end of the 6th month, this figure was 79%. Deaths in patients with IS due to COVID-19 occur 6 months earlier than in the group of patients with stroke without COVID-19. The leading causes of fatal outcomes in patients with IS due to COVID-19 in the first 3 months were acute myocardial infarction and repeated strokes. A high frequency of unfavorable rehabilitation prognoses and deaths both in the acute period of the disease and at the post-hospital stage was observed in patients with high comorbidity with forms of pathology of the circulatory system.

Conclusion

Conclusion. Patients who have had an ischemic stroke associated with COVID-19, in the first 3 months of the post-hospital period, are at an increased risk of developing thrombotic complications and death and require special attention of outpatient doctors in this period after discharge from the hospital.

ишемический инсультновая коронавирусная инфекцияCOVID-19факторы рискапостковидный синдромischemic strokenovel coronavirus infectionCOVID-19risk factorspost-covid syndromeReferencesLu R., Zhao X., Li J., Niu P., Yang B., Wu H. et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 2020;395(10224):565–574. https://doi.org/10.1016/s0140-6736(20)30251-8.Lu R., Zhao X., Li J., Niu P., Yang B., Wu H. et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 2020;395(10224):565–574. https://doi.org/10.1016/s0140-6736(20)30251-8.Mao L., Jin H., Wang M., Hu Y., Chen S., He Q. et al. Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China. JAMA Neurol. 2020;77(6):683–690. https://doi.org/10.1001/jamaneurol.2020.1127.Mao L., Jin H., Wang M., Hu Y., Chen S., He Q. et al. Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China. JAMA Neurol. 2020;77(6):683–690. https://doi.org/10.1001/jamaneurol.2020.1127.Romero-Sánchez C.M., Díaz-Maroto I., Fernández-Díaz E., Sánchez-Larsen Á., Layos-Romero A., García-García J. et al. Neurologic manifestations in hospitalized patients with COVID-19: The ALBACOVID registry. Neurology. 2020;95(8):e1060–e1070. https://doi.org/10.1212/WNL.0000000000009937.Romero-Sánchez C.M., Díaz-Maroto I., Fernández-Díaz E., Sánchez-Larsen Á., Layos-Romero A., García-García J. et al. Neurologic manifestations in hospitalized patients with COVID-19: The ALBACOVID registry. Neurology. 2020;95(8):e1060–e1070. https://doi.org/10.1212/WNL.0000000000009937.Trejo-Gabriel-Galán J.M. Stroke as a complication and prognostic factor of COVID-19. Neurologia (Engl Ed). 2020;35(5):318–322. https://doi.org/10.1016/j.nrl.2020.04.015.Trejo-Gabriel-Galán J.M. Stroke as a complication and prognostic factor of COVID-19. Neurologia (Engl Ed). 2020;35(5):318–322. https://doi.org/10.1016/j.nrl.2020.04.015.Carod-Artal F.J. Neurological complications of coronavirus and COVID-19. Rev Neurol. 2020;70(9):311–322. https://doi.org/10.33588/rn.7009.2020179.Carod-Artal F.J. Neurological complications of coronavirus and COVID-19. Rev Neurol. 2020;70(9):311–322. https://doi.org/10.33588/rn.7009.2020179.Jimeno-Almazán A., Pallarés J.G., Buendía-Romero Á., Martínez-Cava A., Franco-López F., Sánchez-Alcaraz Martínez B.J. et al. Post-COVID-19 Syndrome and the Potential Benefits of Exercise. Int J Environ Res Public Health. 2021;18(10):5329. https://doi.org/10.3390/ijerph18105329.Jimeno-Almazán A., Pallarés J.G., Buendía-Romero Á., Martínez-Cava A., Franco-López F., Sánchez-Alcaraz Martínez B.J. et al. Post-COVID-19 Syndrome and the Potential Benefits of Exercise. Int J Environ Res Public Health. 2021;18(10):5329. https://doi.org/10.3390/ijerph18105329.Camargo-Martínez W., Lozada-Martínez I., Escobar-Collazos A., NavarroCoronado A., Moscote-Salazar L., Pacheco-Hernández A. et al. Post-COVID 19 neurological syndrome: Implications for sequelae’s treatment. J Clin Neurosci. 2021;88:219–225. https://doi.org/10.1016/j.jocn.2021.04.001.Camargo-Martínez W., Lozada-Martínez I., Escobar-Collazos A., NavarroCoronado A., Moscote-Salazar L., Pacheco-Hernández A. et al. Post-COVID 19 neurological syndrome: Implications for sequelae’s treatment. J Clin Neurosci. 2021;88:219–225. https://doi.org/10.1016/j.jocn.2021.04.001.Yong S.J. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53(10):737–754. https://doi.org/10.1080/23744235.2021.1924397.Yong S.J. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53(10):737–754. https://doi.org/10.1080/23744235.2021.1924397.Ortelli P., Ferrazzoli D., Sebastianelli L., Engl M., Romanello R., Nardone R. et al. Neuropsychological and neurophysiological correlates of fatigue in post-acute patients with neurological manifestations of COVID-19: Insights into a challenging symptom. J Neurol Sci. 2021;420:117271. https://doi.org/10.1016/j.jns.2020.117271.Ortelli P., Ferrazzoli D., Sebastianelli L., Engl M., Romanello R., Nardone R. et al. Neuropsychological and neurophysiological correlates of fatigue in post-acute patients with neurological manifestations of COVID-19: Insights into a challenging symptom. J Neurol Sci. 2021;420:117271. https://doi.org/10.1016/j.jns.2020.117271.Sagris D., Papanikolaou A., Kvernland A., Korompoki E., Frontera J.A., Troxel A.B. et al. COVID-19 and ischemic stroke. Eur J Neurol. 2021;28(11):3826–3836. https://doi.org/10.1111/ene.15008.Sagris D., Papanikolaou A., Kvernland A., Korompoki E., Frontera J.A., Troxel A.B. et al. COVID-19 and ischemic stroke. Eur J Neurol. 2021;28(11):3826–3836. https://doi.org/10.1111/ene.15008.Qin W., Zhang X., Yang S., Li Y., Yuan J., Yang L. et al. Risk Factors for Multiple Organ Dysfunction Syndrome in Severe Stroke Patients. PLoS ONE. 2016;11(11):e0167189. https://doi.org/10.1371/journal.pone.0167189.Qin W., Zhang X., Yang S., Li Y., Yuan J., Yang L. et al. Risk Factors for Multiple Organ Dysfunction Syndrome in Severe Stroke Patients. PLoS ONE. 2016;11(11):e0167189. https://doi.org/10.1371/journal.pone.0167189.Azevedo R.B., Botelho B.G., Hollanda J.V.G., Ferreira L.V.L., Junqueira de Andrade L.Z., Oei S.S.M.L. et al. COVID-19 and the cardiovascular system: a comprehensive review. J Hum Hypertens. 2021;35(1):4–11. https://doi.org/10.1038/s41371-020-0387-4.Azevedo R.B., Botelho B.G., Hollanda J.V.G., Ferreira L.V.L., Junqueira de Andrade L.Z., Oei S.S.M.L. et al. COVID-19 and the cardiovascular system: a comprehensive review. J Hum Hypertens. 2021;35(1):4–11. https://doi.org/10.1038/s41371-020-0387-4.Clerkin K.J., Fried J.A., Raikhelkar J., Sayer G., Griffin J.M., Masoumi A. et al. COVID-19 and Cardiovascular Disease. Circulation. 2020;141(20):1648–1655. https://doi.org/10.1161/CIRCULATIONAHA.120.046941.Clerkin K.J., Fried J.A., Raikhelkar J., Sayer G., Griffin J.M., Masoumi A. et al. COVID-19 and Cardiovascular Disease. Circulation. 2020;141(20):1648–1655. https://doi.org/10.1161/CIRCULATIONAHA.120.046941.Парфенов В.А., Кулеш А.А. Острые и отдаленные неврологические нарушения у пациентов, перенесших коронавирусную инфекцию. Неврология, нейропсихиатрия, психосоматика. 2022;14(3):4–11. https://doi.org/10.14412/2074-2711-2022-3-4-11.Parfenov V.A., Kulesh A.A. Acute and long-term neurological disorders in patients with coronavirus infection. Neurology, Neuropsychiatry, Psychosomatics. 2022;14(3):4–11. https://doi.org/10.14412/2074-2711-2022-3-4-11.Harrison S.L., Fazio-Eynullayeva E., Lane D.A., Underhill P., Lip G.Y.H. Higher Mortality of Ischaemic Stroke Patients Hospitalized with COVID-19 Compared to Historical Controls. Cerebrovasc Dis. 2021;50(3):326–331. https://doi.org/10.1159/000514137.Harrison S.L., Fazio-Eynullayeva E., Lane D.A., Underhill P., Lip G.Y.H. Higher Mortality of Ischaemic Stroke Patients Hospitalized with COVID-19 Compared to Historical Controls. Cerebrovasc Dis. 2021;50(3):326–331. https://doi.org/10.1159/000514137.Asadi-Pooya A.A., Simani L. Central nervous system manifestations of COVID-19: A systematic review. J Neurol Sci. 2020;413:116832. https://doi.org/10.1016/j.jns.2020.116832.Asadi-Pooya A.A., Simani L. Central nervous system manifestations of COVID-19: A systematic review. J Neurol Sci. 2020;413:116832. https://doi.org/10.1016/j.jns.2020.116832.Ahmed S., Zimba O., Gasparyan A.Y. Thrombosis in Coronavirus disease 2019 (COVID-19) through the prism of Virchow’s triad. Clin Rheumatol. 2020;39(9):2529–2543. https://doi.org/10.1007/s10067-020-05275-1.Ahmed S., Zimba O., Gasparyan A.Y. Thrombosis in Coronavirus disease 2019 (COVID-19) through the prism of Virchow’s triad. Clin Rheumatol. 2020;39(9):2529–2543. https://doi.org/10.1007/s10067-020-05275-1.Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. https://doi.org/10.1016/S0140-6736(20)30183-5.Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. https://doi.org/10.1016/S0140-6736(20)30183-5.Tang N., Li D., Wang X., Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost. 2020;18(4):844–847. https://doi.org/10.1111/jth.14768.Tang N., Li D., Wang X., Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost. 2020;18(4):844–847. https://doi.org/10.1111/jth.14768.Akhtar N., Abid F., Singh R., Kamran S., Imam Y., Al-Jerdi S. et al. Ischemic stroke in patients that recover from COVID-19: Comparisons to historical stroke prior to COVID-19 or stroke in patients with active COVID-19 infection. PLoS ONE. 2022;17(6):e0270413. https://doi.org/10.1371/journal.pone.0270413.Akhtar N., Abid F., Singh R., Kamran S., Imam Y., Al-Jerdi S. et al. Ischemic stroke in patients that recover from COVID-19: Comparisons to historical stroke prior to COVID-19 or stroke in patients with active COVID-19 infection. PLoS ONE. 2022;17(6):e0270413. https://doi.org/10.1371/journal.pone.0270413.Asirvatham T., Abubacker M., Isaac Chandran P., Boppana A., Salim Al Abdulla S., Mohammed Saad R. Post-COVID-19 Stroke Rehabilitation in Qatar: A Retrospective, Observational Pilot Study. Qatar Med J. 2022;2022(1):10. https://doi.org/10.5339/qmj.2022.10.Asirvatham T., Abubacker M., Isaac Chandran P., Boppana A., Salim Al Abdulla S., Mohammed Saad R. Post-COVID-19 Stroke Rehabilitation in Qatar: A Retrospective, Observational Pilot Study. Qatar Med J. 2022;2022(1):10. https://doi.org/10.5339/qmj.2022.10.Luo X.H., Zhu Y., Mao J., Du R.C. T cell immunobiology and cytokine storm of COVID-19. Scand J Immunol. 2021;93(3):e12989. https://doi.org/10.1111/sji.12989.Luo X.H., Zhu Y., Mao J., Du R.C. T cell immunobiology and cytokine storm of COVID-19. Scand J Immunol. 2021;93(3):e12989. https://doi.org/10.1111/sji.12989.Quirch M., Lee J., Rehman S. Hazards of the Cytokine Storm and Cytokine-Targeted Therapy in Patients With COVID-19: Review. J Med Internet Res. 2020;22(8):e20193. https://doi.org/10.2196/20193.Quirch M., Lee J., Rehman S. Hazards of the Cytokine Storm and Cytokine-Targeted Therapy in Patients With COVID-19: Review. J Med Internet Res. 2020;22(8):e20193. https://doi.org/10.2196/20193.

The authors declare that there are no conflicts of interest present.