epilepsiaEpilepsy and paroxysmal conditionsЭпилепсия и пароксизмальные состояния2077-83332311-4088IRBIS LLC10.17749/2077-8333/epi.par.con.2021.092epilepsia-732Research ArticleSCIENTIFIC SURVEYSНАУЧНЫЕ ОБЗОРЫNeuroimaging predictors of structural epilepsy in the COVID-19 catamnesisНейровизуализационные предикторы структурных эпилепсий в катамнезе COVID-19https://orcid.org/0000-0001-6098-9146МасловН. Е.MaslovN. E.

Маслов Никита Евгеньевич – ординатор кафедры лучевой диагностики и медицинской визуализации

ул. Аккуратова, д. 2, Санкт-Петербург 197341

РИНЦ SPIN-код: 1422-8694

Nikita E. Maslov – Resident, Chair of Radiology and Medical Imaging

2 Akkuratov Str., Saint Petersburg

RSCI SPIN-code: 1422-8694

atickinwallsome@gmail.comhttps://orcid.org/0000-0001-9419-3533ЮрьеваН. В.YuryevaN. V.

Юрьева Наталья Вячеславовна – к.м.н., доцент кафедры неврологии и нейрохирургии

ул. Крупской, д. 28, Смоленск 214019

 

Natalia V. Yuryeva – MD, PhD, Associate Professor, Chair of Neurology and Neurosurgery

28 Krupskaya Str., Smolensk 214019

RSCI SPIN-code: 4193-3595

https://orcid.org/0000-0002-1986-4621ХамцоваЕ. И.KhamtsovaE. I.

Хамцова Елена Игоревна – к.м.н., доцент кафедры неврологии и нейрохирургии

ул. Крупской, д. 28, Смоленск 214019

РИНЦ SPIN-код: 4091-5210.

Elena I. Khamtsova – MD, PhD, Associate Professor, Chair of Neurology and Neurosurgery

28 Krupskaya Str., Smolensk 214019

RSCI SPIN-code: 4091-5210

https://orcid.org/0000-0003-2845-9983ЛитвиноваА. А.LitvinovaA. A.

Литвинова Александра Алексеевна – студентка 4-го курса лечебного факультета

ул. Крупской, д. 28, Смоленск 214019

РИНЦ SPIN-код: 2234-7591

Aleksandra A. Litvinova – 4th-year Student, Faculty of General Medicine

28 Krupskaya Str., Smolensk 214019

RSCI SPIN-code: 2234-7591

Федеральное государственное бюджетное учреждение «Национальный медицинский исследовательский центр им. В.А. Алмазова» Министерства здравоохранения Российской ФедерацииРоссияAlmazov National Medical Research CenterRussian FederationФедеральное государственное бюджетное образовательное учреждение высшего образования «Смоленский государственный медицинский университет» Министерства здравоохранения Российской ФедерацииРоссияSmolensk State Medical UniversityRussian Federation202128102021133274285Copyright © Maslov N.E., Yuryeva N.V., Khamtsova E.I., Litvinova A.A., 20212021Маслов Н.Е., Юрьева Н.В., Хамцова Е.И., Литвинова А.А.Maslov N.E., Yuryeva N.V., Khamtsova E.I., Litvinova 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.epilepsia.su/jour/article/view/732

Respiratory system pathology is the most common clinical disorder associated with COVID-19. However, there are also lesions of the immune, cardiovascular, genitourinary, endocrine systems, and digestive tract. In addition, there are numerous reports on infection-related neurological manifestations, which can be divided into 3 groups: central nervous system manifestations (headache and dizziness, stroke, encephalopathy, encephalitis, acute myelitis), lesions of the peripheral nervous system (anosmia, Guillain–Barre syndrome), secondary lesions in the skeletal muscles. Brain damage that occurs during novel coronavirus infection and determines some of the above-mentioned manifestations often account for the development of structural epilepsies. Only a few scarce review articles on neuroimaging features in patients with COVID-19 have been found in Russian research publications.The objective of the review was to collect, analyze and summarize the results of brain magnetic resonance imaging (MRI), currently accumulated worldwide in patients with COVID-19. We present the most common diagnoses based on brain MRI in patients with COVID-19 established by foreign researchers from March 2020 to March 2021, as well as initial attempts to interpret the pathophysiological mechanisms of the changes observed in the brain substance.

Патология дыхательной системы является наиболее часто встречающимся клиническим расстройством, связанным с COVID-19. Однако имеют место и поражения иммунной, сердечно-сосудистой, мочеполовой, эндокринной систем, желудочно-кишечного тракта. Встречается также множество сообщений о неврологических проявлениях инфекции, которые можно разделить на три группы: проявления со стороны центральной нервной системы (головная боль и головокружение, острое нарушение мозгового кровообращения, энцефалопатия, энцефалит, острый миелит), поражения периферической нервной системы (аносмия, синдром Гийена–Барре), вторичное поражение скелетных мышц. Повреждения вещества головного мозга, развивающиеся при коронавирусной инфекции и детерминирующие некоторые из вышеуказанных проявлений, зачастую обусловливают развитие структурных эпилепсий. В отечественной литературе на сегодняшний день найдены лишь единичные обзорные публикации по теме особенностей нейровизуализации у пациентов с COVID-19.Цель данного обзора – сбор, анализ и обобщение результатов магнитно-резонансной томографии (МРТ) головного мозга, описанных на настоящий момент в мире у пациентов с COVID-19. Представлены описания наиболее частых заключений, установленных зарубежными исследователями в период с марта 2020 г. по март 2021 г., а также начальные попытки интерпретации патофизиологических механизмов наблюдаемых изменений вещества головного мозга.

COVID-19головной мозгмагнитно-резонансная томографияМРТнейровизуализацияэпилепсияCOVID-19brainmagnetic resonance imagingMRIneuroimagingepilepsyReferencesNikbakht F., Mohammadkhanizadeh A., Mohammadi E. How does the COVID-19 cause seizure and epilepsy in patients? The potential mechanisms. Mult Scler Relat Disord. 2020; 46: 102535. https://doi.org/10.1016/j.msard.2020.102535.Nikbakht F., Mohammadkhanizadeh A., Mohammadi E. How does the COVID-19 cause seizure and epilepsy in patients? The potential mechanisms. Mult Scler Relat Disord. 2020; 46: 102535. https://doi.org/10.1016/j.msard.2020.102535.Vezzani A., Fujinami R.S., White H.S., et al. Infections, inflammation and epilepsy. Acta Neuropathol. 2016; 131 (2): 211–34. https://doi.org/10.1007/s00401-015-1481-5.Vezzani A., Fujinami R.S., White H.S., et al. Infections, inflammation and epilepsy. Acta Neuropathol. 2016; 131 (2): 211–34. https://doi.org/10.1007/s00401-015-1481-5.Mahammedi A., Saba L., Vagal A., et al. Imaging of neurologic disease in hospitalized patients with COVID-19: an Italian multicenter retrospective observational study. Radiology. 2020; 297 (2): E270–3. https://doi.org/10.1148/radiol.2020201933.Mahammedi A., Saba L., Vagal A., et al. Imaging of neurologic disease in hospitalized patients with COVID-19: an Italian multicenter retrospective observational study. Radiology. 2020; 297 (2): E270–3. https://doi.org/10.1148/radiol.2020201933.Mao L., Jin H., Wang M., et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020; 77 (6): 683–90. https://doi.org/10.1001/ jamaneurol.2020.1127.Mao L., Jin H., Wang M., et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020; 77 (6): 683–90. https://doi.org/10.1001/ jamaneurol.2020.1127.Asadi-Pooya A.A. Seizures associated with coronavirus infections. Seizure. 2020; 79: 49–52. https://doi.org/10.1016/j.seizure.2020.05.005.Asadi-Pooya A.A. Seizures associated with coronavirus infections. Seizure. 2020; 79: 49–52. https://doi.org/10.1016/j.seizure.2020.05.005.Asadi-Pooya A.A., Simani L., Shahisavandi M., Barzegar Z. COVID-19, de novo seizures, and epilepsy: a systematic review. Neurol Sci. 2021; 42 (2): 415–31. https://doi.org/10.1007/s10072-020-04932-2.Asadi-Pooya A.A., Simani L., Shahisavandi M., Barzegar Z. COVID-19, de novo seizures, and epilepsy: a systematic review. Neurol Sci. 2021; 42 (2): 415–31. https://doi.org/10.1007/s10072-020-04932-2.Liotta E.M., Batra A., Clark J.R., et al. Frequent neurologic manifestations and encephalopathy-associated morbidity in COVID-19 patients. Ann Clin Transl Neurol. 2020; 7 (11): 2221–30. https://doi.org/10.1002/acn3.51210.Liotta E.M., Batra A., Clark J.R., et al. Frequent neurologic manifestations and encephalopathy-associated morbidity in COVID-19 patients. Ann Clin Transl Neurol. 2020; 7 (11): 2221–30. https://doi.org/10.1002/acn3.51210.Radmanesh A., Raz E., Zan E., et al. Brain imaging use and findings in COVID-19: a single academic center experience in the epicenter of disease in the United States. AJNR Am J Neuroradiol. 2020; 41 (7): 1179–83. https://doi.org/10.3174/ajnr.A6610.Radmanesh A., Raz E., Zan E., et al. Brain imaging use and findings in COVID-19: a single academic center experience in the epicenter of disease in the United States. AJNR Am J Neuroradiol. 2020; 41 (7): 1179–83. https://doi.org/10.3174/ajnr.A6610.Карлов В.А. Эпилепсия у детей и взрослых, женщин и мужчин. Руководство для врачей. 2-е изд. М.: БИНОМ; 2019: 896 с.Karlov V.А. Epilepsy in children and adult women and men. A guide for doctors. 2nd ed. Мoscow: BINOM; 2019: 896 pKubota T., Gajera P.K., Kuroda N. Meta-analysis of EEG findings in patients with COVID-19. Epilepsy Behav. 2021; 115: 107682. https://doi.org/10.1016/j.yebeh.2020.107682.Kubota T., Gajera P.K., Kuroda N. Meta-analysis of EEG findings in patients with COVID-19. Epilepsy Behav. 2021; 115: 107682. https://doi.org/10.1016/j.yebeh.2020.107682.Roberto K.T., Espiritu A.I., Fernandez M.L., Gutierrez J.C. Electroencephalographic findings in COVID-19 patients: a systematic review. Seizure. 2020; 82: 17–22. https://doi.org/10.1016/j.seizure.2020.09.007.Roberto K.T., Espiritu A.I., Fernandez M.L., Gutierrez J.C. Electroencephalographic findings in COVID-19 patients: a systematic review. Seizure. 2020; 82: 17–22. https://doi.org/10.1016/j.seizure.2020.09.007.Rodrigo-Armenteros P., Uterga-Valiente J.M., Zabala-Del-Arco J., et al. Non-convulsive status epilepticus in a patient with COVID-19 infection. Clin Neurophysiol. 2020; 131 (11): 2588–90. https://doi.org/10.1016/j.clinph.2020.08.005.Rodrigo-Armenteros P., Uterga-Valiente J.M., Zabala-Del-Arco J., et al. Non-convulsive status epilepticus in a patient with COVID-19 infection. Clin Neurophysiol. 2020; 131 (11): 2588–90. https://doi.org/10.1016/j.clinph.2020.08.005.DeKosky S.T., Kochanek P.M., Valadka A.B., et al. Blood biomarkers for detection of brain injury in COVID-19 patients. J Neurotrauma. 2021; 38 (1): 1–43. https://doi.org/10.1089/neu.2020.7332.DeKosky S.T., Kochanek P.M., Valadka A.B., et al. Blood biomarkers for detection of brain injury in COVID-19 patients. J Neurotrauma. 2021; 38 (1): 1–43. https://doi.org/10.1089/neu.2020.7332.Whelan C.D., Altmann A., Botía J.A., et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018; 141 (2): 391–408. https://doi.org/10.1093/brain/awx341.Whelan C.D., Altmann A., Botía J.A., et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018; 141 (2): 391–408. https://doi.org/10.1093/brain/awx341.Duncan J.S., Winston G.P., Koepp M.J., Ourselin S. Brain imaging in the assessment for epilepsy surgery. Lancet Neurol. 2016; 15 (4): 420–33. https://doi.org/10.1016/S1474-4422(15)00383-X.Duncan J.S., Winston G.P., Koepp M.J., Ourselin S. Brain imaging in the assessment for epilepsy surgery. Lancet Neurol. 2016; 15 (4): 420–33. https://doi.org/10.1016/S1474-4422(15)00383-X.Белопасов В.В., Яшу Я., Самойлова Е.М., Баклаушев В.П. Поражение нервной системы при СOVID-19. Клиническая практика. 2020; 11 (2): 60–80. https://doi.org/10.17816/clinpract34851.Belopasov V.V., Yachou Y., Samoilova E.M., Baklaushev V.P. The nervous system damage in COVID-19. Journal of Clinical Practice. 2020; 11 (2): 60–80 (in Russ.). https://doi.org/10.17816/clinpract34851.Kremer S., Lersy F., de Sèze J., et al. Brain MRI findings in severe COVID-19: a retrospective observational study. Radiology. 2020; 297 (2): E242–51. https://doi.org/10.1148/radiol.2020202222.Kremer S., Lersy F., de Sèze J., et al. Brain MRI findings in severe COVID-19: a retrospective observational study. Radiology. 2020; 297 (2): E242–51. https://doi.org/10.1148/radiol.2020202222.Moriguchi T., Harii N., Goto J., et al. A first case of meningitis/ encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis. 2020; 94: 55–8. https://doi.org/10.1016/j.ijid.2020.03.062.Moriguchi T., Harii N., Goto J., et al. A first case of meningitis/ encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis. 2020; 94: 55–8. https://doi.org/10.1016/j.ijid.2020.03.062.Budhram A., Leung A., Nicolle M.W., Burneo J.G. Diagnosing autoimmune limbic encephalitis. CMAJ. 2019; 191 (19): E529–34. https://doi.org/10.1503/cmaj.181548.Budhram A., Leung A., Nicolle M.W., Burneo J.G. Diagnosing autoimmune limbic encephalitis. CMAJ. 2019; 191 (19): E529–34. https://doi.org/10.1503/cmaj.181548.Parsons T., Banks S., Bae C., et al. COVID-19-associated acute disseminated encephalomyelitis (ADEM). J Neurol. 2020; 267 (10): 2799–802. https://doi.org/10.1007/s00415-020-09951-9.Parsons T., Banks S., Bae C., et al. COVID-19-associated acute disseminated encephalomyelitis (ADEM). J Neurol. 2020; 267 (10): 2799–802. https://doi.org/10.1007/s00415-020-09951-9.Pohl D., Alper G., Van Haren K., et al. Acute disseminated encephalomyelitis: updates on an inflammatory CNS syndrome. Neurology. 2016; 87 (9 Suppl. 2): S38–45. https://doi.org/10.1212/WNL.0000000000002825.Pohl D., Alper G., Van Haren K., et al. Acute disseminated encephalomyelitis: updates on an inflammatory CNS syndrome. Neurology. 2016; 87 (9 Suppl. 2): S38–45. https://doi.org/10.1212/WNL.0000000000002825.Nabi S., Badshah M., Ahmed S., Nomani A.Z. Weston–Hurst syndrome: a rare fulminant form of acute disseminated encephalomyelitis (ADEM). BMJ Case Rep. 2016; 2016: bcr2016217215. https://doi.org/10.1136/bcr-2016-217215.Nabi S., Badshah M., Ahmed S., Nomani A.Z. Weston–Hurst syndrome: a rare fulminant form of acute disseminated encephalomyelitis (ADEM). BMJ Case Rep. 2016; 2016: bcr2016217215. https://doi.org/10.1136/bcr-2016-217215.Needham E.J., Chou S.H., Coles A.J., Menon D.K. Neurological implications of COVID-19 infections. Neurocrit Care. 2020; 32 (3): 667–71. https://doi.org/10.1007/s12028-020-00978-4.Needham E.J., Chou S.H., Coles A.J., Menon D.K. Neurological implications of COVID-19 infections. Neurocrit Care. 2020; 32 (3): 667–71. https://doi.org/10.1007/s12028-020-00978-4.Reichard R.R., Kashani K.B., Boire N.A., et al. Neuropathology of COVID-19: a spectrum of vascular and acute disseminated encephalomyelitis (ADEM)-like pathology. Acta Neuropathol. 2020; 140 (1): 1–6. https://doi.org/10.1007/s00401-020-02166-2.Reichard R.R., Kashani K.B., Boire N.A., et al. Neuropathology of COVID-19: a spectrum of vascular and acute disseminated encephalomyelitis (ADEM)-like pathology. Acta Neuropathol. 2020; 140 (1): 1–6. https://doi.org/10.1007/s00401-020-02166-2.Radmanesh A., Derman A., Lui Y.W., et al. COVID-19-associated diffuse leukoencephalopathy and microhemorrhages. Radiology. 2020; 297 (1): E223–7. https://doi.org/10.1148/radiol.2020202040.Radmanesh A., Derman A., Lui Y.W., et al. COVID-19-associated diffuse leukoencephalopathy and microhemorrhages. Radiology. 2020; 297 (1): E223–7. https://doi.org/10.1148/radiol.2020202040.Radmanesh F., Rodriguez-Pla A., Pincus M.D., Burns J.D. Severe cerebral involvement in adult-onset hemophagocytic lymphohistiocytosis. J Clin Neurosci. 2020; 76: 236–7. https://doi.org/10.1016/j.jocn.2020.04.054.Radmanesh F., Rodriguez-Pla A., Pincus M.D., Burns J.D. Severe cerebral involvement in adult-onset hemophagocytic lymphohistiocytosis. J Clin Neurosci. 2020; 76: 236–7. https://doi.org/10.1016/j.jocn.2020.04.054.Katyal N., Narula N., George P., et al. Delayed post-hypoxic leukoencephalopathy: a case series and review of the literature. Cureus. 2018; 10 (4): e2481. https://doi.org/10.7759/cureus.2481.Katyal N., Narula N., George P., et al. Delayed post-hypoxic leukoencephalopathy: a case series and review of the literature. Cureus. 2018; 10 (4): e2481. https://doi.org/10.7759/cureus.2481.Kandemirli S.G., Dogan L., Sarikaya Z.T., et al. Brain MRI findings in patients in the intensive care unit with COVID-19 infection. Radiology. 2020; 297 (1): E232–5. https://doi.org/10.1148/radiol.2020201697.Kandemirli S.G., Dogan L., Sarikaya Z.T., et al. Brain MRI findings in patients in the intensive care unit with COVID-19 infection. Radiology. 2020; 297 (1): E232–5. https://doi.org/10.1148/radiol.2020201697.Kishfy L., Casasola M., Banankhah P., et al. Posterior reversible encephalopathy syndrome (PRES) as a neurological association in severe COVID-19. J Neurol Sci. 2020; 414: 116943. https://doi.org/10.1016/j.jns.2020.116943.Kishfy L., Casasola M., Banankhah P., et al. Posterior reversible encephalopathy syndrome (PRES) as a neurological association in severe COVID-19. J Neurol Sci. 2020; 414: 116943. https://doi.org/10.1016/j.jns.2020.116943.Gulko E., Oleksk M.L., Gomes W., et al. MRI brain findings in 126 patients with COVID-19: initial observations from a descriptive literature review. AJNR Am J Neuroradiol. 2020; 41 (12): 2199–203. https://doi.org/10.3174/ajnr.A6805.Gulko E., Oleksk M.L., Gomes W., et al. MRI brain findings in 126 patients with COVID-19: initial observations from a descriptive literature review. AJNR Am J Neuroradiol. 2020; 41 (12): 2199–203. https://doi.org/10.3174/ajnr.A6805.Choi Y., Lee M.K. Neuroimaging findings of brain MRI and CT in patients with COVID-19: a systematic review and meta-analysis. Eur J Radiol. 2020; 133: 109393. https://doi.org/10.1016/j.ejrad.2020.109393.Choi Y., Lee M.K. Neuroimaging findings of brain MRI and CT in patients with COVID-19: a systematic review and meta-analysis. Eur J Radiol. 2020; 133: 109393. https://doi.org/10.1016/j.ejrad.2020.109393.Nepal G., Rehrig J.H., Shrestha G.S., et al. Neurological manifestations of COVID-19: a systematic review. Crit Care. 2020; 24 (1): 421. https://doi.org/10.1186/s13054-020-03121-z.Nepal G., Rehrig J.H., Shrestha G.S., et al. Neurological manifestations of COVID-19: a systematic review. Crit Care. 2020; 24 (1): 421. https://doi.org/10.1186/s13054-020-03121-z.Maas M.B. Critical medical illness and the nervous system. Continuum (Minneap Minn). 2020; 26 (3): 675–94. https://doi.org/10.1212/CON.0000000000000869.Maas M.B. Critical medical illness and the nervous system. Continuum (Minneap Minn). 2020; 26 (3): 675–94. https://doi.org/10.1212/CON.0000000000000869.Radmanesh A., Derman A., Lui Y.W., et al. COVID-19-associated diffuse leukoencephalopathy and microhemorrhages. Radiology. 2020; 297 (1): E223–7. https://doi.org/10.1148/radiol.2020202040.Radmanesh A., Derman A., Lui Y.W., et al. COVID-19-associated diffuse leukoencephalopathy and microhemorrhages. Radiology. 2020; 297 (1): E223–7. https://doi.org/10.1148/radiol.2020202040.Coolen T., Lolli V., Sadeghi N., et al. Early postmortem brain MRI findings in COVID-19 non-survivors. Neurology. 2020; 95 (14): e2016–27. https://doi.org/10.1212/WNL.0000000000010116.Coolen T., Lolli V., Sadeghi N., et al. Early postmortem brain MRI findings in COVID-19 non-survivors. Neurology. 2020; 95 (14): e2016–27. https://doi.org/10.1212/WNL.0000000000010116.Chougar L., Shor N., Weiss N., et al. Retrospective observational study of brain MRI findings in patients with acute SARS-CoV-2 infection and neurologic manifestations. Radiology. 2020; 297 (3): E313–23. https://doi.org/10.1148/radiol.2020202422.Chougar L., Shor N., Weiss N., et al. Retrospective observational study of brain MRI findings in patients with acute SARS-CoV-2 infection and neurologic manifestations. Radiology. 2020; 297 (3): E313–23. https://doi.org/10.1148/radiol.2020202422.D’Amore F., Vinacci G., Agosti E., et al. Pressing issues in COVID-19: probable cause to seize SARS-CoV-2 for its preferential involvement of posterior circulation manifesting as severe posterior reversible encephalopathy syndrome and posterior strokes. AJNR Am J Neuroradiol. 2020; 41 (10): 1800–3. https://doi.org/10.3174/ajnr.A6679.D’Amore F., Vinacci G., Agosti E., et al. Pressing issues in COVID-19: probable cause to seize SARS-CoV-2 for its preferential involvement of posterior circulation manifesting as severe posterior reversible encephalopathy syndrome and posterior strokes. AJNR Am J Neuroradiol. 2020; 41 (10): 1800–3. https://doi.org/10.3174/ajnr.A6679.Li Z., Liu T., Yang N., et al. Neurological manifestations of patients with COVID-19: potential routes of SARS-CoV-2 neuroinvasion from the periphery to the brain. Front Med. 2020; 14 (5): 533–41. https://doi.org/10.1007/s11684-020-0786-5.Li Z., Liu T., Yang N., et al. Neurological manifestations of patients with COVID-19: potential routes of SARS-CoV-2 neuroinvasion from the periphery to the brain. Front Med. 2020; 14 (5): 533–41. https://doi.org/10.1007/s11684-020-0786-5.Yavarpour-Bali H., Ghasemi-Kasman M. Update on neurological manifestations of COVID-19. Life Sci. 2020; 257: 118063. https://doi.org/10.1016/j.lfs.2020.118063.Yavarpour-Bali H., Ghasemi-Kasman M. Update on neurological manifestations of COVID-19. Life Sci. 2020; 257: 118063. https://doi.org/10.1016/j.lfs.2020.118063.

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