References

emcardio

Неотложная кардиология и кардиоваскулярные риски

Emergency Cardiology and Cardiovascular Risks journal

2616-633X

Белорусский государственный медицинский университет

10.51922/2616-633X.2021.5.2.1386

emcardio-162

Research Article

Обзоры и лекции

Reviews and lectures

Магнитно-резонансная томография в диагностике вирусных миокардитов у пациентов с COVID-19: нерешенные проблемы

Cardiac magnetic resonance imagining in viral myocarditis in patients with COVID-19: unsolved problems

Ильина

Т. В.

Ilyina

Плешко

А. А.

Pleshko

Короткая

Т. И.

Korotkaya

Митьковская

Н. П.

Mitkovskaya

ГУ «РНПЦ «Кардиология»Republican Scientific and Practical Center Cardiology

УО «Белорусский государственный медицинский университет»Belarusian State Medical University

УЗ «Городская клиническая больница скорой медицинской помощи г. Минска»Minsk City Emergency Hospital

2021

24102025

1386–1394

2025

Ильина Т.В., Плешко А.А., Короткая Т.И., Митьковская Н.П.

Ilyina T., Pleshko A., Korotkaya T., Mitkovskaya N.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://emcardio.bsmu.by/jour/article/view/162

Сердечные проявления COVID-19, включая повреждение миокарда, сопровождающееся гповышением уровня тропонина, являются распространенным явлением. Сообщается о миокардите как о возможном осложнении у пациентов с коронавирусом, однако прямые доказательства миокардита на фоне SARS-CoV-2 остаются ограниченными. Описанные серии патоморфологических характеристик, относящиеся к миокардиту при COVID-19, различаются по степени выраженности и интерпретации. Клинические проявления неишемического повреждения миокарда неспецифичны, дифференциальная диагностика еще более затруднена на фоне осложнений вирусной пневмонии. Магнитно-резонансная томография (МРТ) является мощным инструментом для исследования структурно-функциональных изменений сердца при миокардиальном повреждении; новые импульсные последовательности параметрического картирования с определением времени Т1 и Т2 релаксации миокарда – уникальный метод для количественной оценки тканевых характеристик миокарда. Коллективом авторов проведен ретроспективный анализ результатов МРТ 45 пациентов с COVID-19, направленных на МРТ сердца в ГУ «РНПЦ Кардиология» за 6 месяцев 2021 года. Удельный вес пациентов с положительными критериями миокардита Lake Louise составил 18% (n = 8), в структуре патологических изменений самым частым изменением тканевых характеристик миокарда было повышение референсных значений T2 ≥ 2σ в 33%. Среди опубликованных данных о повреждении миокарда существует значительная вариативность в частоте выявления миокардита, связанная с методологическими различиями в исследованиях и разночтениями в интерпретации данных параметрических МР-последовательностей. Этот краткий обзор имеет целью пересмотреть и обобщить текущие знания о миокардите у пациентов с COVID-19, подчеркнуть проблемы, связанные с МРТ-диагностикой.

Cardiac manifestations in COVID-19, including myocardial injury with elevated troponin levels, are common. Myocarditis has been reported as a possible complication in coronavirus patients, but direct evidence for SARS-CoV-2 myocarditis remains limited. The described series of histopathological confirmations of myocarditis in COVID-19 differ in severity and interpretation. Clinical manifestations of non-ischemic myocardial injury are nonspecific, differential diagnosis is even more difficult due to the complications after viral pneumonia. Cardiac Magnetic Resonance Imaging (CMRI) is a powerful tool for studying structural and functional changes in myocardial injury. New pulse sequences of parametric mapping with determination of the T1 and T2 relaxation times of the myocardium are a unique method for quantitative assessment of the myocardium tissue. Within 6 months in 2021, we retrospectively analyzed the CMRI results of 45 patients with COVID-19 at the Republican Scientific and Practical Center “Cardiology”. The percentage of patients with positive criteria for Lake Louise myocarditis was 18% (n = 8). The elevated reference values of T2 ≥ 2σ up to 33% was the most frequent pathological change in myocardial tissue characteristics. There is significant variability in the published data collection as to the prevalence of myocarditis associated with different research methodologies in studies and discrepancies in the interpretation of MRI-mapping data. This brief review is aimed at revising and summarizing current knowledge on myocarditis in COVID-19 patients and highlight the problems of CMRI diagnostics.

коронавирусная инфекцияCOVID-19SARS-CoV-2МРТ сердцаострый миокардитповреждение миокарда

coronavirus infectionCOVID-19SARS-CoV-2cardiac MRIacute myocarditismyocardial injury

References1

Ammirati E., Frigerio M., Adler E.D., Basso C., Birnie D.H., Brambatti M., Friedrich M.G., Klingel K., Lehtonen J., Moslehi J.J., Pedrotti P., Rimoldi O.E., Schultheiss H.-P., Tschöpe C., Cooper Jr L.T., Camici P.G. Management of Acute Myocarditis and Chronic Inflammatory Cardiomyopathy. Circ Heart Fail, 2020, vol. 13(11), pp. e007405.

Wang X., Bu X., Wei L., Liu J., Yang D., Mann D.L., Ma A., Hayashi T.nGlobal, Regional, and National Burden of Myocarditis From 1990 to 2017: A Systematic Analysis Based on the Global Burden of Disease Study 2017. Front Cardiovasc Med, 2021, vol. 8, pp. 692990.

Amvrosieva T.V., Mitkovskaya N.P., Bohush Z.F., Arinovich A.S., Balysh E.M. Vozbuditeli virusnyh miokarditov [The causative agents of viral myocarditis]. Neotlozhnaya kardiologiya i kardiovaskulyarnye riski, 2020, vol. 4, no. 1, pp. 817-823. (in Russian).

Thygesen K., Alpert J.S., Jaffe A.S., Chaitman B.R., Bax J.J., Morrow D.A., White H.D. Fourth universal definition of myocardial infarction (2018). Eur Heart J Oxford Academic, 2019, vol. 40(3), pp. 237-269. doi: 10.1093/eurheartj/ehy462.

Tersalvi G., Vicenzi M., Calabretta D., Biasco L., Pedrazzini G., Winterton D.mElevated Troponin in Patients With Coronavirus Disease 2019: Possible Mechanisms. J Card Fail, 2020, vol. 26(6), pp. 470-475.

Lala A., Johnson K.W., Januzzi J.L., Russak A.J., Paranjpe I., Richter F., Zhao S., Somani S., Van Vleck T., Vaid A. et al. Prevalence and Impact of Myocardial Injury in Patients Hospitalized with COVID-19 Infection. J Am Coll Cardiol, 2020, vol. 76(5), pp. 533-546. doi: 10.1016/j.jacc.2020.06.007.

Guo T., Fan Y., Chen M., Wu X., Zhang L., He T., Wang H., Wan J., Wang X., Lu Z. Cardiovascular Implications of Fatal Outcomes of Patients with Coronavirus Disease 2019 (COVID-19). JAMA Cardiol, 2020, vol. 5(7), pp. 811-818.

Singh S., Desai R., Gandhi Z., Fong H.K., Doreswamy S., Desai V., Chockalingam A., Mehta P.K., Sachdeva R., Kumar G. Takotsubo Syndrome in Patients with COVID-19: a Systematic Review of Published Cases. SN Compr Clin Med, 2020, vol. 6, pp. 1-7. doi: 10.1007/s42399-020-00557-w.

Fox S.E., Lameira F.S., Rinker E.B., Vander Heide R.S. Cardiac Endotheliitis and Multisystem Inf lammator y Syndrome Af ter COVID-19. Ann Intern Med, 2020, vol. 173(12), pp. 1025-1027.

Creel-Bulos C., Hockstein M., Amin N., Melhem S., Truong A., Sharifpour M. Acute Cor Pulmonale in Critically Ill Patients with Covid-19. N Engl J Med, 2020, vol. 382(21), pp. e70.

Suh Y.J., Hong H., Ohana M., Bompard F., Revel M.-P., Valle C., Gervaise A., Poissy J., Susen S., Hékimian G. et al. Pulmonary Embolism and Deep Vein Thrombosis in COVID-19: A Systematic Review and Meta-Analysis. Radiology, 2021, vol. 298(2), pp. E70-E80.

Roshdy A., Zaher S., Fayed H., Gerry J. CoghlanCOVID-19 and the Heart: A Systematic Review of Cardiac Autopsies. Front Cardiovasc Med, 2021, vol. 7, pp. 626975. doi: 10.3389/fcvm.2020.626975.

Clerkin K.J., Fried J.A., Raikhelkar J., Sayer G., Griffin J.M., Masoumi A., Jain S.S., Burkhoff D., Kumaraiah D., Rabbani L.R., Schwartz A., Uriel N. COVID-19 and Cardiovascular Disease. Circulation, 2020, vol. 141(20), pp. 1648-1655.

Inciardi R.M., Lupi L., Zaccone G., Italia L., Raffo M., Tomasoni D., Cani D.S., l Cerini M., Farina D., Gavazzi E., Maroldi R., Adamo M., Ammirati E., Sinagra G., Lombardi C.M., Metra M. Cardiac Involvement in a Patient with Coronavirus Disease 2019 (COVID-19). JAMA Cardiol, 2020, vol. 5(7), pp. 819.

Zhou F., Yu T., Du R., Fan G., Liu Y., Liu Z., Xiang J., Wang Y., Song B., Gu X., Guan L., Wei Y., Li H., Wu X., Xu J., Tu S., Zhang Y., Chen H., Cao B. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet, 2020, vol. 395(10229), pp. 1054-1062.

Kogan E.A., Berezovskiy Yu.S., Blagova O.V., Kukleva A.D., Bogacheva G.A., Kurilina E.V., Kalinin D.V., Bagdasaryan T.R., Semeyonova L.A., Gretsov E.M., Ergeshov A.E., Fomin V.V. Miocarditis in Patients with COVID-19 Confirmed by Immunohistochemical. Kardiologiia. 2020, vol 60(7), pp. 4-10. doi: 10.18087/cardio.2020.7.n1209

Halushka M.K., Vander Heide R.S. Myocarditis is rare in COVID-19 autopsies: cardiovascular findings across 277 postmortem examinations. Cardiovasc Pathol, 2021, vol. 50, pp. 107300.

Aretz H.T., Billingham M.E., Edwards W.D., Factor S.M., Fallon J.T., Fenoglio Jr J.J., Olsen E.G., Schoen F.J. Myocarditis. A histopathologic definition and classification. Am J Cardiovasc Pathol, 1987, vol. 1(1), pp. 3-14.

Caforio A.L.P., Pankuweit S., Arbustini E., Basso C., Gimeno-Blanes J., Felix S.B., Fu M., Heliö T., Heymans S., Jahns R., Klingel K., Linhart A., Maisch B., McKenna W., Mogensen J., Pinto Y.M., Ristic A. et al. Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J, 2013, vol. 34(33), pp. 2636-2648, 2648a-2648d.

Kawakami R., Sakamoto A., Kawai K., Gianatti A., Pellegrini D., Nasr A., Kutys B., Guo L., Cornelissen A., Mori M., Sato Y., Pescetelli I., Brivio M., Romero M., Guagliumi G., Virmani R., Finn A.V. Pathological Evidence for SARS-CoV-2 as a Cause of Myocarditis. J Am Coll Cardiol, 2021, vol. 77(3), pp. 314-325.

Fox S.E., Vander Heide R.S. COVID-19: The Heart of the Matter-Pathological Changes and a Proposed Mechanism. J Cardiovasc Pharmacol Ther, 2021, vol. 26(3), pp. 217-224.

Cooper L.T., Baughman K.L., Feldman A.M., Frustaci A., Jessup M., Kuhl U., Levine G.N., Narula J., Starling R.C., Towbin J., Virmani R. et al. The Role of Endomyocardial Biopsy in the Management of Cardiovascular Disease a Scientific Statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. Circulation, 2007, vol. 116(19), pp. 2216-2233.

Cenko E., Badimon L., Bugiardini R., Claeys M.J., de Luca G., de Wit C., Derumeaux G., Dorobantu M., Duncker D.J., Eringa E.C. Cardiovascular disease and COVID-19: a consensus paper from the ESC Working Group on Coronary Pathophysiology & Microcirculation, ESC Working Group on Thrombosis and the Association for Acute CardioVascular Care (ACVC), in collaboration with the European Heart Rhythm Association (EHRA). Cardiovasc Res, 2021, Sep 16, cvab298. doi: 10.1093/cvr/cvab298.

ESC Guidance for the Diagnosis and Management of CV Disease during the COVID-19 Pandemic: part 2-care pathways, treatment, and follow-up. Eur Heart J, 2021, Nov 16, ehab697. doi: 10.1093/eurheartj/ehab697.

Catapano F., Marchitelli L., Cundari G., Cilia F., Mancuso G., Pambianchi G., Galea N., Ricci P., Catalano C., Francone M. Role of advanced imaging in COVID-19 cardiovascular complications. Insights Imaging, 2021, vol. 12(1), pp. 28. doi: 10.1186/s13244-021-00973-z.

Long B., Brady W.J., Bridwell R.E., Ramzy M., Montrief T., Singh M., Gottlieb M. Electrocardiographic manifestations of COVID-19. Am J Emerg Med, 2021, vol. 41, pp. 96-103.

Giustino G., Croft L.B., Stefanini G.G., Bragato R., Silbiger J.J., Vicenzi M., Danilov T., Kukar N., Shaban N., Kini A. et al. Characterization of Myocardial Injury in Patients with COVID-19. J Am Coll Cardiol, 2020, vol. 76(18), pp. 2043-2055.

Dweck M.R., Bularga A., Hahn R.T., Bing R., Lee K.K., Chapman A.R., White A., Di Salvo G., Sade L.E., Pearce K., Newby D.E., Popescu B.A., Donal E., Cosyns B., Edvardsen T., Mills N.L., Haugaa K. Global evaluation of echocardiography in patients with COVID-19. Eur Heart J Cardiovasc Imaging, 2020, vol. 21(9), pp. 949-958.

Kelle S., Bucciarelli-Ducci C., Judd R.M., Kwong R.Y., Simonetti O., Plein S., Raimondi F., Weinsaft J.W., Wong T.C., Carr J. Society for Cardiovascular Magnetic Resonance (SCMR) recommended CMR protocols for scanning patients with active or convalescent phase COVID-19 infection. J Cardiovasc Magn Reson, 2020, vol. 22(1), pp. 61.

Ferreira V.M., Schulz-Menger J., Holmvang G., Kramer C.M., Carbone I., Sechtem U., Kindermann I., Gutberlet M., Cooper L.T., Liu P., Friedrich M.G. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation: Expert Recommendations. J Am Coll Cardiol, 2018, vol. 72(24), pp. 3158-3176.

Kotecha T., Knight D.S., Razvi Y., Kumar K., Vimalesvaran K., Thornton G., Patel R., Chacko L., Brown J.T., Coyle C. Patterns of myocardial injury in recovered troponin-positive COVID-19 patients assessed by cardiovascular magnetic resonance. Eur Heart J, 2021, vol. 42(19), pp. 1866-1878.

Rajpal S., Tong M.S., Borchers J., Zareba K.M., Obarski T.P., Simonetti O.P., Daniels C.J. Cardiovascular Magnetic Resonance Findings in Competitive Athletes Recovering from COVID-19 Infection. JAMA Cardiol, 2021, vol. 6(1), pp. 116-118.

Raman B., Cassar M.P., Tunnicliffe E.M., Filippini N., Griffanti L., Alfaro-Almagro F., Okell T., Sheerin F., Xie C., Mahmod M., Mózes F.E. Medium-term effects of SARS-CoV-2 infection on multiple vital organs, exercise capacity, cognition, quality of life and mental health, post-hospital discharge. EClinicalMedicine, 2021, vol. 31, pp. 100683. doi: 10.1016/j.eclinm.2020.100683.

Puntmann V.O., Carerj M.L., Wieters I., Fahim M., Arendt C., Hoffmann J., Shchendrygina A., Escher F., Vasa-Nicotera M., Zeiher A.M., Vehreschild M., Nagel E. Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered from Coronavirus Disease 2019 (COVID-19). JAMA Cardiol, 2020, vol. 5(11), pp. e203557.

Schulz-Menger J., Bluemke D.A., Bremerich J., Flamm S., Fogel M.A., Friedrich M.G., Kim R.J., von Knobelsdorff-Brenkenhoff F., Kramer C.M., Pennell D.J., Plein S., Nagel E. Standardized image interpretation and post-processing in cardiovascular magnetic resonance - 2020 update. J Cardiovasc Magn Reson, 2020, vol. 22(1), pp. 19.

Kramer C.M., Barkhausen J., Bucciarelli-Ducci C., Flamm S.D., Kim R.J., Nagel E. Standardized cardiovascular magnetic resonance imaging (CMR) protocols: 2020 update. J Cardiovasc Magn Reson, 2020, vol. 22(1), pp. 17.

von Knobelsdorff-Brenkenhoff F., Schüler J., Dogangüzel S., Dieringer M.A., Rudolph A., Greiser A., Kellman P., Schulz-Menger J. Detection and Monitoring of Acute Myocarditis Applying Quantitative Cardiovascular Magnetic Resonance. Circ Cardiovasc Imaging, 2017, vol. 10(2), pp. e005242. doi: 10.1161/CIRCIMAGING.116.005242.

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