COVID-19-related cardiac lesion: The questions of pathogenesis and diagnostics
- Authors: Filatova D.A.1, Mershina E.A.1,2, Sinitsyn V.E.1,2
-
Affiliations:
- Lomonosov Moscow State University
- Medical Research and Education Center of Lomonosov Moscow State University
- Issue: Vol 4, No 2 (2023)
- Pages: 156-169
- Section: Systematic reviews
- URL: https://journals.rcsi.science/DD/article/view/146883
- DOI: https://doi.org/10.17816/DD284706
- ID: 146883
Cite item
Abstract
Coronavirus infection is still a topic of interest in the medical community today. Among the heterogeneous clinical manifestations of this disease, lesions of cardiac structures often occur. They are mainly inflammatory in nature and can be acute or delayed. Aside from myocarditis, coronavirus infection can induce cardiac injuries, including acute coronary syndrome, thromboembolic events, heart failure, and heart rhythm disturbances. It is well known that the prognosis for patients with cardiac lesions significantly worsens; timely diagnosis and treatment initiation play an important role in preventing severe complications.
This review presents the most recent literature data on the pathogenesis of cardiac lesions in COVID-19 patients and discusses the rational diagnosis of this pathology using modern techniques, such as laboratory, functional imaging (cardiac magnetic resonance is the most important of these), and invasive ones. It is now established that diagnosing myocarditis caused by coronavirus infection differs fundamentally from diagnosing other types of myocarditis. Furthermore, the main aspects of inflammatory heart lesions associated with COVID-19 vaccination are discussed, as this complication occurs more frequently than is commonly believed. It is often used as a rationale for refusing vaccination; however, this decision may severely affect the individual and the population.
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##article.viewOnOriginalSite##About the authors
Daria A. Filatova
Lomonosov Moscow State University
Email: dariafilatova.msu@mail.ru
ORCID iD: 0000-0002-0894-1994
SPIN-code: 2665-5973
Russian Federation, Moscow
Elena A. Mershina
Lomonosov Moscow State University; Medical Research and Education Center of Lomonosov Moscow State University
Email: elena_mershina@mail.ru
ORCID iD: 0000-0002-1266-4926
SPIN-code: 6897-9641
MD, Cand. Sci. (Med), Associate Professor
Russian Federation, Moscow; MoscowValentin E. Sinitsyn
Lomonosov Moscow State University; Medical Research and Education Center of Lomonosov Moscow State University
Author for correspondence.
Email: vsini@mail.ru
ORCID iD: 0000-0002-5649-2193
SPIN-code: 8449-6590
MD, Dr. Sci. (Med), Professor
Russian Federation, Moscow; MoscowReferences
- Shi S, Qin M, Shen B, et al. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiol. 2020;5(7):802–810. doi: 10.1001/jamacardio.2020.0950
- Lala A, Johnson KW, Januzzi JL, et al. Prevalence and impact of myocardial injury in patients hospitalized with COVID-19 infection. J Am Coll Cardiol. 2020;76(5):533–546. doi: 10.1016/j.jacc.2020.06.007
- Lindner D, Fitzek A, Bräuninger H, et al. Association of cardiac infection with SARS-CoV-2 in confirmed COVID-19 autopsy cases. JAMA Cardiol. 2020;5(11):1–5. doi: 10.1001/jamacardio.2020.3551
- Sala S, Peretto G, Gramegna M, et al. Acute myocarditis presenting as a reverse Tako-Tsubo syndrome in a patient with SARS-CoV-2 respiratory infection. Eur Heart J. 2020;41(19):1861–1862. doi: 10.1093/eurheartj/ehaa286
- Escher F, Pietsch H, Aleshcheva G, et al. Detection of viral SARS-CoV-2 genomes and histopathological changes in endomyocardial biopsies. ESC Heart Fail. 2020;7(5):2440–2447. doi: 10.1002/ehf2.12805
- Tavazzi G, Pellegrini C, Maurelli M, et al. Myocardial localization of coronavirus in COVID-19 cardiogenic shock. Eur J Heart Fail. 2020;22(5):911–915. doi: 10.1002/ejhf.1828
- Wichmann D. Autopsy findings and venous thromboembolism in patients with COVID-19. Ann Intern Med. 2020;173(12):1030. doi: 10.7326/L20-1206
- Buja LM, Wolf DA, Zhao B, et al. The emerging spectrum of cardiopulmonary pathology of the coronavirus disease 2019 (COVID-19): Report of 3 autopsies from Houston, Texas, and review of autopsy findings from other United States cities. Cardiovasc Pathol. 2020;(48):107233. doi: 10.1016/j.carpath.2020.107233
- Fox SE, Akmatbekov A, Harbert JL, et al. Pulmonary and cardiac pathology in African American patients with COVID-19: An autopsy series from New Orleans. Lancet Respir Med. 2020;10(7):681–686. doi: 10.1016/S2213-2600(20)30243-5
- Alijotas-Reig J, Esteve-Valverde E, Belizna C, et al. Immunomodulatory therapy for the management of severe COVID-19. Beyond the anti-viral therapy: A comprehensive review. Autoimmun Rev. 2020;19(7):102569. doi: 10.1016/j.autrev.2020.102569
- Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet Lond Engl. 2020;395(10234):1417–1418. doi: 10.1016/S0140-6736(20)30937-5
- Bikdeli B, Madhavan MV, Jimenez D, et al. COVID-19 and thrombotic or thromboembolic disease: Implications for prevention, antithrombotic therapy, and follow-up: JACC state-of-the-art review. J Am Coll Cardiol. 2020;75(23):2950–2973. doi: 10.1016/j.jacc.2020.04.031
- Choudry FA, Hamshere SM, Rathod KS, et al. High thrombus burden in patients with Covid-19 presenting with ST-segment elevation myocardial infarction. J Am Coll Cardiol. 2020;76(10):1168–1176. doi: 10.1016/j.jacc.2020.07.022
- Bangalore S, Hamshere SM, Rathod KS, et al. ST-Segment elevation in patients with Covid-19: A case series. N Engl J Med. 2020;382(25):2478–2480. doi: 10.1056/NEJMc2009020
- Guglin ME, Etuk A, Shah C, et al. Fulminant myocarditis and cardiogenic shock following COVID-19 infection versus COVID-19 vaccination: A systematic literature review. J Clin Med. 2023;12(5):1849. doi: 10.3390/jcm12051849
- Wang D, Hu B, Hu C, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020;323(11):1061–1069. doi: 10.1001/jama.2020.1585
- Siripanthong B, Nazarian S, Muser D, et al. Recognizing COVID-19-related myocarditis: The possible pathophysiology and proposed guideline for diagnosis and management. Heart Rhythm. 2020;17(9):1463–1471. doi: 10.1016/j.hrthm.2020.05.001
- Peretto G, Sala S, Rizzo S, et al. Ventricular arrhythmias in myocarditis: Characterization and relationships with myocardial inflammation. J Am Coll Cardiol. 2020;75(9):1046–1057. doi: 10.1016/j.jacc.2020.01.036
- Peretto G, Sala S, Rizzo S, et al. Arrhythmias in myocarditis: State of the art. Heart Rhythm. 2019;16(5):793–801. doi: 10.1016/j.hrthm.2018.11.024
- Chen L, Li X, Chen M, et al. The ACE2 expression in human heart indicates new potential mechanism of heart injury among patients infected with SARS-CoV-2. Cardiovasc Res. 2020;116(6):1097–1100. doi: 10.1093/cvr/cvaa078
- Asimaki A, Tandri H, Duffy ER, et al. Altered desmosomal proteins in granulomatous myocarditis and potential pathogenic links to arrhythmogenic right ventricular cardiomyopathy. Circ Arrhythm Electrophysiol. 2011;4(5):743–752. doi: 10.1161/CIRCEP.111.964890
- Gemayel C, Pelliccia A, Thompson PD. Arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol. 2001;38(7):1773–1781. doi: 10.1016/s0735-1097(01)01654-0
- Coomes EA, Haghbayan H. Interleukin-6 in Covid-19: A systematic review and meta-analysis. Rev Med Virol. 2020;30(6):1–9. doi: 10.1002/rmv.2141
- Modica G, Bianco M, Sollazzo F, et al. Myocarditis in athletes recovering from COVID-19: A systematic review and meta-analysis. Int J Environ Res Public Health. 2022;19(7):4279. doi: 10.3390/ijerph19074279
- Eichhorn C, Biere L, Schnell F, et al. Myocarditis in athletes is a challenge: Diagnosis, risk stratification, and uncertainties. JACC Cardiovasc Imaging. 2020;13(2):494–507. doi: 10.1016/j.jcmg.2019.01.039
- Azevedo RB, Botelho BG, de Hollanda G, et al. Covid-19 and the cardiovascular system: A comprehensive review. J Hum Hypertens. 2021;35(1):4–11. doi: 10.1038/s41371-020-0387-4
- Klok FA, Kruip MJ, van der Meer HJ, et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res. 2020;(191):145–147. doi: 10.1016/j.thromres.2020.04.013
- Guo T, Fan Y, Chen M, et al. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5(7):811–818. doi: 10.1001/jamacardio.2020.1017
- Larina OM. Cardiac magnetic resonance imaging in the diagnosis of acute myocarditis: A clinical case and review of the literature. Bulletin Radiol Radiol. 2014;(5):54–59. (In Russ).
- Arutyunov GB, Paleev FN, Moiseeva OM. Myocarditis in adults. Clinical recommendations 2020. Russ Cardiol J. 2021;26(11):4790. (In Russ). doi: 10.15829/1560-4071-2021-4790
- Friedrich MG, Sechtem U, Schulz-Menger J, et al. Cardiovascular magnetic resonance in myocarditis: A JACC white paper. J Am Coll Cardiol. 2009;53(17):1475–1487. doi: 10.1016/j.jacc.2009.02.007
- Tijmes SF, Thavendiranathan P, Udell JA, et al. Cardiac MRI assessment of nonischemic myocardial inflammation: State of the art review and update on myocarditis associated with COVID-19 Vaccination Radiol Cardiothorac Imaging. 2021;3(6):e210252. doi: 10.1148/ryct.210252
- Srichai MB, Lim RP, Lath N, et al. Diagnostic performance of dark-blood T2-weighted CMR for evaluation of acute myocardial injury. Invest Radiol. 2013;48(1):24–31. doi: 10.1097/RLI.0b013e3182718672
- Galán-Arriola C, Lim RP, Lath N, et al. Serial magnetic resonance imaging to identify early stages of anthracycline-induced cardiotoxicity. J Am Coll Cardiol. 2019;73(7):779–791. doi: 10.1016/j.jacc.2018.11.046
- Blagova OV, Pavlenko EV, Varionchik NV, et al. Myocarditis as a natural phenomenon in patients with primary non-compact myocardium: Diagnosis, treatment and impact on outcomes // Russ J Cardiol. 2018;(2):44–52. (In Russ). doi: 10.15829/1560-4071-2018-2-44-52
- Caforio AL, Pankuweit S, Arbustini E, 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;34(33)2636–2648, 2648a–2648d. doi: 10.1093/eurheartj/eht210
- Cooper LT, Baughman KL, Feldman AM, 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;116(19):2216–2233. doi: 10.1161/CIRCULATIONAHA.107.186093
- Aretz HT. Myocarditis: The Dallas criteria. Hum Pathol. 1987;18(6):619–624. doi: 10.1016/s0046-8177(87)80363-5
- Dennert R, Crijns HJ, Heymans S. Acute viral myocarditis. Eur Heart J. 2008;29(17):2073–2082. doi: 10.1093/eurheartj/ehn296
- Zhang M, Tavora F, Zhang Y, et al. The role of focal myocardial inflammation in sudden unexpected cardiac and noncardiac deaths: A clinicopathological study. Int J Legal Med. 2013;127(1):131–138. doi: 10.1007/s00414-011-0634-x
- Titov VA, Ignatyeva VS, Mitrofanova LB. Comparative study of informativeness of noninvasive methods for diagnosis of myocardial inflammatory diseases. Russ J Cardiol. 2018;23(2):53–59. (In Russ).
- Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet Lond Engl. 2020;395(10229):1054–1062. doi: 10.1016/S0140-6736(20)30566-3
- Mehta P, McAuley DF, Brown M, et al. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet Lond Engl. 2020;395(10229):1033–1034. doi: 10.1016/S0140-6736(20)30628-0
- Castiello T, Georgiopoulos G, Finocchiaro G, et al. COVID-19 and myocarditis: A systematic review and overview of current challenges. Heart Fail Rev. 2022;27(1):251–261. doi: 10.1007/s10741-021-10087-9
- Mele D, Flamigni F, Rapezzi C, et al. Myocarditis in COVID-19 patients: Current problems. Intern Emerg Med. 2021;16(5):1123–1129. doi: 10.1007/s11739-021-02635-w
- Halushka MK, Vander Heide RS. Myocarditis is rare in COVID-19 autopsies: Cardiovascular findings across 277 postmortem examinations. Cardiovasc Pathol. 2021;(50):107300. doi: 10.1016/j.carpath.2020.107300
- Huang L, Zhao P, Tang D, et al. Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging. 2020;13(11):2330–2339. doi: 10.1016/j.jcmg.2020.05.004
- Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020;5(11):1265–1273. doi: 10.1001/jamacardio.2020.3557
- Blanco-Domínguez R, Sánchez-Díaz R, de la Fuente H, et al. A novel circulating MicroRNA for the detection of acute myocarditis. N Engl J Med. 2021;384(21):2014–2027. doi: 10.1056/NEJMoa2003608
- Tan L, Wang Q, Zhang D, et al. Lymphopenia predicts disease severity of COVID-19: A descriptive and predictive study. Signal Transduct Target Ther. 2020;5(1):33. doi: 10.1038/s41392-020-0148-4
- Xu Z, Shi L, Wang Y, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8(4):420–422. doi: 10.1016/S2213-2600(20)30076-X
- Kawakami R, Sakamoto A, Kawai K, et al. Pathological evidence for SARS-CoV-2 as a cause of myocarditis. J Am Coll Cardiol. 2021;77(3):314–325. doi: 10.1016/j.jacc.2020.11.031
- Baden LR, El Sahly HM, Essink B, et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 2021;384(5):403–416. doi: 10.1056/NEJMoa2035389
- Logunov DY, Dolzhikova IV, Shcheblyakov DV, et al. Safety and efficacy of an rAd26 and rAd5 vector-based heterologous prime-boost COVID-19 vaccine: An interim analysis of a randomised controlled phase 3 trial in Russia. Lancet. 2021;397(10275):671–681. doi: 10.1016/S0140-6736(21)00234-8
- Polack FP, Thomas SJ, Kitchin N, et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med. 2020;383(27):2603–2615. doi: 10.1056/NEJMoa2034577
- Voysey M, Clemens SA, Madhi SA, et al. Safety and efficacy of the ChAdOx1 nCoV-19 vaccine (AZD1222) against SARS-CoV-2: An interim analysis of four randomised controlled trials in Brazil, South Africa, and the UK. Lancet. 2021;397(10269):99–111. doi: 10.1016/S0140-6736(20)32661-1
- Shiravi AA, Ardekani A, Sheikhbahaei E, et al. Cardiovascular complications of SARS-CoV-2 vaccines: An overview. Cardiol Ther. 2021;11(1):13–21. doi: 10.1007/s40119-021-00248-0
- Watad A, De Marco G, Mahajna H, et al. Immune-Mediated disease flares or new-onset disease in 27 subjects following mRNA/DNA SARS-CoV-2 Vaccination: 5. Vaccines. 2021;9(5):435. doi: 10.3390/vaccines9050435
- Albert E, Aurigemma G, Saucedo J, et al. Myocarditis following COVID-19 vaccination. Radiol Case Rep. 2021;16(8):2142–2145. doi: 10.1016/j.radcr.2021.05.033
- Mevorach D, Anis E, Cedar N, et al. Myocarditis after BNT162b2 mRNA vaccine against Covid-19 in Israel. N Engl J Med. 2021;385(23):2140–2149. doi: 10.1056/NEJMoa2109730
- Witberg G, Barda N, Hoss S, et al. Myocarditis after Covid-19 vaccination in a large health care organization. N Engl J Med. 2021;385(23):2132–2139. doi: 10.1056/NEJMoa2110737
- Barda N, Dagan N, Ben-Shlomo Y, et al. Safety of the BNT162b2 mRNA Covid-19 vaccine in a nationwide setting. N Engl J Med. 2021;385(12):1078–1090. doi: 10.1056/NEJMoa2110475