Combined Heart Injuries on the Data of Contrast-Enhanced Cardiac Magnetic Resonance Imaging in Patients With Post-Covid Syndrome

Aim      Prospective assessment of the nature of cardiac injury in patients with post-COVID syndrome according to contrast-enhanced MRI in routine clinical practice.

Material and methods  106 previously unvaccinated patients were evaluated. 62 (58.5%) of them were women with complaints that persisted after COVID-19 (median age, 57.5 [49; 64] years). In addition to standard indexes, markers of inflammation and myocardial injury were determined, and cardiac contrast-enhanced MRI was performed in each patient.

Results The median time from the onset of COVID-19 to cardiac MRI was 112.5 [75; 151] days. The nature of cardiac injury according to MRI in patients with post-COVID syndrome was complex and included a decrease in left ventricular (LV) and right ventricular ejection fraction, pericardial effusion, and pathological foci of late and early contrast enhancement at various locations. In 29 (27.4%) cases, there was a combination of any two signs of heart injury. In 28 (26.4%) patients with focal myocardial injury during the acute phase of COVID-19, hydroxychloroquine and tocilizumab were administered significantly more frequently, but antiviral drugs were administered less frequently. The presence of focal myocardial injury was associated with pathological LV remodeling.

Conclusion      According to contrast-enhanced cardiac MRI, at least 27.4% of patients with post-COVID syndrome may have signs of cardiac injury in various combinations, and in 26.4% of cases, foci of myocardial injury accompanied by LV remodeling are detected. The nature of heart injury after COVID-19 depends on the premorbid background, characteristics of the course of the infectious process, and the type of prescribed therapy. An algorithm for evaluating patients with post-COVID syndrome is proposed.

1. Basso C, Leone O, Rizzo S, De Gaspari M, van der Wal AC, Aubry M-C et al. Pathological features of COVID-19-associated myocardial injury: a multicentre cardiovascular pathology study. European Heart Journal. 2020;41(39):3827–35. DOI: 10.1093/eurheartj/ehaa664

2. Kogan E.A., Berezovskiy Yu.S., Blagova O.V., Kukleva A.D., Bogacheva G.A., Kurilina E.V. et al. Miocarditis in Patients with COVID-19 Confirmed by Immunohistochemical. Kardiologiia. 2020;60(7):4–10. DOI: 10.18087/cardio.2020.7.n1209

3. Hendren NS, Drazner MH, Bozkurt B, Cooper LT. Description and Proposed Management of the Acute COVID-19 Cardiovascular Syndrome. Circulation. 2020;141(23):1903–14. DOI: 10.1161/CIRCULATIONAHA.120.047349

4. Kawakami R, Sakamoto A, Kawai K, Gianatti A, Pellegrini D, Nasr A et al. Pathological Evidence for SARS-CoV-2 as a Cause of Myocarditis. Journal of the American College of Cardiology. 2021;77(3):314–25. DOI: 10.1016/j.jacc.2020.11.031

5. NICE. COVID-19 rapid guideline: managing the long-term effects of COVID-19. -London: National Institute for Health and Care Excellence;2020. ISBN 978-1-4731-3943-5

6. Raman B, Bluemke DA, Lüscher TF, Neubauer S. Long COVID: postacute sequelae of COVID-19 with a cardiovascular focus. European Heart Journal. 2022;43(11):1157–72. DOI: 10.1093/eurheartj/ehac031

7. Gluckman TJ, Bhave NM, Allen LA, Chung EH, Spatz ES, Ammirati E et al. 2022 ACC Expert Consensus Decision Pathway on Cardiovascular Sequelae of COVID-19 in Adults: Myocarditis and Other Myocardial Involvement, Post-Acute Sequelae of SARS-CoV-2 Infection, and Return to Play. Journal of the American College of Cardiology. 2022;79(17):1717–56. DOI: 10.1016/j.jacc.2022.02.003

8. Xie Y, Xu E, Bowe B, Al-Aly Z. Long-term cardiovascular outcomes of COVID-19. Nature Medicine. 2022;28(3):583–90. DOI: 10.1038/s41591-022-01689-3

9. Abbasi J. The COVID Heart—One Year After SARS-CoV-2 Infection, Patients Have an Array of Increased Cardiovascular Risks. JAMA. 2022;327(12):1113–4. DOI: 10.1001/jama.2022.2411

10. Huang L, Zhao P, Tang D, Zhu T, Han R, Zhan C et al. Cardiac Involvement in Patients Recovered From COVID-2019 Identified Using Magnetic Resonance Imaging. JACC: Cardiovascular Imaging. 2020;13(11):2330–9. DOI: 10.1016/j.jcmg.2020.05.004

11. Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J et al. Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From Coronavirus Disease 2019 (CO VID-19). JAMA Cardiology. 2020;5(11):1265–73. DOI: 10.1001/jamacardio.2020.3557

12. Eiros R, Barreiro-Pérez M, Martín-García A, Almeida J, Villacorta E, Pérez-Pons A et al. Pericardial and myocardial involvement after SARS-CoV-2 infection: a cross-sectional descriptive study in healthcare workers. Revista Española de Cardiología (English Edition). 2022;75(9):734–46. DOI: 10.1016/j.rec.2021.11.001

13. Rajpal S, Tong MS, Borchers J, Zareba KM, Obarski TP, Simonetti OP et al. Cardiovascular Magnetic Resonance Findings in Competitive Athletes Recovering From COVID-19 Infection. JAMA Cardiology. 2021;6(1):116–8. DOI: 10.1001/jamacardio.2020.4916

14. Dennis A, Wamil M, Alberts J, Oben J, Cuthbertson DJ, Wootton D et al. Multiorgan impairment in low-risk individuals with post-COVID-19 syndrome: a prospective, community-based study. BMJ Open. 2021;11(3):e048391. DOI: 10.1136/bmjopen-2020-048391

15. Kotecha T, Knight DS, Razvi Y, Kumar K, Vimalesvaran K, Thornton G et al. Patterns of myocardial injury in recovered troponin-positive COVID-19 patients assessed by cardiovascular magnetic resonance. European Heart Journal. 2021;42(19):1866–78. DOI: 10.1093/eurheartj/ehab075

16. Daniels CJ, Rajpal S, Greenshields JT, Rosenthal GL, Chung EH, Terrin M et al. Prevalence of Clinical and Subclinical Myocarditis in Competitive Athletes With Recent SARS-CoV-2 Infection: Results From the Big Ten COVID-19 Cardiac Registry. JAMA Cardiology. 2021;6(9):1078–87. DOI: 10.1001/jamacardio.2021.2065

17. Singh T, Kite TA, Joshi SS, Spath NB, Kershaw L, Baker A et al. MRI and CT coronary angiography in survivors of COVID-19. Heart. 2022;108(1):46–53. DOI: 10.1136/heartjnl-2021-319926

18. Hanneman K, Houbois C, Schoffel A, Gustafson D, Iwanochko RM, Wintersperger BJ et al. Combined Cardiac Fluorodeoxyglucose–Positron Emission Tomography/Magnetic Resonance Imaging Assessment of Myocardial Injury in Patients Who Recently Recovered From COVID-19. JAMA Cardiology. 2022;7(3):298–308. DOI: 10.1001/jamacardio.2021.5505

19. Morrow AJ, Sykes R, McIntosh A, Kamdar A, Bagot C, Bayes HK et al. A multisystem, cardio-renal investigation of post-COVID-19 illness. Nature Medicine. 2022;28(6):1303–13. DOI: 10.1038/s41591-022-01837-9

20. Giustino G, Croft LB, Stefanini GG, Bragato R, Silbiger JJ, Vicenzi M et al. Characterization of Myocardial Injury in Patients With COVID-19. Journal of the American College of Cardiology. 2020;76(18):2043–55. DOI: 10.1016/j.jacc.2020.08.069

21. Szekely Y, Lichter Y, Taieb P, Banai A, Hochstadt A, Merdler I et al. Spectrum of Cardiac Manifestations in COVID-19: A Systematic Echocardiographic Study. Circulation. 2020;142(4):342–53. DOI: 10.1161/CIRCULATIONAHA.120.047971

22. Dweck MR, Bularga A, Hahn RT, Bing R, Lee KK, Chapman AR et al. Global evaluation of echocardiography in patients with COVID-19. European Heart Journal Cardiovascular Imaging. 2020;21(9):949–58. DOI: 10.1093/ehjci/jeaa178

23. Soulat-Dufour L, Fauvel C, Weizman O, Barbe T, Pezel T, Mika D et al. Prognostic value of right ventricular dilatation in patients with COVID-19: a multicentre study. European Heart Journal – Cardiovascular Imaging. 2022;23(4):569–77. DOI: 10.1093/ehjci/jeab067

24. Ferreira VM, Schulz-Menger J, Holmvang G, Kramer CM, Carbone I, Sechtem U et al. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation. Journal of the American College of Cardiology. 2018;72(24):3158–76. DOI: 10.1016/j.jacc.2018.09.072

25. Petersen SE, Khanji MY, Plein S, Lancellotti P, Bucciarelli-Ducci C. European Association of Cardiovascular Imaging expert consensus paper: a comprehensive review of cardiovascular magnetic resonance normal values of cardiac chamber size and aortic root in adults and recommendations for grading severity. European Heart Journal - Cardiovascular Imaging. 2019;20(12):1321–31. DOI: 10.1093/ehjci/jez232

26. Peretto G, Villatore A, Rizzo S, Esposito A, De Luca G, Palmisano A et al. The Spectrum of COVID-19-Associated Myocarditis: A Patient-Tailored Multidisciplinary Approach. Journal of Clinical Medicine. 2021;10(9):1974. DOI: 10.3390/jcm10091974

27. Blagova O.V., Kogan E.A., Lutokhina Yu.A., Kukleva A.D., Ainetdinova D.H., Novosadov V.M. et al. Subacute and chronic post-covid myoendocarditis: clinical presentation, role of coronavirus persistence and autoimmune mechanisms. Kardiologiia. 2021;61(6):11–27. DOI: 10.18087/cardio.2021.6.n1659

28. Fox SE, Falgout L, Vander Heide RS. COVID-19 myocarditis: quantitative analysis of the inflammatory infiltrate and a proposed mechanism. Cardiovascular Pathology. 2021;54:107361. DOI: 10.1016/j.carpath.2021.107361

29. Blagova O.V., Varionchik N.V., Zaydenov V.A., Savina P.O., Sarkisova N.D. Anticardiac antibodies in patients with severe and moderate COVID-19 (correlations with the clinical performance and prognosis). Russian Journal of Cardiology. 2020;25(11):85–97. DOI: 10.15829/29/1560-4071-2020-4054