Structural reorganization of the myocardium in COVID-19

I n t r o d u c t i o n. The development of a novel coronavirus infection (COVID-19) is not limited to respiratory damage. Adverse outcomes in patients with COVID-19 may be associated with cardiac damage.

A i m. Study of the structural changes in the myocardium and the molecular biological characteristics of the endothelium of blood capillaries in severe forms of COVID-19.

M a t e r i a l s a n d m e t h o d s. An analysis of the medical documentation – inpatient records of 73 deceased with bilateral multisegmental viral pneumonia caused by the SARS-CoV-2 virus, as well as data from 43 autopsies of patients who died (sudden coronary death) between September 2020 to July 2021, was performed. An assessment of some clinical and laboratory data (degree of lung damage; levels of C-reactive protein, troponin I, D-dimer; left ventricular ejection fraction, etc.), structural changes in the myocardium and molecular biological characteristics (CD31, CD34) of the endothelium of blood capillaries in severe forms of COVID-19 was carried out.

R e s u l t s. The analysis of clinical and laboratory data has shown that a decrease in myocardial contractility in severe forms of COVID-19 due to an extensive lung damage was accompanied by an increase in the level of C-reactive protein, D-dimer, troponin I and indicated acute myocardial damage. According to electrocardiography (ECG) monitoring and echocardiography, repolarization disorders and a decrease in myocardial contractility were noted, which was accompanied by a decrease in ejection fraction by 32%. In more than 70% of cases, various arrhythmic disorders (atrial fibrillation, etc.) were observed during ECG.

Light microscopy revealed the presence of sludge phenomenon, as well as swelling, desquamation and proliferation of the endothelium of blood capillaries, formation of diapedetic and focal hemorrhages, in some places leukocyte margination and their migration beyond vascular bed. Fibrin masses were observed in the lumen of blood vessels. Polarization microscopy, along with contractures in cardiomyocytes, revealed groups of cells with myocytolysis and primary granularity. In all observations, lipofuscinosis of cardiomyocytes was detected. Immunohistochemical examination showed a marked decrease in the expression level of CD31 (PECAM-1) and CD34 proteins – markers of blood vessels.

C o n c l u s i o n. The performed clinical and morphological analysis in severe forms of COVID-19 allowed us to obtain new data on degenerative changes in the myocardium and the structure of endothelial cells of blood capillaries, which can be used as a basis for methodological approaches to studying the mechanisms of development of heart failure in a novel coronavirus infection.

1. 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.

2. Italia L., Tomasoni D., Bisegna S. et al. COVID-19 and heart failure: from epidemiology during the pandemic to myocardial injury, myocarditis, and heart failure sequelae. Front. Cardiovasc. Med. 2021;8:713560. DOI: 10.3389/fcvm.2021.713560.

3. Liu P.P., Blet A., Smyth D., Li H. The science underlying COVID-19: implications for the cardiovascular system. Circulation. 2020;142(1):68-78. DOI: 10.1161/CIRCULATIONAHA.120.047549.

4. 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.

5. Rybakova M.G., Karev V.E., Kuznetsova I.A. Anatomical pathology of novel coronavirus (COVID-19) infection. First impressions. Archive of Pathology. 2020;82(5):5-15. DOI: 10.17116/patol12020820515. (In Russ.)

6. Arévalos V., Ortega-Paz L., Rodríguez-Arias J.J. et al. Myocardial injury in COVID-19 patients: association with inflammation, coagulopathy and in-hospital prognosis. J. Clin. Med. 2021;10(10):2096. DOI: 10.3390/jcm10102096.

7. Basso C., Leone O., Rizzo S. et al. Pathological features of COVID-19-associated myocardial injury: a multicentre cardiovascular pathology study. Eur. Heart J. 2020; 41(39):3827-3835. DOI: 10.1093/eurheartj/ehaa66431.

8. Roquetaillade C., Chousterman B.G., Tomasoni D. et al. Unusual arterial thrombotic events in Covid-19 patients. Int. J. Cardiol. 2021;323:281-284. DOI: 10.1016/j.ijcard.2020.08.103.

9. Ackermann M., Verleden S.E., Kuehnel M. et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in COVID-19. N. Engl. J. Med. 2020;383(2):120-128. DOI: 10.1056/NEJMoa2015432.

10. Goshua G., Pine A.B., Meizlish M.L. et al. Endotheliopathy in COVID-19-associated coagulopathy: evidence from a single-centre, cross-sectional study. Lancet Haematol. 2020;7(8):e575-e582. DOI: 10.1016/S2352-3026(20)30216-7.

11. Iba T., Connors J.M., Levy J.H. The coagulopathy, endotheliopathy, and vasculitis of COVID-19. Inflamm. Res. 2020;69(12):1181-1189. DOI: 10.1007/s00011-020-01401-6.

12. Xu S.W., Ilyas I., Weng J.P. Endothelial dysfunction in COVID-19: an overview of evidence, biomarkers, mechanisms and potential therapies. Acta Pharmacol. Sin. 2023;44(4):695-709. DOI: 10.1038/s41401-022-00998-0.

13. Saenko A.V. (1998). Assessment of fibrin to determine the duration of mechanical injury. In Current Issues in the Theory and Practice of Forensic Medicine. Мoscow. P. 71–72. (In Russ.)

14. Guervilly C., Burtey S., Sabatier F. et al. Circulating endothelial cells as a marker of endothelial injury in severe COVID-19. J. Infect. Dis. 2020;222(11):1789-1793. DOI: 10.1093/infdis/jiaa528.

15. Mancuso P., Gidaro A., Gregato G. et al. Circulating endothelial progenitors are increased in COVID-19 patients and correlate with SARS-CoV-2 RNA in severe cases. J. Thromb. Haemost. 2020;18(10):2744-2750. DOI: 10.1111/jth.15044.