Diagnosis of non-ischemic myocardial injury in acute COVID-19 cardiovascular syndrome


DOI: https://dx.doi.org/10.18565/therapy.2022.3.81-90

Oleynikov V.E., Donetskaya N.A., Vdovkin A.V., Avdeeva I.V., Sretenskaya E.A., Borisova N.A.

1) Penza State University; 2) N.N. Burdenko Penza Regional Clinical Hospital
Abstract. It is proposed to designate the cardiological manifestations of a new coronavirus infection with the term «acute COVID-19-associated cardiovascular syndrome». The syndrome is characterized by acute myocardial damage with decreased left ventricular ejection fraction in the absence of obstructive coronary arteries failure. The main manifestations of acute myocardial injury in this case are myocarditis and cytokine dysregulation, less often stress-induced cardiomyopathy. Still there are no clear explanations for the variability of manifestations, and there remains considerable uncertainty regarding the cause of acute myocardial injury during coronavirus infection in patients without coronary artery obstruction. Literature data on the diagnosis of myocardial damage against COVID- 19 background are collected in the current article. The literature was searched and analyzed for articles published up to November 2021 in MEDLINE databases. Inclusion criteria to this review were reports of myocardial injury diagnosis in patients with laboratory-confirmed infection who underwent comprehensive diagnostic studies, including cardiac MRI.

Literature


1. Huang C., Wang Y., Li X. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020; 395(10223): 497–506. https://dx.doi.org/10.1016/S0140-6736(20)30183.


2. Hendren N.S., Drazner M.H., Bozkurt B. et al. Description and proposed management of the acute COVID-19 cardiovascular syndrome. Circulation. 2020; 141(23): 1903–14. https://dx.doi.org/10.1161/ CIRCULATIONAHA.120.047349.


3. Zou F., Qian Z., Wang Y. et al. Cardiac injury and COVID-19: A systematic review and meta-analysis. CJC Open. 2020; 2(5): 386–94. https://dx.doi.org/10.1016/j.cjco.2020.06.010.


4. Rathore S.S., Rojas G.A., Sondhi M. et al. Myocarditis associated with Covid-19 disease: A systematic review of published case reports and case series. Int J Clin Pract. 2021; 75(11): e14470. https://dx.doi.org/10.1111/ijcp.14470.


5. Halushka M.K., Vander Heide R.S. Myocarditis is rare in COVID-19 autopsies: Cardiovascular findings across 277 postmortem examinations. Cardiovasc Pathol. 2021; 50: 107300. https://dx.doi.org/10.1016/j.carpath.2020.107300.


6. Coyle J., Igbinomwanhia E., Sanchez-Nadales A. et al. A recovered case of COVID-19 myocarditis and ARDS treated with corticosteroids, tocilizumab, and experimental AT-001. JACC Case Rep. 2020; 2(9): 1331–36. https://dx.doi.org/10.1016/j.jaccas.2020.04.025.


7. Ammirati E., Frigerio M., Adler E.D. et al. Management of acute myocarditis and chronic inflammatory cardiomyopathy: An expert consensus document. Circ Heart Fail. 2020; 13(11): e007405. https://dx.doi.org/10.1161/CIRCHEARTFAILURE.120.007405.


8. Hoffmann M., Kleine-Weber H., Schroeder S. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020; 181(2): 271–80.e8. https://dx.doi.org/10.1016/j.cell.2020.02.052.


9. Tikellis C., Thomas M.C. Angiotensin-converting enzyme 2 (ACE2) is a key modulator of the renin angiotensin system in health and disease. Int J Pept. 2012; 2012: 256294. https://dx.doi.org/10.1155/2012/256294.


10. Tavazzi G., Pellegrini C., Maurelli M. et al. Myocardial localization of coronavirus in COVID-19 cardiogenic shock. Eur J Heart Fail. 2020; 22(5): 911–15. https://dx.doi.org/10.1002/ejhf.1828.


11. Sala S., Peretto G., Gramegna M. et al. Acute myocarditis presenting as a reverse takotsubo syndrome in a patient with SARS-CoV-2 respiratory infection. Eur Heart J. 2020; 41(19): 1861–62. https://dx.doi.org/10.1093/eurheartj/ehaa286.


12. 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): 2440–47. https://dx.doi.org/10.1002/ehf2.12805.


13. Wenzel P., Kopp S., Gobel S. et al. Evidence of SARS-CoV-2 mRNA in endomyocardial biopsies of patients with clinically suspected myocarditis tested negative for COVID-19 in nasopharyngeal swab. Cardiovasc Res. 2020; 116(10): 1661–63. https://dx.doi.org/10.1093/cvr/cvaa160.


14. Van Linthout S., Klingel K., Tschope C. SARS-CoV-2-related myocarditis-like syndromes Shakespeare’s question: What’s in a name? Eur J Heart Fail. 2020; 22(6): 922–25. https://dx.doi.org/10.1002/ejhf.1899.


15. Hendren N.S., Grodin J.L., Drazner M.H. Unique patterns of cardiovascular involvement in coronavirus disease-2019. J Card Fail. 2020; 26(6): 466–69. https://dx.doi.org/10.1016/j.cardfail.2020.05.006.


16. Mehta P., McAuley D.F., Brown M. et al. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet. 2020; 395(10229): 1033–34. https://dx.doi.org/10.1016/S0140-6736(20)30628-0.


17. Zhou F., Yu T., Du R. et al. Clinical course and risk factors for mortality of adult in patients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet. 2020; 395(10229): 1054–62. https://dx.doi.org/10.1016/S0140-6736(20)30566-3.


18. Zeng J.H., Liu Y.X., Yuan J. et al. First case of COVID-19 complicated with fulminant myocarditis: A case report and insights. Infection. 2020; 48(5): 773–77. https://dx.doi.org/10.1007/s15010-020-01424-5.


19. Komarowska I., Coe D., Wang G. et al. Hepatocyte growth factor receptor c-met instructs T cell cardiotropism and promotes T cell migration to the heart via autocrine chemokine release. Immunity. 2015; 42(6): 1087–99. https://dx.doi.org/10.1016/j.immuni.2015.05.014.


20. Esfandiarei M., McManus B.M. Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol. 2008; 3: 127–55. https://dx.doi.org/10.1146/annurev.pathmechdis.3.121806.151534.


21. Коган Е.А., Березовский Ю.С., Благова О.В. с соавт. Миокардит у пациентов с COVID-19, подтвержденный результатами иммуногистохимического исследования. Кардиология. 2020; 7: 4–10. [Kogan E.A., Berezovskiy Yu.S., Blagova O.V. et al. Miocarditis in patients with COVID-19 confirmed by immunohistochemical. Kardiologiya = Cardiology. 2020; 7: 4–10 (In Russ.)]. https://dx.doi.org/10.18087/cardio.2020.7.n1209.


22. Trachtenberg B.H., Hare J.M. Inflammatory cardiomyopathic syndromes. Circ Res. 2017; 121(7): 803–18. https://dx.doi.org/10.1161/CIRCRESAHA.117.310221.


23. Tersalvi G., Vicenzi M., Calabretta D. et al. Elevated troponin in patients with coronavirus disease 2019: possible mechanisms. J Card Fail. 2020; 26(6): 470–75. https://dx.doi.org/10.1016/j.cardfail.2020.04.009.


24. Ruan Q., Yang K., Wang W. et al. Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med. 2020; 46(5): 846–48. https://dx.doi.org/10.1007/s00134-020-05991-x.


25. Bearse M., Hung Y.P., Krauson A.J. et al. Factors associated with myocardial SARS-CoV-2 infection, myocarditis, and cardiac inflammation in patients with COVID-19. Mod Pathol. 2021; 34(7): 1345–57. https://dx.doi.org/10.1038/s41379-021-00790-1.


26. Inciardi R.M., Lupi L., Zaccone G. et al. Cardiac involvement in a patient with coronavirus disease 2019 (COVID-19). JAMA Cardiol. 2020; 5(7): 819–24. https://dx.doi.org/10.1001/jamacardio.2020.1096.


27. Wang D., Li S., Jiang J. et al. Section of Precision Medicine Group of Chinese Society of Cardiology; Editorial Board of Chinese Journal of Cardiology; Working Group of Adult Fulminant Myocarditis. Chinese Society of Cardiology expert consensus statement on the diagnosis and treatment of adult fulminant myocarditis. Sci China Life Sci. 2019; 62(2): 187–202. https://dx.doi.org/10.1007/s11427-018-9385-3.


28. Ойноткинова О.Ш., Масленникова О.М., Ларина В.Н. с соавт. Согласованная экспертная позиция по диагностике и лечению фульминантного миокардита в условиях пандемии COVID-19. Академия медицины и спорта. 2020; 2: 28–40. [Oynotkinova O.Sh., Maslennikova O.M., Larina V.N. et al. Expert consensus statement on the diagnosis and treatment of fulminant myocarditis in the context of the COVID-19 pandemic. Akademiya meditsiny i sporta = Academy of Medicine and Sports. 2020; 2: 28–40 (In Russ.)]. https://dx.doi.org/10.15829/2712-7567-2020-2-13.


29. Kociol R.D., Cooper L.T., Fang J.C. et al. American Heart Association Heart Failure and Transplantation Committee of the Council on Clinical Cardiology. Recognition and initial management of fulminant myocarditis: A scientific statement from the American Heart Association. Circulation. 2020; 141(6): e69–e92. https://dx.doi.org/10.1161/CIR.0000000000000745.


30. Peltzer B., Manocha K.K., Ying X. et al. Outcomes and mortality associated with atrial arrhythmias among patients hospitalized with COVID-19. J Cardiovasc Electrophysiol. 2020; 31(12): 3077–85. https://dx.doi.org/10.1111/jce.14770.


31. Fine N.M. Giant cell myocarditis: Still the deadly giant. JACC Case Rep. 2020; 2(10): 1489–91. https://dx.doi.org/10.1016/j.jaccas.2020.07.001.


32. Mele D., Flamigni F., Claudio Rapezzi C. et al. Myocarditis in COVID-19 patients: Current problems. Intern Emerg Med. 2021; 16(5): 1123–29. https://dx.doi.org/10.1007/s11739-021-02635-w.


33. Paul J.F., Charles P., Richaud C. et al. Myocarditis revealing COVID-19 infection in a young patient. Eur Heart J Cardiovasc Imaging. 2020; 21(7): 776. https://dx.doi.org/10.1093/ehjci/jeaa107.


34. Murad M.H., Sultan S., Haffar S., Bazerbachi F. Methodological quality and synthesis of case series and case reports. BMJ Evid Based Med. 2018; 23(2): 60–63. https://dx.doi.org/10.1136/bmjebm-2017-110853.


35. Kim I.C., Kim J.Y., Kim H.A. et al. COVID-19-related myocarditis in a 21-year-old female patient. Eur Heart J. 2020; 41(19): 1859. https://dx.doi.org/10.1093/eurheartj/ehaa288.


36. Jaiswal V., Sarfraz Z., Sarfraz A. et al. COVID-19 infection and myocarditis: A state-of-the-art systematic review. J Prim Care Community Health. 2021; 12(6): 215013272110568. https://dx.doi.org/10.1177/21501327211056800.


37. Благова О.В., Вариончик Н.В., Зайденов В.А. с соавт. Оценка уровня антикардиальных антител у больных с тяжелым и среднетяжелым течением COVID-19 (корреляции с клинической картиной и прогнозом). Российский кардиологический журнал. 2020; 11: 4054. [Blagova O.V., Varionchik N.V., Zaydenov V.A. et al. Anticardiac antibodies in patients with severe and moderate COVID-19 (correlations with the clinical performance and prognosis). Rossiyskiy kardiologicheskiy zhurnal= Russian Journal of Cardiology. 2020; 11: 4054 (In Russ.)]. https://dx.doi.org/10.15829/1560-4071-2020-4054.


38. Xu Y., Qian Y., Qin Gu Q. et al. Relationship between D-dimer concentration and inflammatory factors or organ function in patients with coronavirus disease 2019. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 2020; 32(5): 559–63. https://dx.doi.org/10.3760/cma.j.cn121430-20200414-00518.


39. Gao L., Jiang D., Wen X.S. et al. Prognostic value of NT-proBNP in patients with severe COVID-19. Respir Res. 2020; 21(1): 83. https://dx.doi.org/10.1186/s12931-020-01352-w.


40. Imazio M., Klingel K., Kindermann I. et al. COVID-19 pandemic and troponin: Indirect myocardial injury, myocardial inflammation or myocarditis? Heart. 2020; 106(15): 1127–31. https://dx.doi.org/10.1136/heartjnl-2020-317186.


41. 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): 1463–71. https://dx.doi.org/10.1016/j.hrthm.2020.05.001.


42. Lauer B., Niederau C., Kuhl U. et al. Cardiac troponin T in patients with clinically suspected myocarditis. J Am Coll Cardiol. 1997; 30(5): 1354–59. https://dx.doi.org/10.1016/s0735-1097(97)00317-3.


43. Heymans S. Myocarditis and heart failure: Need for better diagnostic, predictive, and therapeutic tools. Eur Heart J. 2007; 28(11): 1279–80. https://dx.doi.org/10.1093/eurheartj/ehm111.


44. Auer J., Neuhierl F., Hetzmann Z. COVID-19-related fatal myocarditis in a 42-year-old female patient. Cardiol J. 2020; 27(5): 642–43. https://dx.doi.org/10.5603/CJ.2020.0155.


45. Sardari A., Tabarsi P., Borhany H. et al. Myocarditis detected after COVID-19 recovery. Eur Heart J Cardiovasc Imaging. 2021; 22(1): 131–32. https://dx.doi.org/10.1093/ ehjci/jeaa166.


46. Oberweis M.L., Codreanu A., Boehm W. et al. Pediatric life-threatening coronavirus disease 2019 with myocarditis. Pediatr Infect Dis J. 2020; 39(7): e147–e149. https://dx.doi.org/10.1097/INF.0000000000 002744.


47. Khatri A., Wallach F. Coronavirus disease 2019 (Covid-19) presenting as purulent fulminant myopericarditis and cardiac tamponade: A case report and literature review. Heart Lung. 2020; 49(6): 858–63. https://dx.doi.org/10.1016/j.hrtlng.2020.06.003.


48. De Vita S., Ippolito S., Caracciolo M.M. et al. Peripartum cardiomyopathy in a COVID-19-infected woman: Differential diagnosis with acute myocarditis – A case report from a Hub Institution during the COVID-19 outbreak. Echocardiography. 2020; 37(10): 1673–77. https://dx.doi.org/10.1111/echo.14873.


49. Garot J., Amour J., Pezel T. et al. SARS-CoV-2 fulminant myocarditis. JACC Case Rep. 2020; 2(9): 1342–46. https://dx.doi.org/10.1016/j.jaccas.2020.05.060.


50. Ezekowitz J.A., O’Meara E., McDonald M.A. et al. 2017 comprehensive update of the Canadian Cardiovascular Society guidelines for the management of heart failure. Can J Cardiol. 2017; 33(11): 1342–433. https://dx.doi.org/10.1016/j.cjca.2017.08.022.


51. Abdel-Aty H., Boye P., Zagrosek A. et al. Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol. 2005; 45(11): 1815–22. https://dx.doi.org/10.1016/j.jacc.2004.11.069.


52. Friedrich M.G., Sechtem U., Schulz-Menger J. et al. International Consensus Group on Cardiovascular Magnetic Resonance in Myocarditis. Cardiovascular magnetic resonance in myocarditis: A JACC White Paper. J Am Coll Cardiol. 2009; 53(17): 1475–87. https://dx.doi.org/10.1016/j.jacc.2009.02.007.


53. Friedrich M.G., Marcotte F. Cardiac magnetic resonance assessment of myocarditis. Circ Cardiovasc Imaging. 2013; 6(5): 833–39. https://dx.doi.org/10.1161/CIRCIMAGING.113.000416.


54. Han Y., Chen T., Bryant J. et al. J. Society for Cardiovascular Magnetic Resonance (SCMR) guidance for the practice of cardiovascular magnetic resonance during the COVID-19 pandemic. J Cardiovasc Magn Reson. 2020; 22(1): 26. https://dx.doi.org/10.1186/s12968-020-00628-w.


55. Luetkens J.A., Isaak A., Zimmer S. et al. Diffuse myocardial inflammation in COVID-19 associated myocarditis detected by multiparametric cardiac magnetic resonance imaging. Circ Cardiovasc Imaging. 2020; 13(5): e010897. https://dx.doi.org/10.1161/CIRCIMAGING.120.010897.


56. Hu H., Ma F., Wei X. et al. Coronavirus fulminant myocarditis treated with glucocorticoid and human immunoglobulin. Eur Heart J. 2021; 42(2): 206. https://dx.doi.org/10.1093/eurheartj/ehaa190.


57. Irabien-Ortiz A., Carreras-Mora J., Sionis A. et al. Fulminant myocarditis due to COVID-19. Rev Esp Cardiol. 2020; 73(6): 503–4. https://dx.doi.org/10.1016/j.rec.2020.04.005.


58. Caforio A.L., Pankuweit S., Arbustini E. et al. European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. 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): 2636–48, 2648a–2648d. https://dx.doi.org/10.1093/eurheartj/eht210.


59. Bozkurt B., Colvin M., Cook J. et al.; American Heart Association Committee on Heart Failure and Transplantation of the Council on Clinical Cardiology; Council on Cardiovascular Disease in the Young; Council on Cardiovascular and Stroke Nursing; Council on Epidemiology and Prevention; and Council on Quality of Care and Outcomes Research. Current diagnostic and treatment strategies for specific dilated cardiomyopathies: A scientific statement from the American Heart Association. Circulation. 2016; 134(23): e579–e646. https://dx.doi.org/10.1161/CIR.0000000000000455.


60. Арутюнов Г.П., Палеев Ф.Н., Моисеева О.М. с соавт. Миокардиты у взрослых. Клинические рекомендации 2020. Российский кардиологический журнал. 2021; 11: 4790. [Arutyunov G.P., Paleev F.N., Moiseeva O.M. et al. 2020 Clinical practice guidelines for myocarditis in adults. Rossiyskiy kardiologicheskiy zhurnal = Russian Journal of Cardiology. 2021; 11: 4790. (In Russ.)]. https://dx.doi.org/10.15829/1560-4071-2021-4790.


61. Sato H., Taiteishi H., Uchida T. et al. Takotsubo-type cardiomyopathy due to multivessel spasm. In: Kodama K., Haze K., Hon M. Clinical aspect of myocardial injury: from ischemia to heart failure. Tokyo: Kagakuhyouronsha. 1990; pp. 56–64.


62. Nef H.M., Mollmann H., Akashi Y.J. et al. Mechanisms of stress (takotsubo) cardiomyopathy. Nat Rev Cardiol. 2010; 7(4): 187–93. https://dx.doi.org/10.1038/nrcardio.2010.16.


63. Minhas A.S., Scheel P., Garibaldi B. et al. Takotsubo syndrome in the setting of COVID-19 infection. JACC Case Rep. 2020; 2(9):1321– 25. https://dx.doi.org/10.1016/j.jaccas.2020.04.023.


64. Dabbagh M.F., Aurora L., D’Souza P. et al. Cardiac tamponade secondary to COVID-19. JACC Case Rep. 2020; 2(9): 1326–30. https://dx.doi.org/10.1016/j.jaccas.2020.04.009.


65. Roca E., Lombardi C., Campana M. et al. Takotsubo syndrome associated with COVID-19. Eur J Case Rep Intern Med. 2020; 7(5): 001665. https://dx.doi.org/10.12890/2020_001665.


66. Solano-Lopez J., Sanchez-Recalde A., Zamorano J.L. SARS-CoV-2, a novel virus with an unusual cardiac feature: Inverted takotsubo syndrome. Eur Heart J. 2020; 41(32): 3106. https://dx.doi.org/10.1093/eurheartj/ehaa390.


67. Зелтынь-Абрамов Е.М., Белавина Н.И., Фролова Н.Ф. с соавт. Covid-19 ассоциированные поражения сердца у пациентов на программном гемодиализе. Серия клинических наблюдений и краткий обзор литературы. Нефрология и диализ. 2020; S: 21–32. [Zeltyn-Abramov E.M., Belavina N.I., Frolova N.F. et al. Covid-19 associated heart disease in patients on program hemodialysis. A series appears and a brief review of the literature. Nefrologiya i dializ = Nephrology and Dialysis. 2020; S: 21–32 (In Russ.)]. https://dx.doi.org/10.28996/2618-9801-2020-Special_Issue-21-32.


68. De Giorgi A., Fabbian F., Pala M. Takotsubo cardiomyopathy and acute infectious diseases: A mini-review of case reports. Angiology. 2015; 66(3): 257–61. https://dx.doi.org/10.1177/0003319714523673.


69. Bybee K.A., Kara T., Prasad A. et al. Systematic review: transient left ventricular apical ballooning: A syndrome that mimics ST-segment elevation myocardial infarction. Ann Intern Med. 2004; 141(11): 858–65. https://dx.doi.org/10.7326/0003- 4819-141-11-200412070-00010.


70. Kawai S., Kitabatake A., Tomoike H. Guidelines for diagnosis of takotsubo (ampulla) cardiomyopathy. Circ J. 2007; 71(6): 990–92. https://dx.doi.org/10.1253/circj.71.990.


71. Prasad A., Lerman A., Rihal C.S. Apical ballooning syndrome (Tako-Tsubo or stress cardiomyopathy): A mimic of acute myocardial infarction. Am Heart J. 2008; 155(3): 408–17. https://dx.doi.org/10.1016/j.ahj.2007.11.008.


72. Chadha S. «COVID-19 pandemic» anxiety induced takotsubo cardiomyopathy. QJM. 2020; 113(7): 488–90. https://dx.doi.org/10.1093/qjmed/hcaa135.


73. Meyer P., Degrauwe S., Delden C.V. et al. Typical takotsubo syndrome triggered by SARS-CoV-2 infection. Eur. Heart J. 2020; 41(19): 1860. https://dx.doi.org/10.1093/eurheartj/ehaa306.


74. Minhas A.S., Hughey A.B., Kolias T.J. Nationwide trends in reported incidence of takotsubo cardiomyopathy from 2006 to 2012. Am J Cardiol. 2015; 116(7): 1128–31. https://dx.doi.org/10.1016/j.amjcard.2015.06.042.


75. Scantlebury D.C., Prasad A. Diagnosis of Takotsubo cardiomyopathy. Circ J. 2014; 78(9): 2129–39. https://dx.doi.org/10.1253/circj.cj-14-0859.


76. Wan S.-H., Liang J.J. Takotsubo cardiomyopathy: etiology, diagnosis, and optimal management. Research Reports in Clinical Cardiology. 2014; 2014(5): 297–303. https://dx.doi.org/10.2147/RRCC.S46021.


77. Templin C., Ghadri J.R., Diekmann J. Clinical features and outcomes of takotsubo (stress) cardiomyopathy. N Engl J Med. 2015; 373(10): 929–38. https://dx.doi.org/10.1056/NEJMoa1406761.


78. Akashi Y.J., Tejima T., Sakurada H. et al. Left ventricular rupture associated with Takotsubo cardiomyopathy. Mayo Clin Proc. 2004; 79(6): 821–24. https://dx.doi.org/10.4065/79.6.821.


About the Autors


Valentin E. Oleynikov, Dr. med. habil., professor, head of the Department of therapy, Penza State University. Address: 440026, Penza, 28 Lermontova Str. E-mail: v.oleynikof@gmail.com. ORCID: https://orcid.org/0000-0002-7463-9259
Natalia A. Donetskaya, radiologist, head of the Department of radiation diagnostics, N.N. Burdenko Penza Regional Clinical Hospital. Address: 440026, Penza, 28 Lermontova Str. E-mail: otdelenield@yandex.ru
Alexander V. Vdovkin, radiologist of the Department of radiation diagnostics, N.N. Burdenko Penza Regional Clinical Hospital. Address: 440026, Penza, 28 Lermontova Str. E-mail: otdelenield@yandex.ru
Irina V. Avdeeva, PhD, associate professor of the Department of therapy, Penza State University. Address: 440026, Penza, 28 Lermontova Str. E-mail: eliseeva.iv1@gmail.com. ORCID: https://orcid.org/0000-0003-4266-5900
Ekaterina A. Sretenskaya, radiologist of the Department of radiation diagnostics, N.N. Burdenko Penza Regional Clinical Hospital. Address: 440026, Penza, 28 Lermontova Str. E-mail: otdelenield@yandex.ru
Natalya A. Borisova, PhD in Medicine, associate professor of the Department of therapy, Penza State University. Address: 440026, Penza, 28 Lermontova Str. E-mail: borisovi2000@yandex.ru.
ORCID: https://orcid.org/0000-0001-8218-9457


Similar Articles


Бионика Медиа