Structural and functional сhanges of the right ventricle in COVID-19 according to echocardiography

Authors: Golukhova E.Z.1, Slivneva I.V.1, Rybka M.M.1, Mamalyga M.L.1, Alekhin M.N.2, Klyuchnikov I.V.1, Antonova D.E.1, Marapov D.I.3, Volkovskaya I.V.1

Company: 1 Bakoulev National Medical Research Center for Cardiovascular Surgery, Moscow, 121552, Russian Federation 2 Central Clinical Hospital with a Polyclinic, Presidential Administration, Moscow, 121359, Russian Federation. 3 Department of Public Health, Economics and Health Management of the Kazan State Medical Academy Affiliate of the Russian Medical Academy of Continuing Professional Education, Kazan, 420012, Russian Federation.

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Type:  Original articles


For citation: Golukhova E.Z., Slivneva I.V., Rybka M.M., Mamalyga M.L., Alekhin M.N., Klyuchnikov I.V., Antonova D.E., Marapov D.I., Volkovskaya I.V. Structural and functional сhanges of the right ventricle in COVID-19 according to echocardiography. Creative Cardiology. 2020; 14 (3): 206–23 (in Russ.). DOI: 10.24022/1997-3187-2020-14-3-206-223

Received / Accepted:  10.08.2020 / 20.08.2020

Keywords: COVID-19 echocardiography right ventricle systolic function

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Objective. Comprehensive echocardiographic assessment of right ventricle (RV) dysfunction depending on the course of COVID-19.

Material and methods. A study of 109 patients with COVID-19. The patients were divided into 2 groups: group 1 – with a compensated state of COVID-19 (n=86) and group 2 – with a severe state, decompensated according to the right ventricular failure (n=23). All patients underwent a comprehensive echocardiographic examination at baseline, including tissue Doppler imaging (TDI) and speckle tracking echocardiography (STE). In group 2, parameters were assessed in dynamics (stage A – initially, stage B – disease progression according to computed tomography data). Hospitalization period from the onset of the disease – 7 days (Q1–Q3: 5–10 days).

Results. There was a statistically significant difference among the Echo parameters when comparing 1-2B groups: TAPSE (tricuspid annular plane systolic excursion) (р=0.032), tricuspid annular peak systolic velocity (S') (р=0.032), IVA RV (isovolumetric myocardial acceleration of RV) global (р=0.035) and apical (р=0.039), Strain RV at the middle level (р=0.006) and global (р=0.014), LS RV (right ventricular longitudinal strain) basal, middle and global (р<0.001), LS RV apical (р=0.022), pulmonary artery pressure (р<0.001). When comparing group 2 at stages A and B, significant differences were noted about: FAC RV (right ventricular fractional area change) (р=0.033), IVA RV global (р=0.041), Strain RV at the middle level (р=0.047), pulmonary artery pressure (р<0.001).

Conclusion. The determination of the mean LS RV (STE) values, in contrast to the peak values in the TDI mode, demonstrated a higher diagnostic value in identifying signs of RV systolic dysfunction. Early detection of signs of progression of right ventricular dysfunction makes it possible to more accurately predict the progression of COVID-19 and, thereby, look for new ways to solve the problem of timely maintenance therapy in the future.


  1. Rothan H.A., Byrareddy S.N. The epidemiology and pathogenesis of coronavirus disease (COVID-19) outbreak. J. Autoimmun. 2020; 102433. DOI: 10.1016/j.jaut.2020.102433
  2. Jin Y., Yang H., Ji W., Wu W., Chen S., Zhang W., Duan G. Virology, epidemiology, pathogenesis, and control of COVID-19. Viruses. 2020; 12 (4): 372. DOI: 10.3390/v12040372
  3. Abaturov A.E., Agafonova E.A., Krivusha E.L., Nikulina A.A. Pathogenesis of COVID-19. Zdorov'e Rebenka. 2020; 15 (2): 133–44. DOI: 10.22141/2224-0551.15.1.2020.2005984 (in Russ.).
  4. Chuchalin A.G. The right-sided heart failure. Pulmonology. 2019; 29 (2): 135–47. DOI: 10.18093/0869-0189-2019-29-2-135-147
  5. Lang R.M., Badano L.P., Mor-Avi V., Afilalo J., Armstrong A., Ernande L. et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur. Heart J. Cardiovasc. Imaging. 2015; 16 (3): 233–71. DOI: 10.1093/ehjci/jev014
  6. Tei C., Dujardin K.S., Hodge D.O., Bailey K.R., McGoon M.D., Tajik A.J., Seward J.B. Doppler echocardiographic index for assessment of global right ventricular function. J. Am. Soc. Echocardiogr. 1996; 9 (6): 838–47. DOI: 10.1016/S0894- 7317(96)90476-9
  7. Rudski L.G., Lai W.W., Afilalo J., Hua L., Handschumacher M.D., Chandrasekaran K. et al. Guidelines for the echocardiography assessment of the right heart in adults: а report from the American Society of Echocardiography Endorsed by the European Society of Cardiology, and the Canadian Society of Echocardiography. J. Am. Soc. Echocardiogr. 2010; 23: 685–713. DOI: 10.1016/j.echo.2010.05.010
  8. Voigt J.U., Pedrizzetti G., Lysyansky P., Marwick T.H., Houle H., Baumann R. et al. Definition for a common standard for 2D speckle tracking echocardiography: a consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. Eur. Heart J. Cardiovasc. Imaging. 2015; 16: 1–11. DOI: 10.1093/ehjci/jeu184
  9. Masuyama T., Kodama K., Kitakabe A., Sato H., Nanto H., Inoue M. Continuous-wave Doppler echocardiographic detection of pulmonary regurgitation and its application to noninvasive estimation of pulmonary artery pressure. Circulation. 1986; 74: 484–92. DOI: 10.1161/01.CIR.74.3.484
  10. Alekhin M.N., Zateischikova A.A., Kiselev D.G., Shavrin I.V., Privalov D.V., Vtorushkin D.V. et al. Importance of echocardiographic postcava evalution for calculations of average pressure in the pulmonary artery in patients with chronic obstructive lung disease. Kremlin medicine. Clinical Bulletin. 2010; 2: 64–7 (in Russ.).
  11. Foale R., Nihoyannopoulos P., McKenna W., Kleinebenne A., Nadazdin A., Rowland E. et al. Echocardiographic measurement of the normal adult right ventricle. Br. Heart J. 1986; 56: 33–44.DOI: 10.1136/hrt.56.1.33
  12. Jurcut R., Giusca S., La Gerche A., Vasile S., Ginghina C., Voigt J.U. The echocardiographic assessment of the right ventricle: what to do in 2010? European journal of echocardiography: the journal of the Working Group on Echocardiography of the European Society of Cardiology. 2010; 11 (2): 81–96. DOI: 10.1093/ejechocard/jep234
  13. Nartsissova G.P. Role of right ventricle in cardiovascular pathology. Circulatory pathology and cardiac surgery. 2014; 18 (1): 32–6. DOI: 10.21688/1681-3472-2014-1-32-36 (in Russ.).
  14. McConnell M.V., Solomon S.D., Rayan M.E., Come P.C., Goldhaber S.Z., Lee R.T. Regional right ventricular dysfunction detected by echocardiography in acute pulmonary embolism. Am. J. Cardiol. 1996; 78: 469–73. DOI: 10.1016/S0002-9149(96)00339-6
  15. Lodato J.A., Ward R.P., Lang R.M. Echocardiographic predictors of pulmonary embolism in patients referred for helical CT. Echocardiography 2008; 25: 584–90. DOI: 10.1111/j.1540-8175.2008.00665.x
  16. Casazza F., Bongarzoni A., Capozi A., Agostoni O. Regional right ventricular dysfunction in acute pulmonary embolism and right ventricular infarction. Eur. J. Echocardiogr. 2005; 6: 11–4. DOI: 10.1016/j.euje.2004.06.002
  17. Torbicki A. Echocardiographic diagnosis of pulmonary embolism: a rise and fall of McConnell sign? Eur. J. Echocardiogr. 2005; 6: 2–3. DOI: 10.1016/j.euje.2004.11.007
  18. Fields J.M., Davis J., Girson L., Au A., Potts J., Morgan C.J., Vetter I., Riesenberg L.A. Transthoracic echocardiography for diagnosing pulmonary embolism: a systematic review and meta-analysis. J. Am. Soc. Echocardiogr. 2017; 30 (7): 714–23.e4. DOI: 10.1016/j.echo.2017.03.004
  19. Anavekar N.S., Gerson D., Skali H., Kwong R.Y., Yucel E.K., Solomon S.D. Two-dimensional assessment of right ventricular function: an echocardiographic-MRI correlative study. Echocardiography. 2007; 24: 452–6. DOI: 10.1111/j.1540-8175.2007.00424.x
  20. Zornoff L.A.M., Skali H., Pfeffer M.A., Sutton J.M., Rouleau J.L., Lamas G.A. et al. Right ventricular dysfunction and risk of heart failure and mortality after myocardial infarction. J. Am. Coll. Cardiol. 2002; 39: 1450–5. DOI: 10.1016/S0735-1097(02)01804-1
  21. Ghio S., Gavazzi A., Campana C., Inserra C., Klersy C., Sebastiani R. et al. Independent and additive prognostic value of right ventricular systolic function and pulmonary artery pressure in patients with chronic heart failure. J. Am. Coll. Cardiol. 2001; 37: 183–8. DOI: 10.1016/S0735-1097(00)01102-5
  22. Anavekar N.S., Skali H., Bourgoun M., Ghali J.K, Kober L., Maggioni A.P. et al. Usefulness of right ventricular fractional area change to predict death, heart failure, and stroke following myocardial infarction (from the Valiant ECHO study). Am. J. Cardiol. 2008; 101: 607–12. DOI: 10.1016/j.amjcard.2007.09.115
  23. Karnati P.K., El-Hajjar M., Torosoff M., Fein S.A. Myocardial performance index correlates with right ventricular ejection fraction measured by nuclear ventriculography. Echocardiography. 2008; 25 (3): 81–5. DOI: 10.1111/J.1540-8175.2007.00601.X
  24. Yoshifuku S., Otsuji Y., Takasaki K., Yuge K., Kisanuki A., Toyonaga K. et al. Pseudonormalized Doppler total ejection isovolume (Tei) index in patients with right ventricular acute myocardial infarction. Am. J. Cardiol. 2003; 91: 527–31. DOI: 10.1016/S0002-9149(02)03299-X
  25. Kukulski T., Hьbbert L., Arnold M., Wranne B., Hatle L., Sutherland G.R. Normal regional right ventricular function and its change with age: a Doppler myocardial imaging study. J. Am. Soc. Echocardiogr. 2000; 13: 194–204. DOI: 10.1067/mje.2000.103106
  26. Lindqvist P., Waldenstrom A., Henein M., Mцrner S., Kazzam E. Regional and global right ventricular function in healthy individuals aged 20–90 years: a pulsed Doppler tissue imaging study: Umea General Population Heart Study. Echocardiography 2005; 22: 305–14. DOI: 10.1111/j.1540-8175.2005.04023.x
  27. Frigiola A., Redington A.N., Cullen S., Vogel M. Pulmonary regurgitation is an important determinant of right ventricular contractile dysfunction in patients with surgically repaired tetralogy of Fallot. Circulation. 2004; 110 (11 Suppl. 1): II153–7. DOI: 10.1161/01.CIR.0000138397.60956.c2
  28. Mazur E.S., Mazur V.V., Rabinovich R.M., Myasnikov K.S., Orlov Y.A. Cardiac strain in right ventricular myocardial infarction and pulmonary embolism. Russian Journal of Cardiology. 2020; 25 (2): 3731. DOI: 10.15829/1560-4071-2020-2-3731 (in Russ.).
  29. Alekhin M.N. Ultrasound techniques for assessing myocardial deformation and their clinical significance. Doppler tissue imaging in assessing myocardial deformation (lecture 1). Ultrasound and Functional Diagnostics. 2011; 1: 105–17(in Russ.).
  30. Alekhin M.N. Ultrasound techniques for assessing myocardial deformation and their clinical significance. Two-dimensional tracking of gray-scale spots of an ultrasound image of the myocardium in the assessment of its deformation and twisting (Lecture 2). Ultrasound and Functional Diagnostics. 2011; 3: 107–20 (in Russ.).
  31. Motoji Y., Tanaka H., Fukuda Y., Ryo K., Emoto N., Kawai H., Hirata K. Efficacy of right ventricular free-wall longitudinal speckle-tracking strain for predicting long-term outcome in patients with pulmonary hypertension. Circ. J. 2013; 77 (3): 756–63. DOI: 10.1253/circj.CJ-12-1083
  32. Muraru D., Onciul S., Peluso D., Soriani N., Cucchini U., Aruta P. et al. Sex- and method-specific reference values for right ventricular strain by 2-dimensional speckle-tracking echocardiography. Circ. Cardiovasc. Imaging. 2016; 9: e003866. DOI: 10.1161/CIRCIMAGING.115.003866
  33. Li Y., Li H., Zhu S., Xie Y., Wang B., He L. et al. Prognostic Value of Right Ventricular Longitudinal Strain in Patients with COVID-19. JACC: Cardiovasc. Imaging. 2020; 13 (11): 2287–99. DOI: 10.1016/j.jcmg.2020.04.014
  34. Noordegraaf A.V., Westerhof B.E., Westerhof N. The relationship between the right ventricle and its load in pulmonary hypertension. J. Am. Coll. Cardiol. 2017; 69: 236–43. DOI: 10.1016/j.jacc.2016.10.047
  35. Mamalyga M.L. Application of innovative technologies for a comprehensive assessment of hemodynamics in the study of interdependent physiological processes in the brain and heart [Electronic resource]: scientific and educational recommendations. Moscow; 2015 (in Russ.).
  36. Kjaergaard J. Assessment of right ventricular systolic function by tissue Doppler echocardiography. Dan. Med. J. 2012; 59 (3): B4409.
  37. Haddad F., Hunt S.A., Rosenthal D.N., Murphy D.J. Right ventricular function in cardiovascular disease, part I: Anatomy, physiology, aging, and functional assessment of the right ventricle. Circulation 2008; 117 (11): 1436–48. DOI: 10.1161/CIRCULATIONAHA.107.653576
  38. Jamal F., Bergerot C., Argaud L., Loufouat J., Ovize M. Longitudinal strain quantitates regional right ventricular contractile function. Am. J. Physiol. Heart Circ. Physiol. 2003; 285 (6): H2842–7. DOI: 10.1152/ajpheart.00218.2003
  39. Naito H., Arisawa J., Harada K., Yamagami H., Kozuka T., Tamura S. Assessment of right ventricular regional contraction and comparison with the left ventricle in normal humans: a cine magnetic resonance study with presaturation myocardial tagging. Br. Heart J. 1995; 74 (2): 186–91. DOI: 10.1136/hrt.74.2.186

About Authors

  • Голухова Елена Зеликовна, доктор мед. наук, профессор, академик РАН, заведующий кафедрой, и. о. директора НМИЦССХ им. А.Н. Бакулева, зам. главного редактора журнала, ORCID
  • Сливнева Инесса Викторовна, канд. мед. наук, науч. сотр., доцент, ORCID
  • Рыбка Михаил Михайлович, доктор мед. наук, профессор, зам. директора по анестезиологии и реаниматологии, заведующий отделением, ORCID
  • Мамалыга Максим Леонидович, доктор мед. наук, ст. науч. сотр., ORCID
  • Алехин Михаил Николаевич, доктор мед. наук, профессор, вице-президент РАСУДМ, заведующий отделением, ORCID
  • Ключников Иван Вячеславович, доктор мед. наук, профессор, гл. науч. сотр., ORCID
  • Антонова Диана Евгеньевна, ординатор, ORCID
  • Марапов Дамир Ильдарович, канд. мед. наук, доцент, ORCID
  • Волковская Ирина Васильевна, канд. мед. наук, руководитель отдела, ORCID

Chief Editor

Leo A. Bockeria, MD, PhD, DSc, Professor, Academician of Russian Academy of Sciences, Director of Bakoulev National Medical Research Center for Cardiovascular Surgery