Spectrum of Cardiac Manifestations in COVID-19: A Systematic Echocardiographic Study

Yishay Szekely, Yael Lichter, Philippe Taieb, Ariel Banai, Aviram Hochstadt, Ilan Merdler, Amir Gal Oz, Ehud Rothschild, Guy Baruch, Yogev Peri, Yaron Arbel, Yan Topilsky, Yishay Szekely, Yael Lichter, Philippe Taieb, Ariel Banai, Aviram Hochstadt, Ilan Merdler, Amir Gal Oz, Ehud Rothschild, Guy Baruch, Yogev Peri, Yaron Arbel, Yan Topilsky

Abstract

Background: Information on the cardiac manifestations of coronavirus disease 2019 (COVID-19) is scarce. We performed a systematic and comprehensive echocardiographic evaluation of consecutive patients hospitalized with COVID-19 infection.

Methods: One hundred consecutive patients diagnosed with COVID-19 infection underwent complete echocardiographic evaluation within 24 hours of admission and were compared with reference values. Echocardiographic studies included left ventricular (LV) systolic and diastolic function and valve hemodynamics and right ventricular (RV) assessment, as well as lung ultrasound. A second examination was performed in case of clinical deterioration.

Results: Thirty-two patients (32%) had a normal echocardiogram at baseline. The most common cardiac pathology was RV dilatation and dysfunction (observed in 39% of patients), followed by LV diastolic dysfunction (16%) and LV systolic dysfunction (10%). Patients with elevated troponin (20%) or worse clinical condition did not demonstrate any significant difference in LV systolic function compared with patients with normal troponin or better clinical condition, but they had worse RV function. Clinical deterioration occurred in 20% of patients. In these patients, the most common echocardiographic abnormality at follow-up was RV function deterioration (12 patients), followed by LV systolic and diastolic deterioration (in 5 patients). Femoral deep vein thrombosis was diagnosed in 5 of 12 patients with RV failure.

Conclusions: In COVID-19 infection, LV systolic function is preserved in the majority of patients, but LV diastolic function and RV function are impaired. Elevated troponin and poorer clinical grade are associated with worse RV function. In patients presenting with clinical deterioration at follow-up, acute RV dysfunction, with or without deep vein thrombosis, is more common, but acute LV systolic dysfunction was noted in ≈20%.

Keywords: COVID-19; echocardiography; heart ventricles; thromboembolism.

Figures

Figure 1.
Figure 1.
Patterns of cardiac disease in hospitalized patients with coronavirus disease 2019 (COVID-19). LV indicates left ventricular; and RV, right ventricular.
Figure 2.
Figure 2.
Forest plots for association of imaging with outcome.A, Forest plot for association of imaging with clinical deterioration. Impact of left and right imaging parameters on clinical deterioration in patients with coronavirus disease 2019 (COVID-19) infection. B, Forest plot for association of imaging with mortality. Impact of left and right ventricular imaging parameters on mortality in patients with COVID-19 infection. AT indicates pulmonic acceleration time; EF, ejection fraction; RVEDA, right ventricular end-diastolic area; and SV, stroke volume.
Figure 3.
Figure 3.
A patient with a sudden decrease in systolic function. Doppler interrogation of the mitral inflow (A and B), tissue Doppler of mitral annulus (C and D), and left ventricular (LV) outflow tract (LVOT) flow (E and F). Images on the left (A, C, and E) are at baseline. Images on the right (B, D, and F) were obtained 2 days later, after clinical deterioration and an increase in troponin level. Note the increase in E/e’ ratio, suggesting an increase in left filling pressure, and decrease in LV S’ and LVOT flow velocity, suggesting a decrease in stroke volume. Time bar scale is 40 milliseconds between every thin line and 200 milliseconds between every thick line.
Figure 4.
Figure 4.
A patient with sudden right ventricular dysfunction with an acute rise in afterload. Doppler interrogation of mitral inflow (A and D), left ventricular (LV) outflow tract (LVOT) flow (B and E), and pulmonary flow acceleration time (C and F) in patients with right ventricular (RV) dysfunction and deep vein thrombosis. Top images (A–C) are at baseline; bottom images (D–F) are after clinical deterioration. Note that mitral inflow velocity decreases as a result of unloading of the LV by the failing RV and the mild decrease in LVOT velocity, suggesting a decrease in stroke volume caused by the underfilled LV. On the right, note the change in pulmonic flow acceleration time from symmetrical to early picking, suggesting an elevation in pulmonary vascular resistance. Time bar scale is 40 milliseconds between every thin line and 200 milliseconds between every thick line.

References

    1. Bhatraju PK, Ghassemieh BJ, Nichols M, Kim R, Jerome KR, Nalla AK, Greninger AL, Pipavath S, Wurfel MM, Evans L, et al. Covid-19 in critically ill patients in the Seattle region: case series. N Engl J Med 20203822012–2022doi: 10.1056/NEJMoa2004500
    1. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 20203951054–1062doi: 10.1016/S0140-6736(20)30566-3
    1. Guo T, Fan Y, Chen M, Wu X, Zhang L, He T, Wang H, Wan J, Wang X, Lu Z. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19) [published online March 27, 2020]. JAMA Cardiol. doi:10.1001/jamacardio.2020.1017.
    1. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, 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. J Am Soc Echocardiogr 2015281–39.e14doi: 10.1016/j.echo.2014.10.003
    1. Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE, Jr, Drazner MH, Fonarow GC, Geraci SA, Horwich T, Januzzi JL, et al. 2013 ACCF/AHA guideline for the management of heart failure: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 20131281810–1852doi: 10.1161/CIR.0b013e31829e8807
    1. Lambden S, Laterre PF, Levy MM, Francois B. The SOFA score: development, utility and challenges of accurate assessment in clinical trials. Crit Care. 2019;23:374. doi: 10.1186/s13054-019-2663-7.
    1. Liao X, Wang B, Kang Y. Novel coronavirus infection during the 2019-2020 epidemic: preparing intensive care units–the experience in Sichuan Province, China. Intensive Care Med 202046357–360doi: 10.1007/s00134-020-05954-2
    1. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, 3rd, Dokainish H, Edvardsen T, Flachskampf FA, Gillebert TC, Klein AL, Lancellotti P, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 201629277–314doi: 10.1016/j.echo.2016.01.011
    1. Kitabatake A, Inoue M, Asao M, Masuyama T, Tanouchi J, Morita T, Mishima M, Uematsu M, Shimazu T, Hori M, et al. Noninvasive evaluation of pulmonary hypertension by a pulsed Doppler technique. Circulation 198368302–309doi: 10.1161/01.cir.68.2.302
    1. Kirkpatrick JN, Mitchell C, Taub C, Kort S, Hung J, Swaminathan M. ASE statement on protection of patients and echocardiography service providers during the 2019 novel coronavirus outbreak [published online April 6, 2020]. J Am Coll Cardiol. doi: 10.1016/j.jacc.2020.04.002.
    1. Topilsky Y, Khanna AD, Oh JK, Nishimura RA, Enriquez-Sarano M, Jeon YB, Sundt TM, Schaff HV, Park SJ. Preoperative factors associated with adverse outcome after tricuspid valve replacement. Circulation 20111231929–1939doi: 10.1161/CIRCULATIONAHA.110.991018
    1. Bouhemad B, Mongodi S, Via G, Rouquette I. Ultrasound for “lung monitoring” of ventilated patients. Anesthesiology 2015122437–447doi: 10.1097/ALN.0000000000000558
    1. Hu H, Ma F, Wei X, Fang Y. Coronavirus fulminant myocarditis saved with glucocorticoid and human immunoglobulin [published online March 16, 2020]. Eur Heart J. doi: 10.1093/eurheartj/ehaa190.
    1. Zeng JH, Liu YX, Yuan J, Wang FX, Wu WB, Li JX, Wang LF, Gao H, Wang Y, Dong CF, et al. First case of COVID-19 complicated with fulminant myocarditis: a case report and insights [published online April 10, 2020]. Infection. doi: 10.1007/s15010-020-01424-5.
    1. Li SS, Cheng CW, Fu CL, Chan YH, Lee MP, Chan JW, Yiu SF. Left ventricular performance in patients with severe acute respiratory syndrome: a 30-day echocardiographic follow-up study. Circulation 20031081798–1803doi: 10.1161/01.CIR.0000094737.21775.32
    1. Landesberg G, Gilon D, Meroz Y, Georgieva M, Levin PD, Goodman S, Avidan A, Beeri R, Weissman C, Jaffe AS, et al. Diastolic dysfunction and mortality in severe sepsis and septic shock. Eur Heart J 201233895–903doi: 10.1093/eurheartj/ehr351
    1. Wang J, Hajizadeh N, Moore EE, McIntyre RC, Moore PK, Veress LA, Yaffe MB, Moore HB, Barrett CD. Tissue plasminogen activator (tPA) treatment for COVID-19 associated acute respiratory distress syndrome (ARDS): a case series [published online April 8, 2020]. J Thromb Haemost. doi: 10.1111/jth.14828.
    1. Tang N, Bai H, Chen X, Gong J, Li D, Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy [published online May 18, 2020]. J Thromb Haemost. doi: 10.1111/jth.14817.

Source: PubMed

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