Prognostic Value of Right Ventricular Longitudinal Strain in Patients With COVID-19

Yuman Li, He Li, Shuangshuang Zhu, Yuji Xie, Bin Wang, Lin He, Danqing Zhang, Yongxing Zhang, Hongliang Yuan, Chun Wu, Wei Sun, Yanting Zhang, Meng Li, Li Cui, Yu Cai, Jing Wang, Yali Yang, Qing Lv, Li Zhang, Mingxing Xie, Yuman Li, He Li, Shuangshuang Zhu, Yuji Xie, Bin Wang, Lin He, Danqing Zhang, Yongxing Zhang, Hongliang Yuan, Chun Wu, Wei Sun, Yanting Zhang, Meng Li, Li Cui, Yu Cai, Jing Wang, Yali Yang, Qing Lv, Li Zhang, Mingxing Xie

Abstract

Objectives: The aim of this study was to investigate whether right ventricular longitudinal strain (RVLS) was independently predictive of higher mortality in patients with coronavirus disease-2019 (COVID-19).

Background: RVLS obtained from 2-dimensional speckle-tracking echocardiography has been recently demonstrated to be a more accurate and sensitive tool to estimate right ventricular (RV) function. The prognostic value of RVLS in patients with COVID-19 remains unknown.

Methods: One hundred twenty consecutive patients with COVID-19 who underwent echocardiographic examinations were enrolled in our study. Conventional RV functional parameters, including RV fractional area change, tricuspid annular plane systolic excursion, and tricuspid tissue Doppler annular velocity, were obtained. RVLS was determined using 2-dimensional speckle-tracking echocardiography. RV function was categorized in tertiles of RVLS.

Results: Compared with patients in the highest RVLS tertile, those in the lowest tertile were more likely to have higher heart rate; elevated levels of D-dimer and C-reactive protein; more high-flow oxygen and invasive mechanical ventilation therapy; higher incidence of acute heart injury, acute respiratory distress syndrome, and deep vein thrombosis; and higher mortality. After a median follow-up period of 51 days, 18 patients died. Compared with survivors, nonsurvivors displayed enlarged right heart chambers, diminished RV function, and elevated pulmonary artery systolic pressure. Male sex, acute respiratory distress syndrome, RVLS, RV fractional area change, and tricuspid annular plane systolic excursion were significant univariate predictors of higher risk for mortality (p < 0.05 for all). A Cox model using RVLS (hazard ratio: 1.33; 95% confidence interval [CI]: 1.15 to 1.53; p < 0.001; Akaike information criterion = 129; C-index = 0.89) was found to predict higher mortality more accurately than a model with RV fractional area change (Akaike information criterion = 142, C-index = 0.84) and tricuspid annular plane systolic excursion (Akaike information criterion = 144, C-index = 0.83). The best cutoff value of RVLS for prediction of outcome was -23% (AUC: 0.87; p < 0.001; sensitivity, 94.4%; specificity, 64.7%).

Conclusions: RVLS is a powerful predictor of higher mortality in patients with COVID-19. These results support the application of RVLS to identify higher risk patients with COVID-19.

Keywords: 2D, 2-dimensional; AIC, Akaike information criterion; ARDS, acute respiratory distress syndrome; CI, confidence interval; COVID-19; COVID-19, coronavirus disease-2019; HR, hazard ratio; LS, longitudinal strain; LV, left ventricular; LVEF, left ventricular ejection fraction; PASP, pulmonary artery systolic pressure; ROC, receiver-operating characteristic; RV, right ventricular; RVFAC, right ventricular fractional area change; RVLS, right ventricular longitudinal strain; SARS-CoV-2; SARS-CoV-2, severe acute respiratory syndrome-coronavirus-2; STE, speckle-tracking echocardiography; S’, tricuspid lateral annular systolic velocity; TAPSE, tricuspid annular plane systolic excursion; TR, tricuspid regurgitation; right ventricular function; speckle tracking echocardiography; strain.

Conflict of interest statement

This work was supported by the National Natural Science Foundation of China (grants 81727805, 81922033, and 81401432). The authors have reported that they have no relationships relevant to the contents of this paper to disclose.

© 2020 by the American College of Cardiology Foundation. Published by Elsevier.

Figures

Graphical abstract
Graphical abstract
Figure 1
Figure 1
RVLS Obtained From 2-Dimensional Speckle Tracking Echocardiography in Patients With COVID-19 (A) Representative images of the highest tertile of right ventricular longitudinal strain (RVLS). (B) Representative images of the middle tertile of RVLS. (C) Representative images of the lowest tertile of RVLS.
Figure 2
Figure 2
Distribution of RVLS in Patients With COVID-19 (A) Distribution of right ventricular longitudinal strain (RVLS) in patients with coronavirus disease-2019 (COVID-19) (blue, highest tertile; green, middle tertile; red, lowest tertile). (B) Tukey box-and-whisker plots of RVLS values in patients with COVID-19 according to the tertiles. (C) Distribution of RVLS in patients with COVID-19 (red) and healthy control subjects (green). RVLS values are absolute values.
Figure 3
Figure 3
Receiver-Operating Characteristic Curves of RVLS, FAC, and TAPSE for Adverse Clinical Outcome FAC = fractional area change; RVLS = right ventricular longitudinal strain; TAPSE = tricuspid annular plane systolic excursion.
Figure 4
Figure 4
Kaplan-Meier Survival Curves Showing the Association of Higher Mortality and Right Ventricular Function (A) Kaplan-Meier curve of survival in patients stratified by the cutoff value of tricuspid annular plane systolic excursion (TAPSE). (B) Kaplan-Meier curve of survival in patients stratified by the cutoff value of right ventricular fractional area change (FAC).
Central Illustration
Central Illustration
Association of Right Ventricular Longitudinal Strain and Mortality in Patients With COVID-19 In the upper panel, examples of strain plot of right ventricular longitudinal strain (RVLS) are shown: (A) a 42-year-old patient with impaired RVLS (16.8%), who died of coronavirus disease-2019 17 days after the echocardiographic examination; and (B) a 57-year-old patient with preserved RVLS (29.3%), who did not experience an event during 61 days of follow-up. In the lower panel, survival curves for all-cause mortality are shown (C) according to the cutoff value of RVLS (23%) and (D) according to tertiles of RVLS (≤20.5%, 20.6% to 25.4%, and ≥25.5%). RVLS values are absolute values.

References

    1. Guo T., Fan Y., Chen M. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19) JAMA Cardiol. 2020;5:811–818.
    1. Shi S., Qin M., Shen B. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiol. JAMA Cardiol. 2020;5:802–810.
    1. Huang C., Wang Y., Li X. Clinical features of patients with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497–506.
    1. Yang X., Yu Y., Xu J. Clinical course and outcomes of critically ill patients with SARSCoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study. Lancet. Respir Med. 2020;8:475–481.
    1. Carluccio E., Biagioli P., Alunni G. Prognostic value of right ventricular dysfunction in heart failure with reduced ejection fraction: superiority of longitudinal strain over tricuspid annular plane systolic excursion. Circ Cardiovasc Imaging. 2018;11
    1. Mor-Avi V., Lang R.M., Badano L.P. Current and evolving echocardiographic techniques for the quantitative evaluation of cardiac mechanics: ASE/EAE consensus statement on methodology and indications endorsed by the Japanese Society of Echocardiography. Eur J Echocardiogr. 2011;12:167–205.
    1. Longobardo L., Suma V., Jain R. Role of two-dimensional speckle-tracking echocardiography strain in the assessment of right ventricular systolic function and comparison with conventional parameters. J Am Soc Echocardiogr. 2017;30:937–946.e6.
    1. Li Y., Xie M., Wang X. Impaired right and left ventricular function in asymptomatic children with repaired tetralogy of Fallot by two-dimensional speckle tracking echocardiography study. Echocardiography. 2015;32:135–143.
    1. Xie M., Li Y., Cheng T.O. The effect of right ventricular myocardial remodeling on ventricular function as assessed by two-dimensional speckle tracking echocardiography in patients with tetralogy of Fallot: a single center experience from China. Int J Cardiol. 2015;178:300–307.
    1. Park S.J., Park J.H., Lee H.S. Impaired RV global longitudinal strain is associated with poor long-term clinical outcomes in patients with acute inferior STEMI. J Am Coll Cardiol Img. 2015;8:161–169.
    1. Motoki H., Borowski A.G., Shrestha K. Right ventricular global longitudinal strain provides prognostic value incremental to left ventricular ejection fraction in patients with heart failure. J Am Soc Echocardiogr. 2014;27:726–732.
    1. World Health Organization Clinical management of severe acute respiratory infection when COVID-19 is suspected. Available at:
    1. World Medical Association World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310:2191–2194.
    1. Rudski L.G., Lai W.W., Afilalo J. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography and the Canadian Society of Echocardiography. J Am Soc Echocardiogr. 2010;23:685–713.
    1. Lang R.M., Badano L.P., Mor-Avi V. 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. 2015;28:1–39.e14.
    1. Chen N., Zhou M., Dong X. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395:507–513.
    1. Chen T., Wu D., Chen H.L. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: retrospective study. BMJ. 2020;368:m1295.
    1. Li S.S., Cheng C.W., Fu C.L. Left ventricular performance in patients with severe acute respiratory syndrome: a 30-day echocardiographic follow-up study. Circulation. 2003;108:1798–1803.
    1. Alashi A., Mentias A., Abdallah A. Incremental prognostic utility of left ventricular global longitudinal strain in asymptomatic patients with significant chronic aortic regurgitation and preserved left ventricular ejection fraction. J Am Coll Cardiol Img. 2017;11:673–682.
    1. Houard L., Benaets M.B., de Meester de Ravenstein C. Additional prognostic value of 2D right ventricular speckle-tracking strain for prediction of survival in heart failure and reduced ejection fraction: a comparative study with cardiac magnetic resonance. J Am Coll Cardiol Img. 2019;12:2373–2385.
    1. Li B., Yang J., Zhao F. Prevalence and impact of cardiovascular metabolic diseases on COVID-19 in China. Clin Res Cardiol. 2020;109:531–538.
    1. Lazzeri C., Bonizzoli M., Cozzolino M. Serial measurements of troponin and echocardiography in patients with moderate-to-severe acute respiratory distress syndrome. J Crit Care. 2016;33:132–136.
    1. Liu C.L., Lu Y.T., Peng M.J. Clinical and laboratory features of severe acute respiratory syndrome vis-a-vis onset of fever. Chest. 2004;126:509–517.
    1. D’Ascenzi F., Anselmi F., Piu P. Cardiac magnetic resonance normal reference values of biventricular size and function in male athlete’s heart. J Am Coll Cardiol Img. 2019;12:1755–1765.
    1. Mast T.P., Taha K., Cramer M.J. The prognostic value of right ventricular deformation imaging in early arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol Img. 2019;12:446–455.
    1. Medvedofsky D., Koifman E., Jarrett H. Association of right ventricular longitudinal strain with mortality in patients undergoing transcatheter aortic valve replacement. J Am Soc Echocardiogr. 2020;33:452–460.
    1. Cameli M., Bernazzali S., Lisi M. Right ventricular longitudinal strain and right ventricular stroke work index in patients with severe heart failure: left ventricular assist device suitability for transplant candidates. Transplant Proc. 2012;44 2013–5.

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