Archives of Academic Emergency Medicine. 2021; 9(1): e21 https://doi.org/10.22037/aaem.v9i1.1155 OR I G I N A L RE S E A RC H Echocardiographic Abnormalities as Independent Prog- nostic Factors of In-Hospital Mortality among COVID-19 Patients Mehdi Pishgahi1, Kimia Karimi Toudeshki1, Saeed Safari2,3∗, Mahmoud Yousefifard4 † 1. Cardiology Department, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 2. Proteomic Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 3. Emergency Department, Shohadaye Tajrish Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran. 4. Physiology Research Center, Iran University of Medical Sciences, Tehran, Iran. Received: January 2021; Accepted: January 2021; Published online: 24 February 2021 Abstract: Introduction: Direct and indirect sequels of COVID-19 in the cardiovascular system are unclear. The present study aims to investigate the echocardiography findings in COVID-19 patients and possible correlations be- tween the findings and the disease outcome. Methods: In this cross-sectional study, baseline characteristics and echocardiographic findings of hospitalized COVID-19 cases, and their correlation with mortality were evaluated. Furthermore, computed tomography (CT) angiography was performed to assess possible pulmonary embolism. In-hospital mortality was considered as the main outcome of the present study. Results: 680 confirmed COVID- 19 cases with the mean age of 55.15 ± 10.92 (range: 28 – 79) years were studied (63.09% male). Analysis showed that history of ischemic heart disease (RR=1.14; 95% CI: 1.08-1.19), history of hypertension (RR=1.04; 95% CI: 1.00-1.08), presence of embolism in main pulmonary artery (RR=1.53; 95% CI: 1.35-1.74), CT involvement more than 70% (RR=1.08; 95% CI: 1.1.01-1.16), left ventricular ejection fraction < 30 (RR=1.19; 95% CI: 1.07-1.32), pleu- ral effusion (RR=1.08; 95% CI: 1.00-1.16), pulmonary artery systolic blood pressure 35 to 50 mmHg (RR=1.11; 95% CI: 1.03-1.18), right ventricular dysfunction (RR=1.54; 95% CI: 1.40-1.08), and collapsed inferior vena-cava (RR=1.05; 95% CI: 1.01-1.08) were independent prognostic factors of in-hospital mortality. Conclusion: Our study showed that cardiac involvement is a prevalent complication in COVID-19 patients. Echocardiography findings have independent prognostic value for prediction of in-hospital mortality. Since echocardiography is an easy and accessible method, echocardiography monitoring of COVID-19 patients can be used as a screening tool for identification of high-risk patients. Keywords: Electrocardiography; COVID-19; SARS-CoV-2; outcome; mortality Cite this article as: Pishgahi M, Karimi Toudeshki K, Safari S, Yousefifard M. Echocardiographic Abnormalities as Independent Prognostic Factors of In-Hospital Mortality among COVID-19 Patients. Arch Acad Emerg Med. 2021; 9(1): e21. 1. Introduction The COVID-19 pandemic has become a global challenge, and the number of those affected with the disease is increasing. Initial reports indicated a 3 to 5% mortality rate among the patients having this respiratory infection. However, with the ∗Corresponding Author: Saeed Safari; Emergency Department, Shohadaye Tajrish Hospital, Tajrish Square, Tehran, Iran. Email: s.safari@sbmu.ac.ir; sa- fari266@gmail.com; Tel: +9822721155. † Corresponding Author: Mahmoud Yousefifard; Physiology Research Center, Iran University of Medical Sciences, Hemmat Highway, P.O Box: 14665-354, Tehran, Iran; Phone/Fax: +982186704771; E-mail: yousefifard.m@iums.ac.ir. spread of the disease in different parts of the world, the mor- tality rate of the disease has risen. As of today, considering closed cases of the disease, the mortality rate among COVID- 19 patients has been reported to be 21% (1). While the mentioned mortality rate for COVID-19 is consid- erably high, there is no definitive cure for the disease, and all interventions performed for the patients are rather support- ive (2, 3). Current evidence suggests that the host tissue for severe acute respiratory syndrome coronavirus 2 (SARS-CoV- 2) is not only the lung, and since its receptor, angiotensin converting enzyme 2, is present in vascular tissue, kidneys, brain and cardiac tissue, symptoms other than respiratory in- volvements have been reported in COVID-19 patients (4-6). This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem M. Pishgahi et al. 2 A number of studies show that SARS-CoV-2 attacks cardiac and vascular tissues and blood vessels, causing various alter- ations and resulting events (4, 6), including thromboembolic accidents such as pulmonary embolism and stroke. Clinical evaluations of the patients indicate that cardiac manifesta- tions present in one of every five patients (7). These car- diac injuries can occur even without presenting symptoms of pneumonia (8). A meta-analysis on three articles showed that cardiac tro- ponin I levels in patients with severe form of COVID-19 are significantly higher compared to that of non-severe patients (9). Hence, COVID-19 seems to affect the heart directly. On the other hand, pulmonary involvement and increased pressure of pulmonary artery can cause right heart overload. Also, vascular endothelium involvement in lungs increases the risk of stasis, followed by thrombosis, which may lead to right heart failure through increasing pulmonary artery pres- sure. As a result, considering the direct and indirect effects of COVID-19 on heart, the present study aims to investigate the echocardiography findings in COVID-19 patients and possi- ble correlations between the findings and the disease out- come. 2. Methods 2.1. Study design and patients Data of 680 confirmed COVID-19 patients admitted to Shohadaye Tajrish and Modarres educational Hospitals, Tehran, Iran, from April to November 2020 were included, prospectively. COVID-19 pneumonia was confirmed based on chest CT scan and RT-PCR. Out-of-hospital mortality and pregnancy were exclusion criteria. Before patient recruit- ment, ethical approval was obtained from Ethic Committee of Shahid Beheshti University of Medical Sciences (Ethics code: IR.SBMU.RETECH.REC.1399.060). Written informed consent was obtained and researchers adhered to principles of Helsinki declaration. 2.2. Data Gathering and outcome During hospitalization, demographic and baseline charac- teristics were recorded. Echocardiography was performed using SonoSite set (Edge L1, USA) and in standard position. All patients were assessed by an expert cardiologist with 10 years of clinical experience in echocardiography. All echocar- diography abnormalities was assessed and reported. Per- forming and interpretation of echocardiography was done according to American Society of Echocardiography Guide- line (10). The echocardiograms were ordered by in-charge physicians for intensive care unit (ICU)-admitted patients, intubated patients, severely ill cases, patients with hemody- namic instability, and those with suspected concomitant car- diac problem with COVID-19 pneumonia. In addition, pul- monary involvement on CT scan was assessed. Furthermore, CT pulmonary angiogram was performed to assess possible pulmonary embolism (11). In-hospital mortality was consid- ered as the main outcome of the present study. 2.3. Statistical analysis All analyses were performed in STATA 14.0. T-test and chi- squared (or exact Fisher) test were used to evaluate asso- ciation of baseline and echocardiography findings with in- hospital mortality. Then, potential prognostic factors (factors with a p value less than 0.1 in univariate analyses) were en- tered into a backward (stepwise) regression model using gen- eral linear models. Multivariate analysis was adjusted for age, comorbidity, percentage of CT involvement, and presence of thromboembolism in pulmonary vessels. Significance level was considered as p <0.05. 3. Results 680 confirmed COVID-19 cases with the mean age of 55.15 ± 10.92 (range: 28 – 79) years were studied (63.09% male). Hypertension (43.82%), diabetes mellitus (24.56%), and is- chemic heart disease (16.47%) were among the most frequent underlying disease of this series, respectively. The rate of mortality was 8.38% in all hospitalized cases. CT scan in- volvement was less than 50%, 40-70%. and >70% in 62.94%, 28.09%, and 8.97% of patients, respectively. CT pulmonary angiogram was normal in 91.76% of the patients. 6.03% had segmental/sub segmental embolism and 2.21% had main pulmonary artery embolism. Table 1 compares the baseline characteristics of COVID-19 cases between survived and non-survived cases. There was a significant correlation between age (p=0.0006), history of ischemic heart diseases (p<0.0001), history of diabetes mel- litus (p = 0.010), and hypertension (p=0.001) with higher rate of mortality. In addition, higher lung involvement in CT scan and presence of embolism in CT pulmonary angiogram cor- related with patients’ mortality (p=0.0002). 3.1. Echocardiographic findings Table 2 summarizes the echocardiographic findings of COVID-19 cases. Left ventricular ejection fraction (EF) < 50% (22.94%), right ventricular dilation (18.53%), left ventricular dilation (7.06%), pleural effusion (6.03%), right ventricular clot (0.44%), moderate and moderate-severe tricuspid regur- gitation (17.35%), pulmonary artery systolic pressure (PASP) of 35-50 mmHg (7.65%), PASP more than 50 mmHg (2.5%), and dilated (13.82%) and collapsed (45.59%) inferior vena cava (IVC) were the most important findings in echocardiog- raphy. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 3 Archives of Academic Emergency Medicine. 2021; 9(1): e21 3.2. Prognostic factors of death Univariate logistic regression showed a significant associa- tion between COVID-19 patients’ mortality and left ventric- ular EF (p=0.0001), left ventricular dilation (p<0.0001), pleu- ral effusion (p<0.0001), right ventricular dilation (p<0.0001), right ventricular clot (p=0.020), tricuspid regurgitation (p<0.0001), PASP level (p=0.0001), and inferior vena cava size (p<0.0001). Stepwise multiple regression showed that history of ischemic heart disease (RR=1.14; 95% CI: 1.08-1.19), history of hyper- tension (RR=1.04; 95% CI: 1.00-1.08), presence of embolism in main pulmonary artery (RR=1.53; 95% CI: 1.35-1.74), CT involvement more than 70% (RR=1.08; 95% CI: 1.1.01-1.16), left ventricular ejection fraction < 30 (RR=1.19; 95% CI: 1.07- 1.32), pleural effusion (RR=1.08; 95% CI: 1.00-1.16), PASP 35 to 50 mmHg (RR=1.11; 95% CI: 1.03-1.18), right ventricular dysfunction (RR=1.54; 95% CI: 1.40-1.08), and collapsed IVC (RR=1.05; 95% CI: 1.01-1.08) were independent prognostic factors of in-hospital mortality (Table 3). 4. Discussion Findings of the present study demonstrated that echocar- diographic abnormalities in COVID-19 patients are common, and among the abnormalities, history of ischemic heart dis- ease, history of hypertension, EF<30%, Pleural effusion, RV dysfunction, increased PASP and IVC collapse are indepen- dent prognostic factors of patients’ mortality. These factors can predict mortality independent from pulmonary involve- ment and presence of pulmonary embolism. Cardiovascu- lar complications and coagulopathies have been evaluated in different studies and have shown to be directly related to the mortality rate of patients (7, 9, 12). Evidences observed in echocardiography, provided in the current study, are in line with previous researches. Initially, the lung tissue was presumed to be the only target of SARS-CoV-2, but as time went on, other tissues were found to be hosting the virus as well. SARS-CoV-2 receptor, ACE2, is expressed largely in blood vessel walls and heart (13). There- fore, if the virus enters the blood stream, it can easily infect the mentioned tissues. Hence, cardiovascular complications and coagulopathies have been evaluated in different studies and have shown to be directly related to the mortality rate of patients (7, 9, 12). Evidences observed in echocardiography, provided in the current study are suggestive of the prior men- tioned hypothesis. It has been thus far shown that COVID-19 could cause a hy- percoagulable state in the body throughout the course of vi- ral infection, through causing alterations in coagulation fac- tors or changes in homeostasis (14-16). Thrombosis lead to many problems, including pulmonary embolism and car- diac muscle injury. Moreover, COVID-19-associated pneu- monia has been shown to be a risk factor for pulmonary embolism (17). Considering the mentioned evidence, there seems to be an undeniable relationship between COVID- 19, thrombosis and PTE, and the results of this study are in line with these findings. Therefore, it is of great impor- tance to closely monitor COVID-19 patients admitted to hos- pital for possible incidence of thrombosis, and even start pro- phylactic anticoagulant therapy (18) . However, in multi- variate analysis, echocardiographic abnormalities indepen- dently predicted in-hospital mortality of COVID-19 patients after adjusting the analysis for CT angiography findings. This suggests that in addition to the effects of COVID-19 on blood vessels and the increased odds of thrombosis, its direct ef- fects on the cardiac muscle also is associated with poor prog- nosis of patients. RV dilatation and dysfunction, LV dysfunction and subse- quent reduced EF were the echocardiography manifestations implicating heart muscle weakness and injury during the acute state of disease in this study. To be illustrated, viral in- fections can contribute to a complication, known as viral car- diomyopathy, which is one of the primary reasons of cardiac dilation (19); and coronaviruses are known to be one of the major viral causes of cardiomyopathy (20). This study, in line with the results of other studies, suggests that the presence of right and left heart dysfunction in a hospitalized COVID-19 patient’s echocardiogram, could be an independent predic- tor of death. In the early studies on COVID-19, age was considered to be a risk factor for mortality in patients (21, 22). However, age seems to be the prerequisite of changes in different tissues, rather than being an independent factor. While aging, an individual becomes more prone to cardiovascular disorders (23), and in case of SARS-CoV-2 infection, severe symptoms of the disease and cardiovascular manifestations are more likely to happen. In the present study, age was not indepen- dently correlated with mortality, as observed in multivariate analysis, but it may affect the patients as a dependent factor. Seemingly, various tissue changes in the elderly people cause serious complications following COVID-19 infection. Results of the present study suggest that respiratory and cardiovascular monitoring should be performed for COVID- 19 patients, as early as possible; some of the patients may have underlying cardiovascular disorders without showing any significant respiratory symptoms (8). Accordingly, in ad- dition to pulmonary CT scans, cardiovascular evaluations are recommended in the process of patient care. This matter is of utmost importance when patients have a positive history for cardiovascular disorders. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem M. Pishgahi et al. 4 5. Limitations Several limitations are present in the current study. In this study, echocardiography assessments were performed on different days of hospital admission for different patients, and were carried out only when the patient’s status had wors- ened. Anyhow, the present study is a preliminary study, aiming to provide evidences of cardiovascular involvement in COVID-19 patients. In addition, measurement of RV di- latation is very difficult in ICU patients, lying on their back. Moreover, the effect of ventilation on RV dilatation is another factor that could influence the validity of findings. Therefore, more clinical and laboratory factors should be taken into ac- count in future studies. 6. Conclusion Our study showed that cardiac involvement is a preva- lent complication among COVID-19 patients. In addition, echocardiography findings are independent prognostic fac- tors in prediction of in-hospital mortality. Since echocardio- graphy is an easy and accessible method, echocardiography monitoring of COVID-19 patients can be used as a screening tool for detection of high-risk patients. 7. Declarations 7.1. Acknowledgement The personnel of Cardiology Departments of Shohadaye Tajr- ish and Modarres Hospitals, who helped us in management of these patients, are thanked and appreciated. 7.2. Author contribution Study design and data gathering: MP, SS, MY Analysis: SS and MY Interpreting the results: All authors. Drafting: MY and SS Critically revised: All authors All authors read and approved the final version of the paper to be submitted. 7.3. Conflict of interest None. 7.4. Funding This study was support by vice chancellor of research and technology, Shahid Beheshti University of Medical Sciences (grant number: 23317). References 1. World Metrics. COVID-19 coronavirus out- break: World Metrics; [Available from: https://www.worldometers.info/coronavirus/. 2. Ai T, Yang Z, Hou H, Zhan C, Chen C, Lv W, et al. Corre- lation of chest CT and RT-PCR testing in coronavirus dis- ease 2019 (COVID-19) in China: a report of 1014 cases. Radiology. 2020:200642. 3. 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Pishgahi et al. 6 Table 1: Baseline characteristics of included COVID-19 patients Variable Survived (n=623) Died (n=57) Total (n=680) P value Age (year; mean and SD) 54.72±10.88 59.88±10.32 55.15±10.92 0.0006 28-39 54 (8.67) 1 (1.75) 55 (8.09) 40-49 173 (27.77) 11 (19.3) 184 (27.06) 50-59 153 (24.56) 19 (33.33) 172 (25.29) 60-69 185 (29.7) 13 (22.81) 198 (29.12) 70-79 58 (9.31) 13 (22.81) 71 (10.44) Gender Male 392 (62.92) 37 (64.91) 429 (63.09) 0.766 Female 231 (37.08) 20 (35.09) 251 (36.91) Comorbidity Ischemic heart disease No 538 (86.36) 30 (52.63) 568 (83.53) <0.0001 Yes 85 (13.64) 27 (47.37) 112 (16.47) Diabetes mellitus No 478 (76.73) 35 (61.4) 513 (75.44) 0.010 Yes 145 (23.27) 22 (38.6) 167 (24.56) Hypertension No 362 (58.11) 20 (35.09) 382 (56.18) 0.001 Yes 261 (41.89) 37 (64.91) 298 (43.82) CT involvement (%) <50 409 (65.65) 19 (33.33) 428 (62.94) 0.0001* 50-70 172 (27.61) 19 (33.33) 191 (28.09) >70 42 (6.74) 19 (33.33) 61 (8.97) CT pulmonary angiogram No embolism 584 (93.74) 40 (70.18) 624 (91.76) 0.0001* Segmental/sub segment embolism 35 (5.62) 6 (10.53) 41 (6.03) Main pulmonary artery embolism 4 (0.64) 11 (19.3) 15 (2.21) Duration of hospitalization (day) 7.42±2.62 8.79±2.89 7.53±2.67 0.0002 Data are presented as mean ± standard deviation or frequency (%). CT: computed tomography; SD: standard deviation; *based on Kruskal–Wallis test. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 7 Archives of Academic Emergency Medicine. 2021; 9(1): e21 Table 2: Echocardiography findings in COVID-19 patients based on in-hospital mortality Variable Survived (n=623) Died (n=57) Total (n=680) P value Left ventricular EF (%) >50 501 (80.42) 23 (40.35) 524 (77.06) 0.0001* 40-50 69 (11.08) 19 (33.33) 88 (12.94) 30-40 40 (6.42) 7 (12.28) 47 (6.91) <30 13 (2.09) 8 (14.04) 21 (3.09) Left ventricular dilation No 586 (94.06) 46 (80.7) 632 (92.94) <0.0001 Yes 37 (5.94) 11 (19.3) 48 (7.06) Pleural effusion No 592 (95.02) 47 (82.46) 639 (93.97) <0.0001 Yes 31 (4.98) 10 (17.54) 41 (6.03) Right ventricular dilation No 535 (85.87) 19 (33.33) 554 (81.47) <0.0001 Yes 88 (14.13) 38 (66.67) 126 (18.53) Right ventricular clot No 622 (99.84) 55 (96.49) 677 (99.56) 0.020 Yes 1 (0.16) 2 (3.51) 3 (0.44) Tricuspid regurgitation No 542 (87.00) 20 (35.09) 562 (82.65) <0.0001 Yes 81 (13.00) 37 (64.91) 118 (17.35) PASP <35 572 (91.81) 39 (68.42) 611 (89.85) 0.0001 35-50 37 (5.94) 15 (26.32) 52 (7.65) >50 14 (2.25) 3 (5.26) 17 (2.5) IVC Size Normal 261 (41.89) 15 (26.32) 276 (40.59) <0.0001 Dilated 73 (11.72) 21 (36.84) 94 (13.82) Collapsed 289 (46.39) 21 (36.84) 310 (45.59) Data are presented as frequency (%); *based on Kruskal–Wallis test; IVC: Inferior vena cava; PASP: Pulmonary arterial systolic pressure; EF: ejection fraction. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem M. Pishgahi et al. 8 Table 3: Multivariate regression for identifying independent prog- nostic factors of COVID-19-related mortality Variable RR 95% CI P value History of ischemic heart diseases No Ref. Ref. Yes 1.14 1.08 - 1.19 <0.0001 History of hypertension No Ref. Ref. Yes 1.04 1.00 - 1.08 0.031 CT pulmonary angiogram No emboli Ref. Ref. Main pulmonary arteries emboli 1.53 1.35 - 1.74 <0.0001 CT involvement (%) <50 Ref. Ref. >70 1.08 1.01 - 1.16 0.023 Left ventricular EF (%) >50 Ref. Ref. <30 1.19 1.07 - 1.32 <0.0001 Pleural effusion No Ref. Ref. Yes 1.08 1.00 - 1.16 0.044 PASP (mmHg) <30 Ref. Ref. 35-50 1.11 1.03 - 1.18 <0.0001 Right ventricular dysfunction No Ref. Ref. Yes 1.54 1.40 - 1.70 <0.0001 IVC size Normal Ref. Ref. Collapsed 1.05 1.01 - 1.08 0.015 CI: Confidence interval; EF: Ejection fraction; IVC: Inferior vena cava; PASP: Pulmonary arterial systolic pressure; RR: relative risk; CT: computed tomography. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem Introduction Methods Results Discussion Limitations Conclusion Declarations References