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. 2021 Feb 13;9(1):e18. doi: 10.22037/aaem.v9i1.1071

Cardiac Complications and Pertaining Mortality Rate in COVID-19 Patients; a Systematic Review and Meta-Analysis

Amirmohammad Toloui 1, Donya Moshrefiaraghi 1, Arian Madani Neishaboori 1, Mahmoud Yousefifard 1,*, Mohammad Haji Aghajani 2,†
PMCID: PMC8035700  PMID: 33870205

Abstract

Introduction:

Raising knowledge over cardiac complications and managing them can play a key role in their recovery. In this study, we aim to investigate the evidence regarding the prevalence of cardiac complications and the resulting mortality rate in COVID-19 patients.

Method:

Search was conducted in electronic databases of Medline (using PubMed), Embase, Scopus, and Web of Science, in addition to the manual search in preprint databases, and Google and Google scholar search engines, for articles published from 2019 until April 30th, 2020. Inclusion criterion was reviewing and reporting cardiac complications in patients with confirmed COVID-19.

Results:

The initial search resulted in 853 records, out of which 40 articles were included. Overall analysis showed that the prevalence of acute cardiac injury, heart failure and cardiac arrest were 19.46% (95% CI: 18.23-20.72), 19.07% (95% CI: 15.38-23.04) and 3.44% (95% CI: 3.08-3.82), respectively. Moreover, abnormal serum troponin level was observed in 22.86% (95% CI: 21.19-24.56) of the COVID-19 patients. Further analysis revealed that the overall odds of mortality is 14.24 (95% CI: 8.67-23.38) times higher when patients develop acute cardiac injury. The pooled odds ratio of mortality when the analysis was limited to abnormal serum troponin level was 19.03 (95% CI: 11.85-30.56).

Conclusion:

Acute cardiac injury and abnormal serum troponin level were the most prevalent cardiac complications/abnormalities in COVID-19 patients. The importance of cardiac complications is emphasized due to the higher mortality rate among patients with these complications. Thus, troponin screenings and cardiac evaluations are recommended to be performed in routine patient assessments.

Key Words: COVID-19, Cardiovascular System, Heart Injuries, Hospital Mortality

Introduction

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a novel coronavirus, which emerged in Wuhan, China in December 2019 and has spread to over 200 countries in the world, ever since (1). Coronavirus disease 2019 (COVID-19) mostly causes lower respiratory tract infection symptoms such as fever, which is its most prevalent symptom, cough, and dyspnea (2). Although people with severe type of the disease form the minority of the patients, it is illustrated that mortality rate is the highest among patients who have comorbidities such as cardiovascular diseases (3).

Angiotensin converting enzyme 2 (ACE2) has been shown to be the receptor of the virus in human cells. Since this enzyme is expressed in many organs such as lungs, heart, kidneys and brain, extrapulmonary manifestations and complications are being studied rigorously, all around the world (4). Cardiac involvement is one of the most common causes of death in COVID-19 patients (5). Cardiovascular complications, whether being chronic or acute, can lead to critically imbalanced homeostasis and could be a serious strike to patient’s recovery from the disease (6). Therefore, raising awareness over cardiac complications caused by the disease and managing them as early as possible can play a key role in recovery of the patients. However, there is no comprehensive evaluation of this issue. Therefore, in this study, we aim to investigate the evidence regarding the prevalence of cardiac complications in COVID-19 patients. Moreover, the risk of mortality after COVID-19 related cardiac involvement has also been assessed.

Methods

Study design

The present systematic review and meta-analysis aims to investigate the evidence regarding cardiac complications in patients, confirmed with COVID-19, and to see whether there is any potential association between the prevalence of cardiac complications and their mortality rate. As a result, PECO in the current study is defined as: P (patients): Patients with confirmed COVID-19 disease, E (exposure): SARS-CoV-2 infection, O (outcome): prevalence of cardiac complications and mortality after COVID-19 related cardiac involvement. As for comparison (C in PECO), mortality rate was compared between COVID-19 patients with cardiac complications and patients without any cardiac involvements.

Search strategy

The searching process was initiated by selecting keywords with the help of experts in the field and screening titles of similar articles. Then, using MeSH and Emtree, equivalent and related synonyms were identified. As a result, a search strategy was constructed based on the instructions of electronic databases of Medline, Embase, Scopus, and Web of Science, and an extensive search was performed in each of the mentioned databases for articles published from the February 1st of 2019 until April 30th, 2020. The search strategy in Medline database through PubMed search engine is presented in Appendix 1. In addition, a search was performed in preprint databases, Google, and Google scholar to obtain preprinted and possibly missed manuscripts (gray litterateur search). Moreover, references of the obtained review articles were screened to find additional articles.

Appendix 1.

Medline search query

Search terms

  1. “COVID-19 “[Supplementary Concept] OR ”severe acute respiratory syndrome coronavirus 2”[Supplementary Concept] OR ”COVID-19 vaccine”[Supplementary Concept] OR ”COVID-19 diagnostic testing”[Supplementary Concept] OR ”COVID-19 drug treatment”[Supplementary Concept] OR “Betacoronavirus”[mh] OR “Coronavirus Infections”[mh] OR COVID-19[tiab] OR 2019 novel coronavirus disease[tiab] OR COVID19[tiab] OR COVID-19 pandemic[tiab] OR SARS-CoV-2 infection[tiab] OR COVID-19 virus disease[tiab] OR 2019 novel coronavirus infection[tiab] OR 2019-nCoV infection[tiab] OR coronavirus disease 2019[tiab] OR coronavirus disease-19[tiab] OR 2019-nCoV disease[tiab] OR COVID-19 virus infection[tiab] OR Severe Acute Respiratory Syndrom Coronavirus 2[tiab] OR Coronavirus[tiab] OR Coronaviruses[tiab] OR severe acute respiratory syndrome coronavirus 2[tiab] OR 2019-nCoV[tiab] OR Wuhan coronavirus[tiab] OR SARS-CoV-2[tiab] OR 2019 novel coronavirus[tiab] OR COVID-19 virus[tiab] OR coronavirus disease 2019 virus[tiab] OR COVID19 virus[tiab] OR Wuhan seafood market pneumonia virus[tiab] OR Betacoronavirus[tiab] OR Betacoronaviruses[tiab] OR Coronavirus Infections[tiab] OR Coronavirus Infection[tiab] OR Infection, Coronavirus[tiab] OR Infections, Coronavirus[tiab] OR COVID-19 vaccine[tiab] OR COVID-19 diagnostic testing[tiab] OR COVID-19 drug treatment[tiab] OR coronavirus disease 2019 drug treatment[tiab] OR Covid-19 treatment[tiab] OR treatment of Covid-19 virus infection[tiab] OR coronavirus disease-19 drug treatment[tiab]

  2. “Troponin”[mh] OR “Heart Injuries”[mh] OR “Myocarditis”[mh] OR “Cardiomyopathies”[mh] OR “Heart Diseases”[mh] OR “Pericarditis”[mh] OR “Cardiovascular Abnormalities”[mh] OR “Cardiovascular Infections”[mh] OR “Cardiovascular Diseases”[mh] OR “Heart Arrest”[mh] OR “Ventricular Dysfunction”[mh] OR “Heart Failure”[mh] OR “Heart Failure, Diastolic”[mh] OR “Heart Failure, Systolic”[mh] OR Heart Injuries[tiab] OR [tiab] OR Injuries, Heart[tiab] OR Heart Injury[tiab] OR Injury, Heart[tiab] OR Myocarditis[tiab] OR Myocarditides[tiab] OR Carditis[tiab] OR Cardiomyopathies[tiab] OR Cardiomyopathy[tiab] OR Myocardial Diseases[tiab] OR Disease, Myocardial[tiab] OR Diseases, Myocardial[tiab] OR Myocardial Disease[tiab] OR Myocardiopathies[tiab] OR Myocardiopathy[tiab] OR Cardiomyopathies, Secondary[tiab] OR Cardiomyopathy, Secondary[tiab] OR Secondary Cardiomyopathies[tiab] OR Secondary Cardiomyopathy[tiab] OR Secondary Myocardial Diseases[tiab] OR Disease, Secondary Myocardial[tiab] OR Diseases, Secondary Myocardial[tiab] OR Myocardial Disease, Secondary[tiab] OR Secondary Myocardial Disease[tiab] OR Myocardial Diseases, Secondary[tiab] OR Heart Diseases[tiab] OR Heart Disease[tiab] OR Cardiac Diseases[tiab] OR Cardiac Disease[tiab] OR Cardiac Disorders[tiab] OR Cardiac Disorder[tiab] OR Heart Disorders[tiab] OR Heart Disorder[tiab] OR Pericarditis[tiab] OR Pleuropericarditis[tiab] OR Endocarditis[tiab] OR Endocarditides[tiab] OR Infective Endocarditis[tiab] OR Endocarditides, Infective[tiab] OR Endocarditis, Infective[tiab] OR Infective Endocarditides[tiab] OR Heart damage[tiab] OR Cardiac injury[tiab] OR Acute cardiac injury[tiab] OR Cardiovascular Abnormalities[tiab] OR Abnormalities, Cardiovascular[tiab] OR Abnormality, Cardiovascular[tiab] OR Cardiovascular Abnormality[tiab] OR Cardiovascular Infections[tiab] OR Cardiovascular Infection[tiab] OR Infection, Cardiovascular[tiab] OR Infections, Cardiovascular[tiab] OR Cardiovascular Diseases[tiab] OR Cardiovascular Disease[tiab] OR Disease, Cardiovascular[tiab] OR Diseases, Cardiovascular[tiab] OR Heart Arrest[tiab] OR Arrest, Heart[tiab] OR Cardiac Arrest[tiab] OR Arrest, Cardiac[tiab] OR Asystole[tiab] OR Asystoles[tiab] OR Cardiopulmonary Arrest[tiab] OR Arrest, Cardiopulmonary[tiab] OR Ventricular Dysfunction[tiab] OR Dysfunction, Ventricular[tiab] OR Dysfunctions, Ventricular[tiab] OR Ventricular Dysfunctions[tiab] OR Heart Failure[tiab] OR Diastolic Heart Failures[tiab] OR Heart Failures, Diastolic[tiab] OR Diastolic Heart Failure[tiab] OR Heart Failure, Diastolic[tiab] OR Cardiac Failure[tiab] OR Heart Decompensation[tiab] OR Decompensation, Heart[tiab] OR Heart Failure, Right-Sided[tiab] OR Heart Failure, Right Sided[tiab] OR Right-Sided Heart Failure[tiab] OR Right Sided Heart Failure[tiab] OR Myocardial Failure[tiab] OR Congestive Heart Failure[tiab] OR Heart Failure, Congestive[tiab] OR Heart Failure, Left-Sided[tiab] OR Heart Failure, Left Sided[tiab] OR Left-Sided Heart Failure[tiab] OR Left Sided Heart Failure[tiab] OR Heart Failure, Systolic[tiab] OR Heart Failures, Systolic[tiab] OR Systolic Heart Failures[tiab] OR Systolic Heart Failure[tiab] OR Troponin[tiab] OR Troponins[tiab] OR Troponin Complex[tiab]

  3. #1 AND #2

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Selection criteria

The inclusion criteria in the present meta-analysis was reporting cardiac complications and cardiac related mortality rate in patients with confirmed COVID-19. Original observational studies were included. Since most COVID-19 studies had a retrospective nature, both retrospective and prospective studies were included. Prevalence of cardiac complications following COVID-19 and its pertaining mortality rate were extracted from cohort and cross-sectional studies. In addition, we added an extra aim to provide evidence on the relationship between cardiac complication occurrence in COVID-19 patients and their mortality. In this section, in addition to cohort and cross-sectional studies, case-control studies were also included. Furthermore, the exclusion criteria were case report studies, review articles, studies that did not report cardiac involvement and studies whose entire target population was patients with cardiac comorbidities as underlying disease.

Data collection

Two independent reviewers screened titles and abstracts of the gathered articles. Then, full texts of the related articles were obtained and included articles were selected and entered the present systematic review and meta-analysis. Finally, a summary of the included studies was recorded using a checklist, consisting of following variables: first author’s name, publication year, country in which the study was conducted in, number of patients, study design, number of patients in which the cardiac complication was assessed in, mean/median age of the patients, number of males among the patients, type of cardiac complication along with its diagnostic method, number of the deceased in patients presenting with cardiac complication (if reported), and number of the deceased among patients without the cardiac complication of the included articles. If several types of cardiac complications were reported in the studies, the number of each cardiac involvement was recorded separately. Any disagreements within the process were resolved using a third reviewer’s opinion.

Outcome

The primary outcome of the present meta-analysis was the prevalence of cardiac complications in COVID-19 patients. Secondary outcome was the risk of mortality after COVID-19 related cardiac involvement. Our screening showed that most studies reported abnormal serum troponin level and acute cardiac injury, separately, as cardiac assessments/complications. Other reported cardiac complications were heart failure, cardiomyopathy, cardiac arrest, myocarditis, pericardial effusion, cardiac insufficiency, and myocardial infarction.

Quality assessment

Two independent reviewers scored the quality of the studies according to National Heart, Lung, and Blood Institute (NHLBI) quality assessment tool (7). This tool contains 14 items on study design, patient selection, sample size justification, analysis, timeframe between exposure and outcome, assessment of different level of exposure, validity and reliability of exposure and outcome assessment, blinding status, missing data management, and considering potential confounders in the analysis. Each reviewer independently assessed the articles and categorized each item as low risk, high risk, unclear risk of bias, cannot determine, or not applicable. Any disagreement was resolved by discussion with a third reviewer.

Statistical analysis

All analyses were performed using STATA 14.0 statistical program. Analyses were performed in two parts. Initially, the cardiac complications reported in the articles were categorized into 9 subgroups: acute cardiac injury, abnormal serum troponin level, heart failure, cardiac arrest, myocarditis, cardiac insufficiency, pericardial effusion, myocardial infarction, and cardiomyopathy. The prevalence of each cardiac complication among the COVID-19 patients was calculated with a 95% confidence interval (95% CI) using the “metaprop_one” command performed on the total sample size and the number of patients presenting each complication in the included articles.

In the second part of the analysis, the association between the manifestation of cardiac complications/abnormalities and mortality rate was calculated and presented as an overall odds ratio (OR) with a 95% CI using the “metan” command performed on four groups of data: number of the deceased in patients with a cardiac complication, number of the alive in patients with the cardiac complication, number of the deceased in patients without the cardiac complication, number of the alive in patients without the cardiac complication. I2 test was performed to assess heterogeneity, and if the heterogeneity among data was considerable, random effect model was used to calculate 95% CI. Egger’s test was used to evaluate publication bias. Finally, a sensitivity analysis was performed to determine whether the results can be considered robust or not. Therefore, in the sensitivity analyses we excluded possible outlier studies.

Results

Study characteristics

The systematic search resulted in 853 records, and after eliminating duplicates, 557 articles remained. Then, after screening titles and abstracts of the remaining articles, 181 studies were deemed potentially eligible. Afterwards, based on the mentioned exclusion and inclusion criteria, 40 articles were included in the present systematic review and meta-analysis (Figure 1) (5, 8-46). These 40 articles were treated as 60 different experiments, as some studies reported more than one cardiac complication/abnormality. Two studies had taken place in the United States (41, 45), one study was conducted in Spain (9), one study was carried out in Italy (42) and the rest of the included studies were conducted in China. Regarding the study design of the included articles, one study was ambispective (22), four studies were conducted prospectively (9, 14, 19, 39) and the other 35 studies were retrospective. Overall, 15616 patients with confirmed COVID-19 were enrolled in the included studies, with 2985 males among them [patients’ gender was not reported in two of the studies (42, 46)]; however, not all of the patients were assessed for each cardiac complication, so the total number of patients tested for each manifestation is presented for each complication in Table 1. In general, 9 different cardiac complications/abnormalities were reported in the studies including acute cardiac injury, which was reported in 26 studies (5, 8, 11, 13, 16, 18-20, 22-24, 26-30, 32, 33, 35, 37-41, 43, 46), abnormal serum troponin level, reported in 19 studies (8, 10-12, 14, 15, 17, 19, 25, 30, 32, 36-38, 40, 41, 43-45), heart failure, reported in four studies (8, 11, 32, 41), cardiac arrest, reported in three studies (5, 34, 42), myocarditis, reported in two studies (9, 44), cardiac insufficiency, reported in two studies (29, 30), pericardial effusion, reported in two studies (21, 31) and cardiomyopathy (45) and myocardial infarction (32), each reported in one study. Mortality rate was reported in 18 studies (8, 11, 13, 14, 16-18, 20, 26, 29, 30, 33, 34, 37, 39, 40, 44, 46). These numbers were further used to evaluate the odds ratio (OR) between the manifestation of each cardiac complication and the mortality rate in COVID-19 patients. Table 1 demonstrates a summary of the characteristics of the included studies.

Figure 1.

Figure 1

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Flow diagram of the present meta-analysis; CVD: Cardiovascular disease

Table 1.

Summary of the included studies

Author; Year; Country Study design Total study population Mean age Number of males Diagnostic methods Type of cardiac complication No. of patients tested for the complication No. of patients with the complication No. of deceased in patients with the complication No. of deceased in patients without the complication
Aggarwal S; 2020; USA Retrospective 16 67 12 Blood Sample, Echo Acute cardiac injury 16 3 NR NR
NR Heart failure 16 2 NR NR
Blood Sample Abnormal Troponin 16 10 NR NR
Arentz M; 2020; USA Retrospective 21 70 11 Blood Sample, Echo, Clinical Cardiomyopathy 21 7 NR NR
Blood Sample Abnormal Troponin 21 3 NR NR
Baldi E; 2020; Italy Retrospective 9806 NR NR Hospital report Cardiac arrest 9806 362 NR NR
Barrasa H; 2020; Spain Prospective 48 63.2 27 NR Myocarditis 48 1 NR NR
Chen C; 2020; China Retrospective 150 59 84 Blood Sample Abnormal Troponin 150 22 NR NR
Chen T; 2020; China Retrospective 274 62 171 NR Acute cardiac injury 203 89 72 22
NR Heart failure 176 43 41 42
Blood Sample Abnormal Troponin 203 83 68 26
Deng Q; 2020; China Retrospective 112 65 57 Blood Sample Abnormal Troponin 112 42 NR NR
Deng Y; 2020; China Retrospective 225 54 124 Blood Sample Acute cardiac injury 225 66 65 44
Du Ra; 2020; China Prospective 179 57.6 97 Blood Sample Abnormal Troponin 179 31 13 8
Du Rb; 2020; China Retrospective 109 70.7 75 Blood Sample Abnormal Troponin 109 52 NR NR
Du Y; 2020; China Retrospective 85 65.8 62 Blood Sample Acute cardiac injury 85 38 NR NR
Clinical Cardiac arrest 85 7 NR NR
Guo T; 2020; China Retrospective 187 58.5 91 Blood Sample Acute cardiac injury 187 52 31 12
Han H; 2020; China Retrospective 273 NR 97 Blood Sample Abnormal Troponin 273 27 13 8
He X; 2020; China Retrospective 54 68 34 Blood Sample Acute cardiac injury 54 24 18 8
Hu L; 2020; China Retrospective 323 61 166 Blood Sample Acute cardiac injury 323 24 NR NR
Blood Sample Abnormal Troponin 323 68 NR NR
Huang C; 2020; China Prospective 41 49 30 Blood Sample Abnormal Troponin 41 5 NR NR
Acute cardiac injury 41 5 NR NR
Lei S; 2020; China Retrospective 34 55 14 Blood Sample Acute cardiac injury 34 5 4 3
Li K; 2020; China Retrospective 83 45.5 44 CT Pericardial effusion 83 4 NR NR
Li X; 2020; China Ambispective 548 60 279 Blood Sample Acute cardiac injury 548 119 NR NR
Li Y; 2020; China Retrospective 54 61.8 34 Blood Sample Acute cardiac injury 41 23 NR NR
Liu M; 2020; China Retrospective 30 35 10 Blood Sample Acute cardiac injury 30 5 NR NR
Liu Y; 2020; China Retrospective 76 45 49 Blood Sample Abnormal Troponin 76 14 NR NR
Ma K; 2020; China Retrospective 84 48 48 Blood Sample Abnormal Troponin 84 36 0 0
Blood Sample, Clinical Symptom Myocarditis 84 4 0 0
Ruan Q; 2020; China Retrospective 150 NR NR NR Acute cardiac injury 68 5 5 63
Shi S; 2020; China Retrospective 416 64 205 Blood Sample Acute cardiac injury 416 82 42 15
Wan S; 2020; China Retrospective 135 47 72 Blood Sample Acute cardiac injury 135 10 NR NR
Wang Da; 2020; China Retrospective 138 56 75 Blood Sample, ECG, Echo Acute cardiac injury 138 10 NR NR
Wang Db; 2020; China Retrospective 107 51 57 Blood Sample Abnormal Troponin 107 6 5 14
Blood Sample, ECG, Echo Acute cardiac injury 12 8 19
Wang La; 2020; China Retrospective 339 69 166 Blood Sample Acute cardiac injury 339 70 39 26
Blood Sample, Clinical Symptom Cardiac insufficiency 339 58 25 52
Wang Lb; 2020; China Retrospective 202 63 88 Blood Sample Acute cardiac injury 202 27 17 14
Blood Sample, ECG, Echo Cardiac insufficiency 202 24 14 19
Blood Sample Abnormal Troponin 202 27 NR NR
Wei J; 2020; China Prospective 101 49 54 Blood Sample Acute cardiac injury 101 16 3 0
Xu X; 2020; China Retrospective 90 50 39 CT Pericardial effusion 90 1 NR NR
Yang F; 2020; China Retrospective 92 69.8 49 Blood Sample Acute cardiac injury 92 31 NR NR
NR Myocardial infarction 92 6 NR NR
NR Heart failure 92 2 NR NR
Blood Sample Abnormal Troponin 92 31 NR NR
Yang X; 2020; China Retrospective 52 59.7 35 Blood Sample Acute cardiac injury 52 12 9 23
Yao W; 2020; China Retrospective 202 63.4 136 Clinical Cardiac arrest 202 4 0 21
Zhang G; 2020; China Retrospective 221 55 108 NR Acute cardiac injury 221 17 NR NR
Zhao X; 2020; China Retrospective 91 46 49 Blood Sample Acute cardiac injury 91 14 NR NR
Blood Sample Abnormal Troponin 88 3 NR NR
Zheng Y; 2020; China Retrospective 99 49.4 51 Blood Sample Abnormal Troponin 99 88 NR NR
Zhou F; 2020; China Retrospective 191 56 119 Blood Sample Abnormal Troponin 145 24 23 31
Heart failure 145 44 28 26
Acute cardiac injury 145 33 32 22
Zou X; 2020; China Retrospective 178 60.68 67 Blood Sample, ECG, Echo Acute cardiac injury 154 45 34 18
Blood Sample Abnormal Troponin 154 33 28 24
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CT: Computed tomography scan; Echo: Echocardiography; ECG: Electrocardiography; NR: Not reported

Risk of bias assessment

No study had provided a sample size justification, power description, or variance and effect estimates. In addition, 39 studies were not measured to have key potential confounders in their assessment of outcomes. 10 studies did not report the details of their inclusion and exclusion criteria. Moreover, the participation rate of eligible persons was not reported in 6 studies (Table 2).

Table 2.

Risk of bias assessment of included studies

Author; Year Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9 Item 10 Item 11 Item 12 Item 13 Item 14
Aggarwal S; 2020 Yes Yes No Yes No Yes Yes NA Yes NA Yes NA Yes No
Arentz M; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Baldi E; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Barrasa H; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Chen C; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Chen T; 2020 Yes Yes No Yes No Yes Yes NA Yes NA Yes NA Yes No
Deng Q; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Deng Y; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Du Ra; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Du Rb; 2020 Yes Yes No Yes No Yes Yes NA Yes NA Yes NA Yes No
Du Y; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Guo T; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Han H; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
He X; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Huang C; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Hu L; 2020 Yes Yes Yes Yes No Yes Yes NA No NA Yes NA Yes No
Lei S; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Li K; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Liu M; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Liu Y; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Li X; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Li Y; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Ma K; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Ruan Q; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Shi S; 2020 Yes Yes No Yes No Yes Yes NA Yes NA Yes NA Yes No
Wang Da; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Wang Db; 2020 Yes Yes No No No Yes Yes NA Yes NA Yes NA Yes No
Wang La; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Wang Lb; 2020 Yes Yes Yes Yes No Yes No NA Yes NA Yes NA Yes No
Wan S; 2020 Yes Yes Yes Yes No Yes No NA Yes NA Yes NA Yes No
Wei J; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Xu X; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Yang F; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes Yes
Yang X; 2020 Yes Yes No Yes No Yes Yes NA Yes NA Yes NA Yes No
Yao W; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Zhang G; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Zhao X; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Zheng Y; 2020 Yes Yes Yes No No Yes Yes NA Yes NA Yes NA Yes No
Zhou F; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
Zou X; 2020 Yes Yes Yes Yes No Yes Yes NA Yes NA Yes NA Yes No
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NA: Not applicable.

Items:

1. Was the research question or objective in this paper clearly stated?

2. Was the study population clearly specified and defined?

3. Was the participation rate of eligible persons at least 50%?

4. Were all the subjects selected or recruited from the same or similar populations (including the same time period)? Were inclusion and exclusion criteria for being in the study prespecified and applied uniformly to all participants?

5. Was a sample size justification, power description, or variance and effect estimates provided?

6. For the analyses in this paper, were the exposure(s) of interest measured prior to the outcome(s) being measured?

7. Was the timeframe sufficient so that one could reasonably expect to see an association between exposure and outcome if it existed?

8. For exposures that can vary in amount or level, did the study examine different levels of the exposure as related to the outcome (e.g., categories of exposure, or exposure measured as continuous variable)?

9. Were the exposure measures (independent variables) clearly defined, valid, reliable, and implemented consistently across all study participants?

10. Was the exposure(s) assessed more than once over time?

11. Were the outcome measures (dependent variables) clearly defined, valid, reliable, and implemented consistently across all study participants?

12. Were the outcome assessors blinded to the exposure status of participants?

13. Was loss to follow-up after baseline 20% or less?

14. Were key potential confounding variables measured and adjusted statistically for their impact on the relationship between exposure(s) and outcome(s)?

Publication bias

There were evidences of publication bias in the assessment of the prevalence of acute cardiac injury (Coefficient= -3.97; p=0.004) and abnormal serum troponin level (Coefficient = -8.65; p < 0.001) among the included studies. However, no evidence of publication bias was observed in the assessment of cardiac related mortality and the prevalence of other cardiac complications (Figure 2).

Figure 2.

Figure 2

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Funnel plot for publication bias in prevalence of cardiac complications in COVID-19 patients and mortality rate after incidence of cardiac manifestation. There are evidences of publication bias among the studies, which reported prevalence of cardiac complications. While, no publication bias was observed regarding the relationship of cardiac complication and mortality in COVID-19 patients

Meta-analysis

In the beginning, the prevalence of cardiac complications following SARS-CoV-2 infection was evaluated, and the results are depicted in figures 3, 4, 5 and 6, and table 3. Abnormal serum level of troponin was observed in 22.86% (95% CI: 21.19 to 24.56) of the patients (Figure 4). Moreover, the prevalence of acute cardiac injury, heart failure and cardiac arrest was 19.46% (95% CI: 18.23 to 20.72), 19.07% (95% CI: 15.38 to 23.04) and 3.44% (95% CI: 3.08 to 3.82), respectively (Figure 3 and Table 3). Furthermore, the I2 test revealed no heterogeneity regarding the prevalence of abnormal troponin levels and acute cardiac injury. The prevalence of other cardiac complications including myocarditis, cardiac insufficiency, pericardial effusion, myocardial infarction, and cardiomyopathy are depicted in Table 3. Sensitivity analysis showed that after excluding the studies with a high prevalence rate, the prevalence of abnormal serum level of troponin (20.16%; 95% CI: 18.54 to 21.82; cut off for high prevalence rate=50%) and acute cardiac injury (17.17%; 95% CI: 15.94 to 18.43; cut off for high prevalence rate=30) decreased slightly.

Figure 3.

Figure 3

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Forest plot for the assessment of the prevalence of acute cardiac injury in COVID-19 patients; CI: confidence interval

Figure 4.

Figure 4

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Forest plot for the assessment of the prevalence of abnormal troponin levels in COVID-19 patients; CI: confidence interval

Figure 5.

Figure 5

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Forrest plot for the assessment of risk of mortality in COVID-19 patients with acute cardiac injury; OR: odds ratio; CI: confidence interval

Figure 6.

Figure 6

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Forrest plot for the assessment of risk of mortality in COVID-19 patients with abnormal troponin level; OR: odds ratio; CI: confidence interval

Table 3.

Summary of findings regarding cardiac complications in COVID-19

Complication Number of studies Prevalence 95% CI Number of studies Odds ratio 95% CI P
Acute cardiac injury 26 19.46 18.23, 20.72 14 14.24 8.67, 23.38 <0.001
Abnormal troponin 19 22.86 21.19, 24.56 6 19.03 11.85, 30.56 <0.001
Heart failure 4 19.07 15.38, 23.04 2 10.66 5.69, 19.97 <0.001
Cardiac arrest 3 3.44 3.08, 3.82 1 0.04 0.00, >999.0 0.651
Myocarditis 2 3.66 0.88, 7.82 1 1.00 0.00, >999.0 >0.99
Pericardial effusion 2 2.62 0.58, 5.73 --- --- --- ---
Cardiac insufficiency 2 15.06 12.15, 18.22 2 4.65 2.82, 7.66 <0.001
Cardiomyopathy 1 33.33 17.19, 54.63 --- --- --- ---
Myocardial infarction 1 6.52 3.02, 13.51 --- --- --- ---
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---: No data; CI: Confidence interval

Further analysis revealed that the odds of mortality in COVID-19 patients with acute cardiac injury is 14.24 (OR = 14.24, 95% CI: 8.67 to 23.38) times higher than the COVID-19 patients without acute cardiac injury. However, I2 test showed some degrees of heterogeneity regarding the relationship of cardiac complication and mortality of COVID-19 patients (Figure 5). There is a possible outlier study in acute cardiac injury section. After excluding this study, the odds of mortality in COVID-19 patients with acute cardiac injury is increased slightly (OR=15.77; 95% CI: 10.49 to 23.69). In the sensitivity analysis the heterogeneity was decreased (I2=45.5%).

Moreover, the odds of mortality in a COVID-19 patient presenting with abnormal serum troponin level in his/her blood sample was 19.03 (OR=19.03; 95% CI: 11.85 to 30.56) times higher than the patients not having this manifestation. Interestingly, no heterogeneity was observed when calculating the OR for the mortality in COVID-19 patients with abnormal serum troponin level (Figure 6). There are two possible outlier studies in abnormal troponin level section. After excluding these studies, the odds of mortality in COVID-19 patients with acute cardiac injury is increased slightly (OR=17.07; 95% CI: 10.41 to 27.99). The odds of mortality of patients having other cardiac complications are presented in Table 3.

Discussion

In this systematic review and meta-analysis, we investigated the prevalence of 9 cardiac complications in COVID-19 patients and their subsequent mortality rates. Abnormal serum level of troponin with 22.86% prevalence, detected by laboratory tests, and acute cardiac injury with 19.46% prevalence, diagnosed with laboratory test results and other diagnostic techniques, were among the most prevalent complications/abnormalities observed in COVID-19 patients. Although a large number of studies reported the prevalence of the two mentioned cardiac complications, no heterogeneity was observed in this section. To contemplate even more on the matter, the prevalence of abnormal troponin level and acute cardiac injury are rather close numbers, which might mean that by close observation of troponin changes in a COVID-19 patient, we could possibly anticipate acute cardiac injuries in them and take appropriate measures. However, serum troponin levels also increase due to damage to other tissues, such as the kidneys, which may make it impossible to use troponin level alone to detect cardiac damage. Other cardiac complications such as heart failure and cardiomyopathy were also prevalent among the patients. However, with the small number of the studies observing them, more data is needed on the matter.

Regarding the limitations, each individual article used a different reference range for troponin or other injury indicators to be classified as abnormal, and each one used different diagnostic and laboratory test results to define acute cardiac injury, which could cause slight differences in the reported prevalence of acute cardiac injury and abnormal serum level of troponin. For example, Huang et al. defined acute cardiac injury as cardiac troponin rising to 3 or more times than normal or appearance of new abnormalities in echocardiography or ECG (19); While many others defined it only with the appearance of abnormal troponin levels in blood samples. Moreover, some articles’ study population only consisted of critically ill patients or deceased ones, which could shift prevalence statistics, causing inevitable heterogeneity in reported numbers (5, 15, 32). Additionally, it is worth mentioning that the mechanism of myocardial injury, whether being done by direct viral invasion to the host tissue or due to imbalanced homeostasis, was of no concern for the writers at the time. Although more research should be conducted to identify the exact causes of this damage, the effects it carries are the most important subject that should be studied at these critical times. Even though limitations were present in data reporting the prevalence of cardiac outcomes, it is important to pay enough attention to these complications, since many of them are directly related to patients’ general situation and illness severity.

On the other hand, our study shows intriguing data regarding mortality rate in patients presenting with cardiac complications, especially acute cardiac injury and abnormal serum level of troponin. Abnormal troponin levels are associated with about 19 times higher mortality risk in COVID-19 patients, which is of great importance in disease management for health care providers around the world. Considering the fact that no heterogeneity was observed regarding the risk of mortality in patients with abnormal troponin level, laboratory screening during routine patient assessments can be critical in early detection of cardiac injury and intervening accordingly. In addition, we suggest that blood levels of troponin should be evaluated as a prognostic factor in patients with cardiac involvement.

Furthermore, our data indicated that acute cardiac injury could raise the mortality to about 14 times more in COVID-19 patients. However, this number was associated with an overall heterogeneity, which could be attributed to different definitions of cardiac injury in studies, discussed above. Nonetheless, although one can conclude that there is a relationship between acute cardiac injury following COVID-19 and increased risk of mortality, the threat that acute cardiac injury poses to patients’ health status in the future is undeniable and demands careful monitoring and managements when confronting this situation. Moreover, it is noteworthy that articles reporting mortality rates of cardiac complications were mostly focused on abnormal troponin level and myocardial injury and the number of the articles reporting correlations between other cardiac complications such as heart failure, and mortality rate was very few; so, we cannot present an exact estimation of the contribution of other cardiac outcomes such as heart failure and myocarditis to patients’ fatality. In addition, inability to blind the outcome assessors in the studies and some articles not explicitly presenting inclusion and exclusion criteria were further limitations detected in the studies.

Finally, we performed a sensitivity analysis and excluded possible outlier studies. The overall effect size slightly changed and therefore, the results seem to be robust.

To conclude, our findings thoroughly approve of other published articles investigating associations between COVID-19 cardiac outcomes and related mortalities (47, 48), confirming that cardiac injury, regardless of the mechanism of establishment, is a factor determining disease severity and patient prognosis reliably in large scale and should be considered and monitored from early stages of disease.

Conclusion

Cardiac complications/abnormalities can be prevalent in COVID-19 patients in the forms of acute cardiac injury, serum troponin levels abnormalities, heart failure, cardiac arrest, and other types. The importance of cardiac involvements is further highlighted when observing the higher mortality rate among COVID-19 patients presenting with cardiac involvements. Thus, careful monitoring of heart involvements should be performed in COVID-19 patients.

Abbreviations

SARS-CoV-2: Severe Acute Respiratory Syndrome Coronavirus 2

COVID-19: Coronavirus disease 2019

ACE2: Angiotensin Converting Enzyme 2

PECO: Problem, Exposure, Comparison, Outcome

NHLBI: National Heart, Lung, and Blood Institute

CI: Confidence Interval

OR: Odds Ratio

ECG: Electrocardiography

Ethics approval and consent to participate

This study received ethics approval from Ethics committee of Iran University of medical Sciences.

Consent for publication

Not applicable.

Availability of data and materials

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Conflict of Interest

There is no conflict of interest.

Funding

This study was supported by Prevention of Cardiovascular Disease Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Authors’ contribution

Study design: MY, MHA; Data gathering: AT, DM, AMN, MY; Analysis: MY; Interpreting the results: MY, MHA; Drafting: AT, DM, AMN; Critically revised the paper: All authors.

Acknowledgments

None.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

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