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Open AccessBrief Report

Incidence of Myocardial Injury in COVID-19-Infected Patients: A Systematic Review and Meta-Analysis

1
Department of Medicine, University of Riverside, Riverside, CA 92521, USA
2
Faculty of Medicine, King Chulalongkorn Memorial Hospital, Chulalongkorn University, Bangkok 10330, Thailand
3
Division of Cardiac Electrophysiology, University of Michigan Health Care, Ann Arbor, MI 48109, USA
4
Department of Medicine, Mayo Clinic, Rochester, MN 55905, USA
5
Department of Internal Medicine, University of Arizona, Tucson, AZ 85721, USA
6
Department of Cardiovascular Medicine, Emory University, Atlanta, GA 30322, USA
*
Authors to whom correspondence should be addressed.
Diseases 2020, 8(4), 40; https://doi.org/10.3390/diseases8040040
Received: 31 August 2020 / Revised: 24 October 2020 / Accepted: 26 October 2020 / Published: 27 October 2020

Abstract

Introduction: The incidence of acute myocardial injury (AMI) among Coronavirus Disease 19 (COVID-19)-infected patients remain unclear. We aimed to conduct a systematic review and meta-analysis to further explore the incidence AMI in these patients. Methods: We comprehensively searched the MEDLINE, EMBASE and Cochrane databases from their inception to August 2020. The included studies were prospective or retrospective cohort studies that reported the event rate of AMI in COVID-19 patients. Data from each study were combined using random-effects to calculate the pooled incidence with 95% confidence intervals. Results: We identified twenty-seven studies consisting of 8971 hospitalized COVID-19-infected patients. The study demonstrated that 20.0% (95% CI 16.1–23.8% with substantial heterogeneity (I2 = 94.9%)) of hospitalized COVID-19 patients had AMI. In addition, our meta-regression suggested that older age, male and comorbidities were associated with a higher risk of AMI. Conclusion: The incidence of COVID-19-related myocardial injury ranges from 16.1–23.8%. Further larger studies are anticipated, as the pandemic is still ongoing.
Keywords: coronavirus; COVID-19; myocardial injury; meta-analysis; systematic review coronavirus; COVID-19; myocardial injury; meta-analysis; systematic review

1. Introduction

Coronavirus disease 2019 (COVID-19)-infected patients have shown unique characteristics, with higher infection and mortality rates than prior pandemic-associated respiratory viral infections. However, the incidence and pattern of cardiac involvement for this new emerging respiratory viral infection remains unclear. COVID-19-infected patients have shown unique characteristics, with higher infection and mortality rates than prior pandemic-associated respiratory viral infections. Particularly, myocardial involvement in COVID-19 seems to be common compared to previous coronavirus outbreaks, and is associated with higher morbidity and mortality [1]. As the current pandemic has not yet been resolved, acute myocardial injury (AMI)—which is mostly defined by elevated troponin higher than upper normal limit [2]—is still of importance. The exact incidence is yet to be elucidated, especially from regions other than China.
Hence, we aimed to conduct a systematic review and meta-analysis to further explore the incidence of myocardial injury among COVID-19-infected patients.

2. Materials and Methods

A systematic literature search of Ovid MEDLINE, EMBASE, and the Cochrane Database of Systematic Reviews (from inception to August 2020) was conducted to identify studies evaluating the incidence/prevalence and clinical significance of myocardial injury among COVID-19-infected patients.
The systematic literature review was undertaken independently by two investigators (R.C. and N.P.) applying a search approach that incorporated the terms “COVID” or “coronavirus” or “SARS-CoV-2” and “myocardial injury’ or “clinical” (Online Supplementary Data). No language limitation was applied.
Eligible studies included cross-sectional, case-control, or cohort studies that assessed the incidence/prevalence and clinical significance of myocardial injury in COVID-19-infected patients. Studies had to provide effect estimates for overall incidence, prevalence, and risk ratios with a 95% confidence interval (CI). Inclusion was not limited by study size. Retrieved articles were reviewed individually for their eligibility by the two investigators noted previously. Analyses were performed using STATA version 14.1. Adjusted point estimates from each study were consolidated using the generic inverse variance approach of DerSimonian and Laird, which designated the weight of each study based on its variance [3]. Meta-regression was also performed to explore risk modifiers.

3. Results

The final analysis included 27 observational studies with 8971 hospitalized COVID-19-infected patients (Table 1). Our meta-analysis demonstrated that 20.0% (95% CI 16.1–23.8% with substantial heterogeneity (I2 = 94.9%)) of hospitalized COVID-19 patients had a myocardial injury manifested mainly by elevated cardiac troponin I levels (Online Supplementary Data).
To account for demographic data, we performed meta-regression showing that age, gender, region, and CVD comorbidities. Our analysis suggested older age, male, hypertension, diabetes, coronary heart disease and chronic kidney disease correlated with higher incidence of myocardial injury. (all p < 0.01) However, no statistical correlation was found between region, race and incidence of myocardial injury (p > 0.1) (Online Supplementary Data).

4. Discussion

Our study highlighted that the incidence of COVID-19 myocardial injury has ranged from 16.1 to 23.8% (Table 2). In comparison with previous epidermic Coronavirus, myocardial injury following COVID-19 seemed to be higher—likely due to underreported incidence of the previous diseases which did not reach pandemic state, suggested by higher mortality rates from those previous diseases limiting their spread. Of note, the diverse incidence of AMI could be explained by differences in demographic data and comorbidities which our study suggested. Despite several studies since the beginning of COVID-19 era, our insight into cardiovascular complications remains limited, warranting further data for better understanding.
Based on our meta-regression, our study also supported that older age, male, and comorbidities—particularly hypertension, diabetes, underlying coronary heart disease and chronic kidney disease—were associated with higher risk of myocardial injury incidence. This suggests that these factors may be casual in cardiac injury process. On the other hand, it was deemed primordial to conclude null impact from races and regions, given the paucity of data from countries other than China. Further studies are encouraged to investigate.
COVID-19 myocardial injury occurs through several mechanisms. One is direct cardiac injury on different parts of the heart by viral entry into the cardiomyocytes. The second is microvascular dysfunction as a consequence of severe inflammatory reaction to the virus. With this cascade come endothelial dysfunction and endothelitis, which further worsen cardiac function [2]. This phenomenon may lead to several manifestations of myocardial injury, from myocarditis and arrhythmia, to Takotsubo cardiomyopathy [35].
Intriguingly, the hypercoagulability state is one of the most unique pathophysiologies proposed in COVID-19, which leads to generalized arterial and venous thrombosis [36]. Owing to the dysregulated immune system, especially in severe infection, several interplays between cytokine storm, platelet hyperactivation and altered microvascular permeability result in abnormal coagulation cascades which promote coronary thrombosis, plaque thrombosis, and even stent thrombosis [37]. Recent studies provided data that support this theory, demonstrating massively elevated Von Willebrand factor, D-Dimer and abnormal procoagulant factors, and even the presence of antiphospholipid antibodies [38,39,40].
Another mechanism is indirect involvement through imbalance between metabolic demand and cardiac reserve in patients with preexisting cardiac disease. Based on Choundry et al. [41], we can infer that COVID-19 posed patients at higher risks for acute coronary events. Exaggerated inflammatory responses following the infection can stimulate acute plaque rupture, leading to demand-supply mismatch [42]. As a result, acute myocardial infarction ensues, complicating the patient’s prognosis and clinical course. Nevertheless, data paucity has remained in regard to the true incidence between AMI by microvascular dysfunction and coronary thrombosis among COVID-19 patients, given the difficulty in designing such dedicated studies.
Given the consequent high fatality rate, several clinical trials have been investigated to treat and prevent its progression. Combined antibiotics with Azithromycin and Chloroquine, however, did not improve mortality outcomes but lengthened QT interval, posing significant arrhythmias [43]. For novel therapies such as Remdesevir and IL-6 inhibitors, the data are still limited. Recently, Sheng et al. began a clinical trial using Canakinumab to minimize the risk of myocardial injury, which is currently in the enrolling state [44]. At the moment, we do not have any effective treatments which reduce COVID-19 complications.
Though informative, our study has certain limitations. First, the statistical heterogeneity is sizable. Thus, meta-regression was performed elucidating the contributions from demographical data and patients’ comorbidities. Moreover, the lack of echocardiographic parameters is cumbersome, further precluding proper variable adjustment. However, the use of echocardiograms in COVID-19-infected patients remains limited due to the disease’s high transmission rate. Second, most studies were from China; thus, real-world incidence may be diverse. Nevertheless, our preliminary analysis suggested no significant difference in myocardial injury incidence. Many more studies from countries other than China are required to demonstrate such diversity. Lastly, true incidence could be overestimated, as most studies used troponin as a marker of cardiac injury, which is not specific to COVID-induced cardiac injury alone, but also to ACS, heart failure, arrhythmia, and so on. Thus, interpretation should be carefully discerned.

5. Conclusions

Our study showed the most updated incidence of COVID-19-related myocardial injury, which ranges from 16.1–23.8%. However, as the pandemic has not yet reached the turning point, further studies investigating this relationship with a larger sample size are anticipated.

Supplementary Materials

The Supplementary Materials are available online at https://www.mdpi.com/2079-9721/8/4/40/s1.

Author Contributions

N.P., R.C., and W.C. contributed to the conception or design of the work. C.T., T.B. and S.V. contributed to the acquisition, analysis, or interpretation of data for the work. N.P., W.C. and R.C. drafted the manuscript. R.C. and W.C. critically revised the manuscript. All gave final approval and agree to be accountable for all aspects of work ensuring integrity and accuracy. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors have declared that no competing interests exist.

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Table 1. Study characteristics.
Table 1. Study characteristics.
Study NameCountryTotal Numbers (n)Mean Age
(Years Old)
Sex
(Male%)
Hypertension (%)DM (%)CHD (%)CKD (%)Myocardial Injury Incidence (%)
He [4]China5468n/a24.114.85.3n/a44
Huang [5]China414973152015n/a12
Wang [6]China1385654.331.210.114.52.97
Zhou [7]China191566230198117
Liu [8]China5653.75551873.6113
Chen [9]China150594433136n/a20
Shi [10]China4166449.33114163.420
Deng [11]China225545526128n/a29
Yang [12]China5259.767n/a95n/a23
an [13]China1354753.39.68.95.2n/a7
Cao [14]China102545227.510.84.93.915
Guo [15]China18758.5n/a32.61511.23.228
Tao [16]China31269.26057.138.829.83.2133
Tu [17]China17453.745.421.29.89.2n/a14
Du [18]China1795854.232.418.416.2n/a23
Xu [19]China8857.140.912312.57.95n/a8
Wu [20]China2015163.119.410.98n/a4
Wei [21]China1014953.52113.95n/a16
Ni [22]China1766757.39492614n/a28
Li [23]China5486050.930.315.16.21.822
Yu [24]China2266461.542.520.89.70.3527
Feng [25]China4765356.923.71080.811
Lombardi [26]Italy6146770.8572422.317.945
Javanian [27]Iran10060513227201214
Saleh [28]Iran38659.561.136.834.525.14.130
Chung [29]South Korea11056.943.633.616.39.1n/a12
Richardson [30]USA35336360.356.633.811.18.523
Abbreviations: CVD: Coronary heart disease; CKD: Chronic kidney disease; DM: Diabetes. n/a: Not applicable.
Table 2. Cardiovascular manifestation among recent epidermic/pandemic Coronavirus.
Table 2. Cardiovascular manifestation among recent epidermic/pandemic Coronavirus.
Summary of Cardiovascular Presentations among Outbreak Coronavirus
Outbreak Period20032015Current
ComparisonSARSMERSCOVID-19
PathophysiologyExaggerated immune response [31]UnclearCytokine storm, direct viral injury, plaque instability
Myocardial injury incidenceNo clear dataVaried from 16.1–23.8%
Cardiovascular manifestationSubclinical diastolic dysfunction, tachycardia, hypotension, cardiomegaly, atrial fibrillation, myocardial ischemia, elevated troponin [31,32,33]Acute myocarditis, Acute heart failure [34]Shock, Acute myocarditis, Acute heart failure, Elevated troponin, Arrhythmia [6,30]
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