Considerations for return-to-play
On March 11, 2020, just prior to the tip-off for the Utah Jazz versus Oklahoma City Thunder game, the National Basketball Association season was abruptly halted in dramatic fashion after it was disclosed one player had tested positive for SARS-CoV-2.
In subsequent and rapid fashion, other iconic American sporting events were canceled and professional sporting seasons were indefinitely postponed. For many in this country, these historic events marked the tangible beginning of the COVID-19 pandemic, which is still ongoing.
For practitioners charged in the care of athletes, there was initial concern about the effects of SARS-CoV-2 infection on the heart and the potential for the development of myocarditis, which is a common cause of sudden cardiac death in young athletes.1 At present, more than two years into this pandemic, much has been learned regarding the effects of COVID-19 infection on the athlete’s heart and the true prevalence of inflammatory heart disease in athletes infected by COVID-19. Rigorously obtained data have established which athletes may be at risk for COVID-19-related inflammatory heart disease and have guided the clinical algorithm in the approach to return-to-play (RTP) for athletes infected by COVID-19.2
In the spring of 2020, it was the higher-than-expected prevalence of myocardial injury observed among hospitalized patients with COVID-193 that fueled significant apprehension regarding the safety of competitive sports for athletes recovered from COVID-19 infection. Notably, however, these were older and sicker patients with underlying cardiac risk factors and not healthy, young athletes.
Nevertheless, given the degree of cardiac injury observed and numerous uncertainties regarding COVID-19 and the risk of myocarditis in healthier individuals at that time, early consensus screening recommendations were put forth4,5 that endorsed a conservative RTP screening approach for athletes consisting of “triad”6 testing with 12-lead electrocardiography (ECG), cardiac troponin assessment and trans-thoracic echocardiography.
In addition, some schools and collegiate athletic conferences added more sensitive imaging with cardiac magnetic resonance imaging (CMR) in addition to triad testing as part of their screening protocols. From these early experiences, several small observational case series were published that reported clinical profiles of athletes recovered from COVID-19 and results with additive CMR.7,8 Limitations of these studies were substantial, including single-center study designs, lack of controls, no independent blinded review of CMRs, non-standardized CMR protocols and small subject numbers.
In the first published case series of U.S. collegiate athletes (N=26), individuals were asymptomatic or only mildly ill.7 Four of 26 (15%) athletes met modified CMR Lake Louise Criteria9 for myocarditis, and eight (31%) had evidence of late gadolinium enhancement (LGE), suggestive of myocardial fibrosis without edema.7
A second case series of 54 U.S. collegiate student-athletes did not reveal any cases of myocarditis, but 40% with pericardial enhancement and/or pericardial effusion.8 Importantly, in no other published study of athletes with COVID-19 has the same degree of pericardial involvement been reported.
In 2021, many clinical uncertainties were finally addressed with the publication of outcomes in three large and multi-center registries of athletes with COVID-19. The first two of these registries included diverse populations of professional (N=789)10 and collegiate athletes (Outcomes Registry of Cardiac Conditions in Athletes [ORCCA], N=3,018)6 and demonstrated a low prevalence of clinical myocarditis in athletes (~0.6-0.7%)6,10 with the vast majority of athletes absent screening CMR.
In ORCCA, 198 collegiate athletes also had a screening CMR, and the prevalence of cardiac abnormalities in this sub-cohort increased to 3%. However, the overall diagnostic yield of CMR was four times higher if the study was clinically directed and not for screening purposes.6
Similar to other viral infections, it was the presence of cardiopulmonary symptoms (chest pain, shortness of breath as examples) and thus increased pre-test probability of myocarditis that were predictive of cardiac involvement after COVID-19 infection. Most importantly, to date, there have been no cases of life-threatening cardiac events reported as a direct consequence of COVID-19 infection in the athletes included in these large registries.6,10,11
The most recent and third registry came from the Big Ten Conference, which included N=1,597 athletes (vast majority asymptomatic or only mildly ill) who all underwent CMR screening in combination with triad testing.11 Abnormalities on CMR consistent with myocarditis were reported in 2.3% of athletes. However, there was marked heterogeneity in myocarditis prevalence (0-7.6%) from the 13 institutions included in this registry.11 Most of these cases were deemed ‘sub-clinical’ myocarditis (N=28) given lack of symptoms but detection by CMR.11
In terms of clinically apparent myocarditis (N=9, 0.6%),11 the data were comparable to ORCCA and the professional athlete registries.6,10 While robust in the number of athletes included in the Big Ten Registry, similar limitations in prior small CMR-based case series remained, particularly the lack of independent, blinded review of CMRs with a core lab.
At present, the compilation of registry data suggest that athletes recovering from COVID-19 with mild-to-moderate, non-cardiopulmonary symptoms are unlikely to have clinically significant inflammatory heart disease. With this as background, in March 2022, the American College of Cardiology recently updated recommendations for the RTP evaluation of athletes after COVID-19 infection.2 In summary, only athletes recovering from COVID-19 with cardiopulmonary symptoms (chest pain or tightness, shortness of breath, palpitations, lightheadedness or syncope) and/or those requiring hospitalization, should undergo further evaluation prior to resuming exercise training (See Figure 1 ).2
For athletes who are asymptomatic or with only mild to moderate non-cardiopulmonary COVID-19 symptoms (e.g., fever [temperature ≥100.4°F], chills, lethargy, myalgias, upper respiratory tract symptoms, gastrointestinal symptoms, anosmia, ageusia), additional cardiac testing is not recommended.2 The initial evaluation should be triad-based testing. With abnormal findings or if there is persistence of cardiopulmonary symptoms (specifically chest pain or tightness, palpitations or syncope) after initial testing, additional evaluation should be performed with CMR.
CMR is not recommended as a first-line diagnostic test or for any screening purposes. For any athlete recovered from COVID-19, a graded return to intense exercise training is recommended to ensure close surveillance for new or persistent cardiopulmonary symptoms that would warrant further clinical evaluation. Additional detail, including the timing of the initiation of training in those with mild to moderate non-cardiopulmonary COVID-19 symptoms, assessment of remote COVID-19 infection and RTP, interpretation of non-specific abnormal findings from cardiac testing, training restrictions in those diagnosed with myocarditis, and long-haul COVID-19 symptoms and RTP, can all be reviewed in this expert consensus decision pathway.2
Looking to the future, we should continue to acknowledge where uncertainties remain, particularly given the dynamic state of the pandemic. With emerging variants of SARS-CoV-2, longitudinal follow-up of outcomes in athletes will be required to assess the extent or severity of potential cardiac involvement. The clinical significance of non-specific abnormal CMR findings in low pre-test probability cases remains to be determined.
Future research requires a core lab with blinded CMR interpretation and more rigorously controlled analyses. Uncertainties regarding mechanisms and best practices in the care of athletes suffering from long-haul symptoms (post-acute sequelae of SARS-CoV-2 infection) remain critical issues. Finally, ongoing COVID-19 athlete registries are essential to accurately determine long-term cardiac and health outcomes.
In reflecting on the dynamic nature of the cardiac evaluation of athletes recovered from COVID-19, we are reminded of the timeless phrase from the famous French novelist Karr, “the more things change, the more they remain the same.”12 Clinical myocarditis prevalence and RTP outcomes data in convalesced athletes from COVID-19 provide reassurance that the evaluation of athletes after COVID-19 should be based on pre-test clinical probability and not a universal-based screening approach.
In accordance with the accepted clinical RTP approach for athletes recovered from any viral pathogen, it is time to move away from mandated intensive cardiac screening strategies after COVID-19 infection and instead return to the evaluation of the athlete recovered from COVID-19 based solely on the clinical presentation.
CDC = Centers for Disease Control and Prevention; CRM = cardiac magnetic resonance imaging; cTn = cardiac troponin; ECG = electrodiagram; PASC = post-acute sequelae of SARS-CoV-2; RTP = return to play; SARS-CoV-2 = severe acute respiratory syndrome coronavirus 2
*CDC Guidelines: COVID-19 Quarantine and Isolation
- Eichhorn C, Bière L, Schnell F, et al. Myocarditis in Athletes Is a Challenge: Diagnosis, Risk Stratification, and Uncertainties. JACC Cardiovasc Imaging. 2020;13(2 Pt 1):494-507.
- Writing C, Gluckman TJ, Bhave NM, et al. 2022 ACC Expert Consensus Decision Pathway on Cardiovascular Sequelae of COVID-19 in Adults: Myocarditis and Other Myocardial Involvement, Post-Acute Sequelae of SARS-CoV-2 Infection, and Return to Play: A Report of the American College of Cardiology Solution Set Oversight Committee. J Am Coll Cardiol. 2022;79(17):1717-1756.
- Clerkin KJ, Fried JA, Raikhelkar J, et al. Coronavirus Disease 2019 (COVID-19) and Cardiovascular Disease. Circulation. 2020.
- Phelan D, Kim JH, Chung EH. A Game Plan for the Resumption of Sport and Exercise After Coronavirus Disease 2019 (COVID-19) Infection. JAMA Cardiol. 2020.
- Kim JH, Levine BD, Phelan D, et al. Coronavirus Disease 2019 and the Athletic Heart: Emerging Perspectives on Pathology, Risks, and Return to Play. JAMA Cardiol. 2020.
- Moulson N, Petek BJ, Drezner JA, et al. SARS-CoV-2 Cardiac Involvement in Young Competitive Athletes. Circulation. 2021.
- Rajpal S, Tong MS, Borchers J, et al. Cardiovascular Magnetic Resonance Findings in Competitive Athletes Recovering From COVID-19 Infection. JAMA Cardiol. 2020.
- Brito D, Meester S, Yanamala N, et al. High Prevalence of Pericardial Involvement in College Student Athletes Recovering From COVID-19. JACC Cardiovasc Imaging. 2020.
- Ferreira VM, Schulz-Menger J, Holmvang G, et al. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation: Expert Recommendations. J Am Coll Cardiol. 2018;72(24):3158-3176.
- Martinez MW, Tucker AM, Bloom OJ, et al. Prevalence of Inflammatory Heart Disease Among Professional Athletes With Prior COVID-19 Infection Who Received Systematic Return-to-Play Cardiac Screening. JAMA Cardiol. 2021;6(7):745-752.
- Daniels CJ, Rajpal S, Greenshields JT, et al. Prevalence of Clinical and Subclinical Myocarditis in Competitive Athletes With Recent SARS-CoV-2 Infection: Results From the Big Ten COVID-19 Cardiac Registry. JAMA Cardiol. 2021;6(9):1078-1087.
- Karr AW, Rev. J. (1855). A Tour Round My Garden. G. Routledge. p. 313.
Dr. Jonathan Kim
Dr. Kim is an associate professor of medicine and Chief of Sports Cardiology at Emory. He completed his residency in internal medicine/pediatrics at Massachusetts General Hospital and his cardiology fellowship at Emory. Dr. Kim conducts NIH-funded sports cardiology research and is the team cardiologist for the Atlanta Falcons, Braves, Hawks, Dream and Georgia Tech. He is a member of the NBA Cardiac Advisory Committee and Chair-Elect for the American College of Cardiology’s Sports and Exercise Council.