Editor's Note: Commentary based on Phelan D, Kim JH, Elliot MD, et al. Screening of potential cardiac involvement in competitive athletes recovering from COVID-19: an expert consensus statement. JACC Cardiovasc Imaging 2020;Oct 28:[Epub ahead of print].¹

Case Presentation

A 22-year-old male baseball first basemen developed chest pain and chest pressure after a recent COVID-19 infection. Given his moderate symptoms, he underwent cardiovascular evaluation prior to returning to play. He had a troponin-I that was undetectable and a normal electrocardiogram (ECG). His transthoracic echocardiogram (TTE) revealed a mild global reduction in left ventricular (LV) ejection fraction (EF) (49%) and his tissue Doppler septal and lateral e' were 6 and 10, respectively. His global longitudinal strain (GLS) was -15%. His findings were felt to be consistent with athletic remodeling and he was cleared to return to sport. His chest pain persisted, and he is now referred to you for further evaluation.

Cardiac imaging after a COVID-19 infection

Guidance for safely resuming training and competition during the COVID-19 pandemic has focused on creating return to play (RTP) protocols that minimize the risk of COVID-19 spread among athletes and prioritize athlete safety. Screening athletes for subclinical cardiac disease has traditionally been a source of controversy given concerns of cost, need for sports cardiology expertise, high false-positive rates, unnecessary downstream testing, and risk of inappropriate medical disqualification.² However, given preliminary data^3,4 suggesting a high prevalence of myocardial injury in hospitalized patients after COVID-19, most RTP algorithms^5-7 have advised cardiac testing in such athletes to identify clinical and subclinical myocarditis. This has resulted in large numbers of athletes across the country undergoing cardiac testing with increased utilization of ECG, troponin and echocardiography which unearths potential negative downstream consequences. Thus, the recently published expert consensus statement¹ in JACC Cardiovascular Imaging is very timely and provides the general cardiologist and the sports cardiologist a framework on how to review cardiac studies in athletes after COVID-19. The authors provide a comprehensive update of the current COVID-19 literature for each cardiac imaging modality and then offer specific guidance and recommendations on how to interpret and differentiate physiologic remodeling from COVID-19 related pathology.

Key Points from the document are highlighted below:

1. Cardiac testing in the RTP evaluation of myocarditis should be considered as complementary as the sensitivity of a single test (ECG, troponin or TTE) is not high enough to be used as a stand-alone screening test. Additionally, normative data for high sensitivity cardiac troponin (hs-cTn) in athletes are lacking, and therefore results should be not be viewed in a binary fashion (normal vs. abnormal based on the 99th percentile) but instead interpreted in the context of the full clinical presentation including findings from the ECG and TTE to help guide need for further testing.
2. Echocardiographic findings of myocarditis are variable and may mimic dilated, hypertrophic and restrictive cardiomyopathies. Data regarding the echocardiographic findings in COVID-19 are still being investigated but initial data from hospitalized patients suggest that impairments in right ventricular (RV) systolic function and LV diastolic dysfunction are more common than reductions in LVEF. While most athletes have a normal LVEF, some elite endurance athletes can have markedly enlarged LV volumes with mildly reduced LVEF, but both scenarios are associated with normal diastolic function. Given poorly defined normal values in athletes, the authors recommend that a GLS worse than -16% should raise concern for myocardial pathology.
3. RV dysfunction is commonly seen in COVID-19 patients and RV dilation with low-normal or mildly abnormal RV systolic function can also be seen among healthy endurance athletes. The authors recommend utilizing a RV to LV basal end-diastolic diameter ratio to better assess for pathologic RV enlargement in athletes, with a ratio of 0.8 ± 0.1 and 0.6 ± 0.1 being normal in the long- and short- axis views, respectively.
4. Cardiac MRI (CMR) remains the gold standard imaging modality for regional and global ventricular function and is valuable when TTE findings are nondiagnostic or when further evaluation of the left or right heart is warranted. Additionally, given its ability to evaluate ventricular inflammation, edema and scar, CMR is an important diagnostic tool for the evaluation of myocarditis in athletes with a moderate to high pretest probability of disease. The authors highlight limitations in recent COVID-19 CMR publications and given the lack of standardization in parametric mapping (T1 and T2), advocate that each CMR program create their own normal reference range from at least 30-50 healthy subjects.
5. Exercise testing can be helpful in the assessment of the athlete after COVID-19. The authors emphasize that exercise testing is contraindicated in acute myocarditis. In those with unexplained dyspnea or exertional intolerance after COVID-19, cardiopulmonary exercise testing may prove to be of high yield given the ability to assess for cardiac and pulmonary sequalae of COVID-19 illness.

During this time of increased utilization of cardiac imaging in young otherwise healthy athletes, the expert consensus document by Phelan et al. provides an important comprehensive review of cardiac imaging modalities and how they relate to athletes in the context of COVID-19 illness. Additionally, given preliminary CMR data suggesting cardiac sequelae occur in non-hospitalized patients⁸ (including athletes)⁹ who have recovered from COVID-19, the authors highlight the utility, strengths and limitations of CMR and advocate for robust, multi-centered data to improve our understanding of COVID-19 associated cardiac disease. Ultimately, the interpretation and evaluation of any study should be done in the context of the athletes age, sex, sport, and race to help better differentiate healthy physiologic changes from COVID-19 related pathology.

Case Follow-Up
A detailed exercise history revealed that while the athlete exercises 6 days a week, the sessions are focused on batting and position skills without routine high doses of aerobic training. Equipped with his exercise history, one would not expect to see a cardiac phenotype that can be seen in elite endurance athletes, namely eccentric remodeling with mildly reduced LVEF. Additionally, the borderline diastolic function and reduced GLS suggest pathology rather than healthy physiologic remodeling. Given the TTE findings and chest pain symptoms, the athlete was referred for CMR which revealed subepicardial late gadolinium enhancement and abnormal T2 imaging, findings that are consistent with a diagnosis of myocarditis. The athlete is being managed according to myocarditis guidelines.¹⁰

References

1. Phelan D, Kim JH, Elliot MD, et al. Screening of potential cardiac involvement in competitive athletes recovering from COVID-19: an expert consensus statement. JACC Cardiovasc Imaging 2020;Oct 28:[Epub ahead of print]
2. Maron BJ, Levine BD, Washington RL, Baggish AL, Kovacs RJ, Maron MS. Eligibility and disqualification recommendations for competitive athletes with cardiovascular abnormalities: Task Force 2: preparticipation screening for cardiovascular disease in competitive athletes: a scientific statement from the American Heart Association and American College of Cardiology. J Am Coll Cardiol 2015;66:2356-61.
3. Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020;395:497-506.
4. Clerkin KJ, Fried JA, Raikhelkar J, et al. COVID-19 and cardiovascular disease. Circulation 2020;141:1648-55.
5. 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;May 13:[Epub ahead of print].
6. 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;Oct 26:[Epub ahead of print].
7. Wilson MG, Hull JH, Rogers J, et al. Cardiorespiratory considerations for return-to-play in elite athletes after COVID-19 infection: a practical guide for sport and exercise medicine physicians. Br J Sports Med 2020;54:1157-61.
8. Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol 2020;Jul 27:[Epub ahead of print].
9. Rajpal S, Tong MS, Borchers J, et al. Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection. JAMA Cardiol 2020;Sep 11:[Epub ahead of print].
10. Maron BJ, Udelson JE, Bonow RO, et al. Eligibility and disqualification recommendations for competitive athletes with cardiovascular abnormalities: Task Force 3: hypertrophic cardiomyopathy, arrhythmogenic right ventricular cardiomyopathy and other cardiomyopathies, and myocarditis: a scientific statement from the American Heart Association and American College of Cardiology. J Am Coll Cardiol 2015;66:2362-71.

Clinical Topics: Cardiovascular Care Team, COVID-19 Hub, Heart Failure and Cardiomyopathies, Sports and Exercise Cardiology

Keywords: Sports, COVID-19, severe acute respiratory syndrome coronavirus 2, Troponin I, Reference Values, Myocarditis, Cardiomyopathy, Restrictive, Stroke Volume, Cicatrix, Consensus, Healthy Volunteers, Dilatation, Prevalence

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