In October 2020, the American College of Cardiology's (ACC) Sports & Exercise Cardiology Council put forth revised consensus recommendations regarding return-to-play (RTP) for athletes after SARS-Coronavirus-2 (COVID-19) infection.¹ At that time, because COVID-19 clinical outcomes and myocarditis prevalence in athletes were still unknown, RTP recommendations remained purely consensus-based. Over the last year, robust prevalence data ascertaining myocardial involvement after COVID-19 infection in athletes were published.^2-4 In addition, although COVID-19 vaccinations are now widely available, the pandemic remains dynamic with highly contagious and immune-evasive variants circulating amongst the general public. New, relevant COVID-19 questions from the sports medicine community, including the appropriate clinical approach to RTP, timing of RTP, vaccination concerns in young athletes, and the clinical impact of new variants, have emerged along with increasing concerns over rising case numbers and how recent updates to Centers for Disease Control and Prevention (CDC) self-isolation protocols may affect RTP protocols.

In the summer of 2021, ACC conducted a virtual roundtable with experts in the arenas of myocarditis, post-acute sequelae of SARS-CoV-2 infection, and sports cardiology to discuss the cardiovascular complications associated with COVID-19. A primary output from this meeting will be a forthcoming Expert Consensus Decision Pathway (ECDP) on the cardiovascular sequalae of COVID-19 in adults, which will include a comprehensive discussion of RTP for athletes after COVID-19. However, given the time-sensitive concerns from the sports medicine community, this current document was written by members of the ECDP RTP Writing Committee to summarize answers to key questions that are also included in the forthcoming, more complete ECDP.

Over the last year, what have we learned regarding the effects of COVID-19 on the 'Athletic Heart'?

Since the last iteration of RTP recommendations,¹ large registries of United States professional (N=789)² and collegiate athletes (N=3,018)³ recovered from COVID-19 documented a low prevalence of clinical myocarditis (0.6-0.7%), most of whom underwent cardiac 'triad' testing (12-lead electrocardiogram [ECG], echocardiogram, troponin-assay [cTn])  regardless of COVID-19 symptoms. In these registries, cardiac magnetic resonance imaging (MRI) was generally obtained if any component of 'triad' testing was abnormal or if symptoms were suggestive of myocarditis.^2,3 The Big Ten Conference also published data on 1,597 collegiate athletes who underwent universal screening with cardiac MRI in addition to 'triad' testing, irrespective of symptoms.⁴ Abnormalities on cardiac MRI consistent with myocarditis (modified Lake Louis Criteria)⁵ were reported in 2.3% (N=37) of athletes. However, 28/37 of these cases were deemed 'sub-clinical' given the lack of clinical myocarditis symptoms and there was marked heterogeneity in the prevalence (0-7.6%) and type of CMR abnormalities among the 13 universities included in this registry.⁴ In terms of clinical myocarditis, the data were comparable to other registries, as only nine athletes (0.6%) had findings consistent with clinical myocarditis.⁴ Within all of these registries, to-date, there have been no adverse cardiac outcomes reported as a direct consequence of COVID-19 and regardless of the inclusion of cardiac MRI in the screening process.^2-4

What symptoms should guide cardiac testing after COVID-19 and what tests should be performed if indicated?

Current data suggest competitive athletes recovering from COVID-19 with mild, non-cardiopulmonary symptoms are unlikely to have myocarditis and clinically significant myocardial involvement.^2,3 Rather, the presence of cardiopulmonary symptoms are of greater relevance when assessing the probability of clinically-important myocardial disease.³ Only for athletes recovering from COVID-19 with cardiopulmonary symptoms concerning for myocarditis or myocardial involvement (chest pain or tightness, dyspnea, palpitations, lightheadedness, or syncope) should further cardiac evaluation be performed prior to RTP. For all others who are asymptomatic or with non-cardiopulmonary symptoms (includes fever [temperature ≥100.4°F], chills, lethargy, myalgias, upper respiratory tract, gastrointestinal, anosmia, ageusia, headache), cardiac testing is not recommended prior to RTP.

For athletes with cardiopulmonary symptoms, the initial evaluation should include ECG, cTn (high-sensitivity assay preferred), and an echocardiogram. The presence of abnormal findings with 'triad' testing or persistence of cardiopulmonary symptoms after initial testing or during return-to-exercise suggests additional evaluation, beginning with cardiac MRI, should be performed. Cardiac MRI is not recommended as a first-line testing modality.

Finally, regardless of symptomatology, it is imperative to proceed with a graded RTP regimen to ensure close monitoring for new cardiopulmonary symptoms in all athletes recovering from COVID-19, even in those with normal 'triad' testing. While consensus-based graded return to exercise regiments have been proposed,⁶ the progression and timeline should be individualized and based on numerous factors including baseline fitness, severity and duration of COVID-19, and tolerance of progressive levels of exertion.

With the recent change in CDC recommendations for COVID-19 self-isolation reduced to 5 days, when can cardiac testing be performed (if clinically indicated)?

We recommend cardiac testing only for those athletes recovering from COVID-19 with initial cardiopulmonary symptoms, or with cardiopulmonary symptoms with resumption of exercise. In these cases, if the athlete has been deemed safe according to the CDC guidelines⁷ to leave self-isolation (from the perspective of spread of infection), it is reasonable to proceed with cardiac testing.

With the recent change in CDC recommendations for COVID-19 self-isolation reduced to 5days, when can athletes resume training?

Past RTP guidance recommended that individuals abstain from exercise training throughout the prior CDC recommended 10-day self-isolation period, in part, because of the concern for potential clinical cardiovascular deterioration.^1,8 However, the low observed rate of clinically significant myocardial involvement among athletes with asymptomatic or mild COVID-192-4 suggests that this longer period of activity restriction is no longer necessary. For asymptomatic athletes with COVID-19, we recommend 3 days of exercise abstinence to ensure that symptoms do not develop. For athletes with non-cardiopulmonary symptoms, exercise training should generally be withheld until symptom resolution. Exceptions are isolated anosmia or ageusia, which may have a more prolonged course. As previously emphasized, a graded return-to-exercise regimen is necessary to ensure close monitoring for new cardiopulmonary symptoms.

It is also imperative to ensure compliance with public health guidance and avoid the potential of transmitting infectious virus through aerosolization during indoor exercise. New CDC guidelines stipulate that, regardless of vaccination status, with COVID-19 test positivity self-isolation may end after 5 days as long as symptoms are not present or are resolving.⁷ In addition, there is the recommendation to wear an appropriate face mask for 5 additional days after cessation of self-isolation. This strategy is generally impractical for an athlete resuming exercise training. At the end of 5 days of self-isolation, if an athlete has resolution of non-cardiopulmonary symptoms, there are four options to consider for resumption of exercise training out of self-isolation: 1) obtain an additional negative COVID-19 PCR test, other negative nucleic acid amplification test, or two negative rapid antigen tests spaced 24-hours apart, if indoor training is planned with other individuals near-by and/or a team sport that involves close interaction with other athletes, 2) remain self-isolated during indoor training sessions (until negative COVID-19 status is obtained or up to 10 days after COVID-19 test positivity), 3) if feasible based on sport type and physical environment, proceed only with socially distanced outdoor training (until negative COVID-19 status is obtained or up to 10 days after COVID-19 test positivity), or 4) if feasible, wear a face mask during indoor training (until negative COVID-19 status is obtained or up to 10 days after COVID-19 test positivity) if facilities are well-ventilated and appropriate social distancing is maintained. At the end of 5 days of self-isolation, if cardiopulmonary COVID-19 symptoms were present, these same options would apply if symptoms were resolved and 'triad' tests are normal. Based on CDC guidance, these options are the same for immunocompetent, vaccinated or unvaccinated athletes.

With the current Omicron surge and increase in recurrent infections observed in athletes, should cardiac testing be obtained in those with recurrent COVID-19 prior to RTP?

Even among fully vaccinated and up-to-date athletes, there has been an increase in the number of professional and collegiate athletes diagnosed with recurrent COVID-19. For those with recurrent COVID-19, cardiac testing is not warranted in the absence of cardiopulmonary symptoms. Each clinical evaluation of an athlete after COVID-19 should remain independent of any prior history of COVID-19.

Specific to young athletes, is the risk of vaccine-associated myocarditis higher than risks of COVID-19?

Myocarditis is a rare complication after the COVID-19 mRNA vaccination and has a much lower risk compared to the risks associated with COVID-19, regardless of age or sex. Young males aged 12-29 years have the highest myocarditis event rate by age grouping with 40.6 cases per million reported.⁹ In a separate analysis within the Military Health System between January-April 2021, out of 2.8 million doses of mRNA COVID vaccinations administered, only 23 men were diagnosed with clinical acute myocarditis (median age 25 [20-51] years).¹⁰ It is important to emphasize the extremely favorable benefit-to-risk ratio for COVID-19 vaccination in all age and sex groups.^9,11 For SARS-CoV-2 infection, the mortality rate is 0.1-1 per 100,000 individuals aged 12-29 years. Although 39-47 estimated cases of myocarditis (primarily mild in severity) would be expected for every 1 million men aged 12–29 years after the second administered dose of mRNA vaccination,⁹ with vaccination, approximately 11,000 COVID-19 cases, 560 hospitalizations, 138 ICU admissions, and six deaths would be estimated to be prevented. Furthermore, beyond helping to reduce the risk of hospitalization and death, vaccination also helps to mitigate the risk of the long-term, debilitating effects of post-acute sequelae of SARS-CoV-2 infection, which is estimated to occur in 10-30% of individuals affected by COVID-19.12,13 Therefore, we continue to support vaccination in all athletes to minimize the risk of serious infection with COVID-19, as well as reduce individual viral load and spread of infection. 

REFERENCES

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2. 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;6:745-52.

3. Moulson N, Petek BJ, Drezner JA, et al. SARS-CoV-2 cardiac involvement in young competitive athletes. Circulation 2021;144:256-66.

4. 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;6:1078-87.

5. Ferreira VM, Schulz-Menger J, Holmvang G, et al. Cardiovascular magnetic resonance in nonischemic myocardial inflammation: expert recommendations. J Am Coll Cardiol 2018;72:3158-76.

6. Salman D, Vishnubala D, Le Feuvre P, et al. Returning to physical activity after covid-19. BMJ 2021;372:m4721.

7. CDC Updates and Shortens Recommended Isolation and Quarantine Period for General Population (CDC website). 2021. Available at: https://www.cdc.gov/media/releases/2021/s1227-isolation-quarantine-guidance.html. Accessed 01/11/2021.

8. 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;5:1085-86.

9. Gargano JW, Wallace M, Hadler SC, et al. Use of mRNA COVID-19 vaccine after reports of myocarditis among vaccine recipients: update from the advisory committee on immunization practices - United States, June 2021. MMWR Morb Mortal Wkly Rep. 2021;70:977-82.

10. Montgomery J, Ryan M, Engler R, et al. Myocarditis following immunization with mRNA COVID-19 vaccines in members of the US Military. JAMA Cardiol 2021;6:1202-06.

11. Bozkurt B, Kamat I, Hotez PJ. Myocarditis with COVID-19 mRNA vaccines. Circulation 2021;144:471-84.

12. Logue JK, Franko NM, McCulloch DJ, et al. Sequelae in adults at 6 months after COVID-19 infection. JAMA Netw Open 2021;4:e210830.

13. Hageman JR. Long COVID-19 or post-acute sequelae of SARS-CoV-2 infection in children, adolescents, and young adults. Pediatr Ann 2021;50:e232-e233.