Cardiac magnetic resonance (CMR) imaging increased the prevalence of clinical and subclinical myocarditis in competitive athletes with recent SARS-CoV-2 infection by a factor of 7.4 as compared with symptom-based screening, according to research published in JAMA Cardiology.1

Competitive athletes are considered a unique population at potential high risk for environmental and situational COVID-19 transmission, as well as sudden cardiac death if infected with SARS-CoV-2. Viral myocarditis in asymptomatic individuals is a common cause of sudden cardiac death, with an incidence of 1 in 50,000 college athletes per year.

Some return-to-play screening protocols developed by universities and athletic conferences have tied CMR and cardiac testing to the presence of cardiac symptoms, while other require advanced testing of all athletes infected with COVID-19. The Big Ten Conference recently required advanced testing for all athletes following a COVID-19 infection before being cleared to return to play; this testing includes an electrocardiogram, echocardiogram, serum troponin level, and CMR imaging. The Big Ten COVID-19 Cardiac Registry was also formed.


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In the current study, researchers sought to estimate myocarditis prevalence among athletes following COVID-19 infection, compare differences in COVID-19 myocarditis across Big Ten universities, and evaluate the utilities of variable diagnostic strategies for screening for myocarditis among athletes, as well as review timing and results of repeat CMR as used to inform safe return-to-play decisions.

Each university investigator reported the number of athletes who were screened for SARS-CoV-2 infection, the number with positive polymerase chain reaction (PCR) results, the number who completed CMR imaging, and the number of athletes who had findings consistent with myocarditis.

Thirteen Big Ten universities participated in the observational study, submitting data for 9255 athletes who underwent COVID-19 testing through December 15, 2020. In this group, 30.4% tested positive for COVID-19 (66.9% men) and 2461 completed cardiac evaluation — 64.9% with CMR imaging and 35.1% without. Among the athletes who had available CMR imaging results, 2.3% (n=37; 27 men) were diagnosed with either clinical or subclinical myocarditis.

A total of 9 athletes with clinical myocarditis reported experiencing cardiac symptoms either before or at the time of cardiac testing; 8 reported chest pain, 3 had dyspnea, and 3 had palpitations. Of the 37 athletes, 28 had subclinical myocarditis and reported no symptoms. In this group, 8 athletes had abnormal cardiac testing other than CMR imaging, including 1 with abnormal ECG findings and 4 with elevated troponin levels.

In total, 20 athletes had subclinical myocarditis with no cardiac symptoms and nondiagnostic ECG, echocardiogram, and troponin level findings.

Based on the cardiac symptom-driven diagnostic strategy published previously in JAMA Cardiology,2 only 5 athletes with myocarditis would have been identified in this cohort. A strategy that combined ECG, echocardiogram, and troponin findings, regardless of symptoms, plus CMR imaging, would have identified 13 athletes. A strategy utilizing CMR imaging regardless of cardiac symptoms or testing results led to a 7.4-fold increase from the symptom-driven strategy and a 2.8-fold increase from the ECG, echocardiogram, and troponin strategy.

With CMR imaging, 31 of 37 findings reported as myocarditis met the modified Lake Louise Criteria (LLC), demonstrating elevated T2 and T1 or late gadolinium enhancement (LGE) in the same location. Among the 6 athletes who did not meet modified LLC criteria, 3 had clinical myocarditis. Among the 3 athletes with subclinical myocarditis and CMR imaging that did not meet modified LLC criteria, 2 showed significantly reduced left ventricular systolic function and LGE patterns typical of myocarditis and 1 had CMR imaging results showing extensive LGE in a “typical pattern for myocarditis.”

During follow-up, 73.0% of athletes completed repeat CMR imaging in a mean of 9.4±3.1 weeks (range, 4-14 weeks). Two patterns were identified: the first was a complete resolution of both T2 mapping abnormalities and LGE in 40.7% of athletes (range between studies, 4-10 weeks); the second was a resolution of T2 mapping abnormalities with LGE persistence in 59.3% of athletes (range between studies, 4-14 weeks).

Findings, including the COVID-19 positivity rate, timing of complete cardiac testing, and myocarditis prevalence, varied among Big Ten universities. Per program, myocarditis presence ranged from 0% to 7.6% (overall, 2.3%; 95% CI, 1.6%-3.2%); 3 universities reported no cases and 10 reported at least 1 case.

In a subgroup analysis of universities where CMR imaging was performed in all cardiac evaluations, 21 athletes were diagnosed from 919 evaluations, with a prevalence of 2.3% (95% CI, 1.4% to 3.5%). Timing between COVID-19 test positivity to cardiac testing and myocarditis diagnosis ranged from 10 to 77 days (median, 22.5 days).

Study limitations include possible selection bias prior to mandated comprehensive cardiac testing, concerns surrounding the use of CMR as a screening tool, and a lack of specific data on each athlete.

“We observed variability in prevalence [of myocarditis] across universities, and this may be based on timing of CMR imaging relative to COVID-19 infection and variability in CMR protocols and interpretation,” the researchers wrote. “Further detailed core analysis will guide CMR screening protocols and Big Ten [return-to-play] recommendations.”

“The role of CMR in routine screening for athletes safe return to play

should be explored further,” the study authors concluded.

References

1. Daniels CJ, Rajpal S, Greenshields JT, et al; Big Ten COVID-19 Cardiac Registry Investigators. 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. Published online May 27, 2021. doi:10.1001/jamacardio.2021.2065

2. 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. 2021;6(2):219-227. doi:10.1001/jamacardio.2020.5890