Myocarditis Screening Methods in Athletes After SARS-CoV-2 Infection – a Systematic Review

Abstract

This review aims to elucidate the myocarditis incidence in SARS-CoV-2-positive athletes and to evaluate different screening approaches to derive sports cardiological recommendations after SARS-CoV-2 infection. The overall incidence of athletes (age span 17–35 years, 70% male) with myocarditis after SARS-CoV-2 infection was 1.2%, with a high variation between studies (which contrasts an incidence of 4.2% in 40 studies within the general population). Studies that used conventional screening based on symptoms, electrocardiogram, echocardiography, and cardiac troponin – only followed by cardiac magnetic resonance imaging in case of abnormal findings – reported lower myocarditis incidences (0.5%, 20/3978). On the other hand, advanced screening that included cardiac magnetic resonance imaging within the primary screening reported higher incidences (2.4%, 52/2160). The sensitivity of advanced screening seems to be 4.8 times higher in comparison to conventional screening. However, we recommend prioritization of conventional screening, as the economical load of advanced screening for all athletes is high and the incidence of myocarditis in SARS-CoV-2-positive athletes and the risk of adverse outcomes seems low. Future research will be important to analyze the long-term effects of myocarditis after infection with SARS-CoV-2 in athletes for risk stratification to optimally guide a safe return to sport.

Key words

return to sport - COVID-19 - CMR - review

Publikationsverlauf

Eingereicht: 05. Oktober 2022

Angenommen: 22. Mai 2023

Accepted Manuscript online:
24. Mai 2023

Artikel online veröffentlicht:
06. Oktober 2023

• References

• 1 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
• 2 Hoffmann M, Kleine-Weber H, Schroeder S. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181: 271-280
• 3 El-Arif G, Farhat A, Khazaal S. et al. The renin-angiotensin system: A key role in SARS-CoV-2-induced COVID-19. Molecules 2021; 26: 1-31
• 4 Clerkin KJ, Fried JA, Raikhelkar J. et al. COVID-19 and cardiovascular disease. Circulation 2020; 141: 1648-1655
• 5 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; 5: 1265-1273
• 6 Wang Y, Wang Y, Chen Y. et al. Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID-19) implicate special control measures. J Med Virol 2020; 92: 568-576
• 7 Zhou F, Yu T, Du R. et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet 2020; 395: 1054-1062
• 8 Huang L, Zhao P, Tang D. et al. Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging 2020; 13: 2330-2339
• 9 Brito D, Meester S, Yanamala N. et al. high prevalence of pericardial involvement in college student athletes recovering from COVID-19. JACC Cardiovasc Imaging 2021; 14: 541-555
• 10 Cavigli L, Frascaro F, Turchini F. et al. A prospective study on the consequences of SARS-CoV-2 infection on the heart of young adult competitive athletes: Implications for a safe return-to-play. Int J Cardiol 2021; 336: 130-136
• 11 Clark DE, Dendy JM, Li DL. et al. Cardiovascular magnetic resonance evaluation of soldiers after recovery from symptomatic SARS-CoV-2 infection: a case-control study of cardiovascular post-acute sequelae of SARS-CoV-2 infection (CV PASC). J Cardiovasc Magn ResonS 2021; 23: 1-9
• 12 Clark DE, Parikh A, Dendy JM. et al. COVID-19 myocardial pathology evaluation in athletes with cardiac magnetic resonance (COMPETE CMR). Circulation 2021; 143: 609-612
• 13 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: 1078-1087
• 14 Hendrickson BS, Stephens RE, Chang JV. et al. Cardiovascular evaluation after COVID-19 in 137 collegiate athletes: Results of an algorithm-guided screening. Circulation 2021; 143: 1926-1928
• 15 Malek LA, Marczak M, Milosz-Wieczorek B. et al. Cardiac involvement in consecutive elite athletes recovered from Covid-19: A magnetic resonance study. J Magn Reson Imaging 2021; 53: 1723-1729
• 16 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: 745-752
• 17 Moulson N, Petek BJ, Drezner JA. et al. SARS-CoV-2 cardiac involvement in young competitive athletes. Circulation 2021; 144: 256-266
• 18 Rajpal S, Tong MS, Borchers J. et al. Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection. JAMA Cardiol 2021; 6: 116-118
• 19 Starekova J, Bluemke DA, Bradham WS. et al. Evaluation for myocarditis in competitive student athletes recovering from coronavirus disease 2019 with cardiac magnetic resonance imaging. JAMA Cardiol 2021; 6: 945-950
• 20 Szabo L, Juhasz V, Dohy Z. et al. Is cardiac involvement prevalent in highly trained athletes after SARS-CoV-2 infection? A cardiac magnetic resonance study using sex-matched and age-matched controls. Br J Sports Med 2022; 56: 553-560
• 21 Cates J, Lucero-Obusan C, Dahl RM. et al. Risk for in-hospital complications associated with COVID-19 and influenza - Veterans Health Administration, United States, October 1, 2018–May 31, 2020. MMWR Morb Mortal Wkly Rep 2020; 69: 1528-1534
• 22 Peake JM, Neubauer O, Walsh NP. et al. Recovery of the immune system after exercise. J Appl Physiol 1985; 2017: 1077-1087
• 23 Harmon KG, Asif IM, Maleszewski JJ. et al. Incidence, cause, and comparative frequency of sudden cardiac death in National Collegiate Athletic Association Athletes: A decade in review. Circulation 2015; 132: 10-19
• 24 Finocchiaro G, Papadakis M, Robertus JL. et al. Etiology of sudden death in sports: insights from a United Kingdom regional registry. J Am Coll Cardiol 2016; 67: 2108-2115
• 25 Peterson DF, Kucera K, Thomas LC. et al. Aetiology and incidence of sudden cardiac arrest and death in young competitive athletes in the USA: a 4-year prospective study. Br J Sports Med 2021; 55: 1196-1203
• 26 Bohm P, Scharhag J, Egger F. et al. Sports-related sudden cardiac arrest in Germany. Can J Cardiol 2021; 37: 105-112
• 27 Imazio M, Demichelis B, Cecchi E. et al. Cardiac troponin I in acute pericarditis. J Am Coll Cardiol 2003; 42: 2144-2148
• 28 Harris KM, Mackey-Bojack S, Bennett M. et al. Sudden unexpected death due to myocarditis in young people, including athletes. Am J Cardiol 2021; 143: 131-134
• 29 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: 219-227
• 30 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: 1717-1756
• 31 Steinacker JM, Schellenberg J, Bloch W. et al. Recommendations for return-to-sport after COVID-19: Expert consensus. Dtsch Z Sportmed 2022; 73: 127-136