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Myocarditis in the Athlete: Arrhythmogenic Substrates, Clinical Manifestations, Management, and Eligibility Decisions

Abstract

Myocarditis is as an important cause of sudden cardiac death (SCD) among athletes. The incidence of SCD ascribed to myocarditis did not change after the introduction of pre-participation screening in Italy, due to the transient nature of the disease and problems in the differential diagnosis with the athlete’s heart. The arrhythmic burden and the underlying mechanisms differ between the acute and chronic setting, depending on the relative impact of acute inflammation versus post-inflammatory myocardial fibrosis. In the acute phase, ventricular arrhythmias vary from isolated ventricular ectopic beats to complex tachycardias that can lead to SCD. Atrioventricular blocks are typical of specific forms of myocarditis, and supraventricular arrhythmias may be observed in case of atrial inflammation. Athletes with acute myocarditis should be temporarily restricted from physical exercise, until complete recovery. However, ventricular tachycardia may also occur in the chronic phase in the context of post-inflammatory myocardial scar.

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Abbreviations

AM:

Acute myocarditis

SCD:

Sudden cardiac death

EMB:

Endomyocardial biopsy

LGE:

Late gadolinium enhancement

CMR:

Cardiac magnetic resonance

AV:

Atrioventricular

LV:

Left ventricular

AF:

Atrial fibrillation

VF:

Ventricular fibrillation

VT:

Ventricular tachycardia

ICD:

Implantable cardioverter defibrillator

ARVC:

Arrhythmogenic right ventricular cardiomyopathy

References

  1. 1.

    Caforio, A. L. P., Pankuweit, S., Arbustini, E., Basso, C., Gimeno-Blanes, J., Felix, S. B., et al. (2013). Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. European Heart Journal, 34(33), 2636–2648.

    PubMed  Google Scholar 

  2. 2.

    Caforio, A. L. P., Marcolongo, R., Basso, C., & Iliceto, S. (2015). Clinical presentation and diagnosis of myocarditis. Heart, 101(16), 1332–1344.

    CAS  PubMed  Google Scholar 

  3. 3.

    Baksi, A. J., Kanaganayagam, G. S., & Prasad, S. K. (2015). Arrhythmias in viral myocarditis and pericarditis. Cardiac Electrophysiology Clinics, 7(2), 269–281.

    PubMed  Google Scholar 

  4. 4.

    Priori, S. G., Blomstrom-Lundqvist, C., Mazzanti, A., Bloma, N., Borggrefe, M., Camm, J., et al. (2015). 2015 ESC guidelines for the management of patients with ventricular arrhythmias and the prevention of sudden cardiac death the Task Force for the Management of Patients with Ventricular Arrhythmias and the Prevention of Sudden Cardiac Death of the European Society of Cardiology (ESC). Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC). European Heart Journal, 36(41), 2793–2867.

    PubMed  Google Scholar 

  5. 5.

    Basso, C., Carturan, E., Corrado, D., & Thiene, G. (2007). Myocarditis and dilated cardiomyopathy in athletes: diagnosis, management, and recommendations for sport activity. Cardiology Clinics, 25(3), 423–429.

    PubMed  Google Scholar 

  6. 6.

    Zorzi, A., Marra, M. P., Rigato, I., De Lazzari, M., Susana, A., Niero, A., et al. (2016). Nonischemic left ventricular scar as a substrate of life-threatening ventricular arrhythmias and sudden cardiac death in competitive athletes. Circulation Arrhythmia and Electrophysiology, 9, e004229.

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Brolinson, P., & Elliott, D. (2007). Exercise and the immune system. Clinical Journal of Sport Medicine, 26(3), 311–319.

    Google Scholar 

  8. 8.

    Nieman, D. C. (1999). Nutrition, exercise, and immune system function. Clinics in Sports Medicine, 18(3), 537–548.

    CAS  PubMed  Google Scholar 

  9. 9.

    Nieman, D. C. (2000). Is infection risk linked to exercise workload? Medicine and Science in Sports and Exercise, 32(7), S406–S411.

    CAS  PubMed  Google Scholar 

  10. 10.

    Keaney, L. C., Kilding, A. E., Merien, F., & Dulson, D. K. (2018). The impact of sport related stressors on immunity and illness risk in team-sport athletes. Journal of Science and Medicine in Sport, 21(12), 1992–1999.

    Google Scholar 

  11. 11.

    Moreira, A., Mortatti, A. L., Arruda, A. F. S., Freitas, C. G., De Arruda, M., & Aoki, M. S. (2014). Salivary IgA response and upper respiratory tract infection symptoms during a 21-week competitive season in young soccer players. Journal of Strength and Conditioning Research, 28(2), 467–473.

    PubMed  Google Scholar 

  12. 12.

    Fahlman, M. M., & Engels, H. J. (2005). Mucosal IgA and URTI in American college football players: a year longitudinal study. Medicine and Science in Sports and Exercise, 37(3), 374–380.

    CAS  PubMed  Google Scholar 

  13. 13.

    Zhao, G., Zhou, S., Davie, A., & Su, Q. (2012). Effects of moderate and high intensity exercise on T1/T2 balance. Exercise Immunology Review, 18, 97–113.

    CAS  Google Scholar 

  14. 14.

    Gleeson, M., & Pyne, D. B. (2016). Respiratory inflammation and infections in high-performance athletes. Immunology and Cell Biology, 94(2), 124–131.

    CAS  PubMed  Google Scholar 

  15. 15.

    Gatmaitan, B., Chason, J., & Lerner, M. (1970). Augmentation of the virulence of murine coxsackie-virus B-3 myocardiopathy by exercise. The Journal of Experimental Medicine, 131(6), 1121–1136.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Kiel, R., Smith, F., Chason, J., Khatib, R., & Reyes, M. (1989). Coxsackievirus B3 myocarditis in C3H/HeJ mice: description of an inbred model and the effect of exercise on virulence. European Journal of Epidemiology, 5(3), 348–350.

    CAS  PubMed  Google Scholar 

  17. 17.

    Gabilondo, A., Alonso-Moran, E., Nuño-Solinis, R., Orueta, J. F., & Iruin, A. (2017). Comorbidities with chronic physical conditions and gender profiles of illness in schizophrenia. Results from PREST, a new health dataset. Journal of Psychosomatic Research, 93, 102–109.

    PubMed  Google Scholar 

  18. 18.

    Lerner, A., & Wilson, F. (1973). Virus myocardiopathy. Progress in Medical Virology, 15, 63–91.

    CAS  Google Scholar 

  19. 19.

    Hosenpud, J. D., Campbell, S. M., Niles, N. R., Lee, J., Mendelson, D., & Hart, M. V. (1987). Exercise induced augmentation of cellular and humoral autoimmunity associated with increased cardiac dilatation in experimental autoimmune myocarditis. Cardiovascular Research, 21(3), 217–222.

    CAS  PubMed  Google Scholar 

  20. 20.

    Maron, B. J., McKenna, W. J., Danielson, G. K., Kappenberger, L. J., Kuhn, H. J., Seidman, C. E., et al. (2003). American College of Cardiology/European Society of Cardiology Clinical Expert Consensus Document on Hypertrophic Cardiomyopathy: a Report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents and the European Society of Cardiology Committee for Practice Guidelines. Journal of the American College of Cardiology, 42(9), 1687–1713.

    PubMed  Google Scholar 

  21. 21.

    Maron, B. J., Doerer, J. J., Haas, T. S., Tierney, D. M., & Mueller, F. O. (2009). Sudden deaths in young competitive athletes analysis of 1866 deaths in the United States, 1980-2006. Circulation, 119(8), 1085–1092.

    PubMed  Google Scholar 

  22. 22.

    Harmon, K. G., Asif, I. M., Maleszewski, J. J., Owens, D. S., Prutkin, J. M., Salerno, J. C., et al. (2015). Incidence, cause, and comparative frequency of sudden cardiac death in National Collegiate Athletic Association Athletes. Circulation, 132(1), 10–19.

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Finocchiaro, G., Papadakis, M., Robertus, J. L., Dhutia, H., Steriotis, A. K., Tome, M., et al. (2016). Etiology of sudden death in sports insights from a United Kingdom Regional Registry. Journal of the American College of Cardiology, 67(18), 2108–2115.

    PubMed  Google Scholar 

  24. 24.

    Thiene, G. (2018). Sudden cardiac death in the young: a genetic destiny? Clinical Medicine (London, England), 18, s17–s23.

    Google Scholar 

  25. 25.

    Corrado, D., Basso, C., Pavei, A., Michieli, P., Schiavon, M., & Thiene, G. (2006). Trends in sudden cardiovascular death in young competitive athletes after implementation of a preparticipation screening program. Journal of the American Medical Association, 296(13), 1593–1601.

    CAS  PubMed  Google Scholar 

  26. 26.

    Cooper, L. T., Baughman, K. L., Feldman, A. M., Frustaci, A., Jessup, M., Kuhl, U., et al. (2007). The role of endomyocardial biopsy in the management of cardiovascular disease. Journal of the American College of Cardiology, 50(19), 1914–1931.

    PubMed  Google Scholar 

  27. 27.

    Ukena, C., Mahfoud, F., Kindermann, I., Kandolf, R., Kindermann, M., & BÖhm, M. (2011). Prognostic electrocardiographic parameters in patients with suspected myocarditis. European Journal of Heart Failure, 13(4), 398–405.

    PubMed  Google Scholar 

  28. 28.

    De Lazzari, M., Zorzi, A., Baritussio, A., Siciliano, M., Migliore, F., Susana, A., et al. (2016). Relationship between T-wave inversion and transmural myocardial edema as evidenced by cardiac magnetic resonance in patients with clinically suspected acute myocarditis: clinical and prognostic implications. Journal of Electrocardiology, 49(4), 587–595.

    PubMed  Google Scholar 

  29. 29.

    Noseworthy, P. A., Weiner, R., Kim, J., Keelara, V., Wang, F., Berkstresser, B., et al. (2011). Early repolarization pattern in competitive athletes: clinical correlates and the effects of exercise training. Circulation. Arrhythmia and Electrophysiology, 4(4), 432–440.

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Calore, C., Zorzi, A., Sheikh, N., Nese, A., Facci, M., Malhotra, A., et al. (2016). Electrocardiographic anterior T-wave inversion in athletes of different ethnicities: differential diagnosis between athlete’s heart and cardiomyopathy. European Heart Journal, 37(32), 2515–2527.

    PubMed  Google Scholar 

  31. 31.

    Zorzi, A., Calore, C., Vio, R., Pelliccia, A., & Corrado, D. (2018). Accuracy of the ECG for differential diagnosis between hypertrophic cardiomyopathy and athlete’s heart: comparison between the European Society of Cardiology (2010) and International (2017) criteria. British Journal of Sports Medicine, 52(10), 667–673.

    PubMed  Google Scholar 

  32. 32.

    Sedaghat-Hamedani, F., Kayvanpour, E., Frankenstein, L., Mereles, D., Amr, A., Buss, S., et al. (2015). Biomarker changes after strenuous exercise can mimic pulmonary embolism and cardiac injury - a metaanalysis of 45 studies. Clinical Chemistry, 61(10), 1246–1255.

    CAS  PubMed  Google Scholar 

  33. 33.

    Pinamonti, B., Alberti, E., Cigalotto, A., Dreas, L., Salvi, A., Silvestri, F., & Camerini, F. (1988). Echocardiographic findings in myocarditis. The American Journal of Cardiology, 62(4), 285–291.

    CAS  PubMed  Google Scholar 

  34. 34.

    Urhausen, A., Kindermann, M., Bohm, M., & Kindermann, W. (2003). Images in cardiovascular medicine. Diagnosis of myocarditis by cardiac tissue velocity imaging in an Olympic athlete. Circulation, 103(4), e21–e22.

    Google Scholar 

  35. 35.

    Eichhorn, C., Bière, L., Schnell, F., Schmied, C., Wilhelm, M., Kwong, R. Y., & Gräni, C. (2019). Myocarditis in athletes is a challenge: diagnosis, risk stratification, and uncertainties. JACC: Cardiovascular Imaging. https://doi.org/10.1016/j.jcmg.2019.01.039.

  36. 36.

    Friedrich, M. G., Sechtem, U., Schulz-Menger, J., Holmvang, G., Alakija, P., Cooper, L. T., et al. (2009). Cardiovascular magnetic resonance in myocarditis: a JACC white paper. Journal of the American College of Cardiology, 53(17), 1475–1487.

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    Caforio, A. L. P., Calabrese, F., Angelini, A., Tona, F., Vinci, A., Bottaro, S., et al. (2007). A prospective study of biopsy-proven myocarditis: prognostic relevance of clinical and aetiopathogenetic features at diagnosis. European Heart Journal, 28(11), 1326–1333.

    PubMed  Google Scholar 

  38. 38.

    Grün, S., Schumm, J., Greulich, S., Wagner, A., Schneider, S., Bruder, O., et al. (2012). Long-term follow-up of biopsy-proven viral myocarditis. Journal of the American College of Cardiology, 59(18), 1604–1615.

    PubMed  Google Scholar 

  39. 39.

    Anzini, M., Merlo, M., Sabbadini, G., Barbati, G., Finocchiaro, G., Pinamonti, B., et al. (2013). Long-term evolution and prognostic stratification of biopsy-proven active myocarditis. Circulation, 128(22), 2384–2394.

    PubMed  Google Scholar 

  40. 40.

    Anderson, B. R., Silver, E. S., Richmond, E., Liberman, L. (2014) Usefulness of Arrhythmias as Predictors of Death and Resource Utilization in Children With Myocarditis. The American Journal of Cardiology 114 (9):1400–1405

  41. 41.

    Begieneman, M. P. V., Emmens, R. W., Rijvers, L., Kubat, B., Paulus, W. J., Vonk, A. B. A., et al. (2016). Ventricular myocarditis coincides with atrial myocarditis in patients. Cardiovascular Pathology, 25(2), 141–148.

    PubMed  Google Scholar 

  42. 42.

    Habara, M., Fujieda, H., & Nakamura, Y. (2006). Images in cardiology - atrial myocarditis: a possible cause of idiopathic enlargement of bilateral atria. Heart, 92(6), 842.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Larsen, B., Maleszewski, J., Edwards, W., Cooper Jr., L., Sobonya, R., Thompson, E., et al. (2013). Atrial giant cell myocarditis: a distinctive clinicopathologic entity. Circulation, 127(1), 39–47.

    PubMed  Google Scholar 

  44. 44.

    Frustaci, A., Cameli, S., & Zeppilli, P. (1995). Biopsy evidence of atrial myocarditis in an athlete developing transient sinoatrial disease. Chest, 108(5), 1460–1462.

    CAS  PubMed  Google Scholar 

  45. 45.

    Schnabel, R. B., Larson, M. G., Yamamoto, J. F., Kathiresan, S., Rong, J., Levy, D., et al. (2009). Relation of multiple inflammatory biomarkers to incident atrial fibrillation. The American Journal of Cardiology, 104(1), 92–96.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Marcus, G. M., Smith, L. M., Ordovas, K., Scheinman, M. M., Kim, A. M., Badhwar, N., et al. (2010). Intracardiac and extracardiac markers of inflammation during atrial fibrillation. Heart Rhythm, 7(2), 149–154.

    PubMed  Google Scholar 

  47. 47.

    Imazio, M., & Trinchero, R. (2008). Myopericarditis: etiology, management, and prognosis. International Journal of Cardiology, 127(1), 17–26.

    PubMed  Google Scholar 

  48. 48.

    Haissaguerre, M., Jais, P., Shah, D., Takahashi, A., Hocini, M., Quiniou, G., et al. (1998). Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins. The New England Journal of Medicine, 339(10), 659–666.

    CAS  PubMed  Google Scholar 

  49. 49.

    Basso, C., Corrado, D., Rossi, L., & Thiene, G. (2001). Ventricular preexcitation in children and young adults: atrial myocarditis as a possible trigger of sudden death. Circulation, 103(2), 269–275.

    CAS  PubMed  Google Scholar 

  50. 50.

    Jais, P., Haissaguerre, M., Shah, D., Chouairi, S., Gencel, L., Hocini, M., & Clementy, J. (1997). A focal source of atrial fibrillation treated by discrete radiofrequency ablation. Circulation, 95(3), 572–576.

    CAS  PubMed  Google Scholar 

  51. 51.

    Haissaguerre, M., Jais, P., Shah, D., Garrigue, S., Takahashi, A., Lervegne, T., et al. (2000). Electrophysiological end point for catheter ablation of atrial fibrillation initiated from multiple pulmonary venous foci. Circulation, 101(12), 1409–1417.

    CAS  PubMed  Google Scholar 

  52. 52.

    Haissaguerre, M., Shah, D., Jais, P., Hocini, M., Yamane, T., Deisenhofer, I., et al. (2000). Electrophysiological breakthroughs from the left atrium to the pulmonary veins. Circulation, 102(20), 2463–2465.

    CAS  PubMed  Google Scholar 

  53. 53.

    Katritsis, D. G., Boriani, G., Cosio, F. G., Hindricks, G., Jais, P., Josephson, M. E., et al. (2018). European Heart Rhythm Association (EHRA) consensus document on the management of supraventricular arrhythmias, endorsed by Heart Rhythm Society (HRS), Asia-Pacific Heart Rhythm Society (APHRS), and Sociedad Latinoamericana de Estimulación Cardiaca y Electrofisiologia (SOLAECE). European Heart Journal, 39(16), 1442–1445.

    PubMed  Google Scholar 

  54. 54.

    Frustaci, A., Chimenti, C., Bellocci, F., Morgante, E., Russo, M. A., & Maseri, A. (1997). Histological substrate of atrial biopsies in patients with lone atrial fibrillation. Circulation, 96(4), 1180–1184.

    CAS  PubMed  Google Scholar 

  55. 55.

    Cooper, L. T., Berry, G. J., & Shabetai, R. (1997). Idiopathic giant-cell myocarditis — natural history and treatment. The New England Journal of Medicine, 336(26), 1860–1866.

    PubMed  Google Scholar 

  56. 56.

    Ekstrom, K., Lehtonen, J., Kandolin, R., Raisanen-Sokolowski, A., Salmenkivi, K., & Kupari, M. (2016). Long-term outcome and its predictors in giant cell myocarditis. European Journal of Heart Failure, 18(12), 1452–1458.

    PubMed  Google Scholar 

  57. 57.

    Hamzeh, N., Steckman, D. A., Sauer, W. H., & Judson, M. A. (2015). Pathophysiology and clinical management of cardiac sarcoidosis. Nature Reviews. Cardiology, 12(5), 278–288.

    PubMed  Google Scholar 

  58. 58.

    Baughman, R. P., & Grutters, J. C. (2015). New treatment strategies for pulmonary sarcoidosis: antimetabolites, biological drugs, and other treatment approaches. The Lancet Respiratory Medicine, 3(10), 813–822.

    CAS  PubMed  Google Scholar 

  59. 59.

    Facco, M., Cabrelle, A., Teramo, A., Olivieri, V., Gnoato, M., Teolato, S., et al. (2011). Sarcoidosis is a Th1/Th17 multisystem disorder. Thorax, 66(2), 144–150.

    PubMed  Google Scholar 

  60. 60.

    Caforio, A. L. P., Adler, Y., Agostini, C., Allanore, Y., Anastasakis, A., Arad, M., et al. (2017). Diagnosis and management of myocardial involvement in systemic immune-mediated diseases: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Disease. European Heart Journal, 38(35), 2649–2662.

    CAS  PubMed  Google Scholar 

  61. 61.

    McAlister, H. F., Klementowicz, P. T., Andrews, C., Fisher, J. D., Feld, M., & Furman, S. (1989). Lyme carditis: an important cause of reversible heart block. Annals of Internal Medicine, 110(5), 339–345.

    CAS  PubMed  Google Scholar 

  62. 62.

    Celik, T., Selimov, N., Vekilova, A., Kursaklioglu, H., Iyisoy, A., Kilic, S., & Isik, E. (2006). Prognostic significance of electrocardiographic abnormalities in diphtheritic myocarditis after hospital discharge: a long-term follow-up study. Annals of Noninvasive Electrocardiology, 11(1), 28–33.

    PubMed  PubMed Central  Google Scholar 

  63. 63.

    Rassi Jr., A., Rassi, A., Little, W. C., Xavier, S. S., Rassi, S. G., Rassi, A. G., et al. (2006). Development and validation of a risk score for predicting death in Chagas’ heart disease. The New England Journal of Medicine, 355(8), 799–808.

    CAS  PubMed  Google Scholar 

  64. 64.

    Punja, M., Mark, D. G., McCoy, J. V., Javan, R., Pines, J. M., & Brady, W. (2010). Electrocardiographic manifestations of cardiac infectious-inflammatory disorders. The American Journal of Emergency Medicine, 28(3), 364–377.

    PubMed  Google Scholar 

  65. 65.

    Yilmaz, A., Mahrholdt, H., Athanasiadis, A., Vogelsberg, H., Meinhardt, G., Voehringer, M., et al. (2008). Coronary vasospasm as the underlying cause for chest pain in patients with PVB19 myocarditis. Heart, 94(11), 1456–1463.

    CAS  PubMed  Google Scholar 

  66. 66.

    Frustaci, A., Verardo, R., Caldarulo, M., Acconcia, M. C., Russo, M. A., & Chimenti, C. (2007). Myocarditis in hypertrophic cardiomyopathy patients presenting acute clinical deterioration. European Heart Journal, 28(6), 733–740.

    PubMed  Google Scholar 

  67. 67.

    Basso, C., Ronco, F., Marcus, F., Abudureheman, A., Rizzo, S., Frigo, A. C., et al. (2008). Quantitative assessment of endomyocardial biopsy in arrhythmogenic right ventricular cardiomyopathy/dysplasia: an in vitro validation of diagnostic criteria. European Heart Journal, 29(22), 2760–2771.

    PubMed  Google Scholar 

  68. 68.

    Chimenti, C., Pieroni, M., Maseri, A., & Frustaci, A. (2004). Histologic findings in patients with clinical and instrumental diagnosis of sporadic arrhythmogenic right ventricular dysplasia. Journal of the American College of Cardiology, 43(12), 2305–2313.

    PubMed  Google Scholar 

  69. 69.

    Bowles, N. E., Ni, J., Marcus, F., & Towbin, J. A. (2002). The detection of cardiotropic viruses in the myocardium of patients with arrhythmogenic right ventricular dysplasia/cardiomyopathy. Journal of the American College of Cardiology, 39(5), 892–895.

    PubMed  Google Scholar 

  70. 70.

    Rademakers, F. E., Rogers, W. J., Guier, W. H., Hutchins, G. M., Siu, C. O., Weisfeldt, M. L., et al. (1994). Relation of regional cross-fiber shortening to wall thickening in the intact heart: three-dimensional strain analysis by NMR tagging. Circulation, 89(3), 1174–1182.

    CAS  PubMed  Google Scholar 

  71. 71.

    Möhlenkamp, S., Lehmann, N., Breuckmann, F., Bröcker-Preuss, M., Nassenstein, K., Halle, M., et al. (2008). Running: the risk of coronary events - prevalence and prognostic relevance of coronary atherosclerosis in marathon runners. European Heart Journal, 29(15), 1903–1910.

    PubMed  Google Scholar 

  72. 72.

    Breuckmann, F., Möhlenkamp, S., Nassenstein, K., Lehmann, N., Ladd, S., Schmermund, A., et al. (2009). Myocardial late gadolinium enhancement: prevalence, pattern, and prognostic relevance in marathon runners. Radiology, 251(1), 50–57.

    PubMed  Google Scholar 

  73. 73.

    Bohm, P., Schneider, G., Linneweber, L., Rentzsch, A., Krämer, N., Abdul-Khaliq, H., et al. (2016). Right and left ventricular function and mass in male elite master athletes: a controlled contrast-enhanced cardiovascular magnetic resonance study. Circulation, 133(20), 1927–1935.

    PubMed  Google Scholar 

  74. 74.

    Sanchis-Gomar, F., López-Ramón, M., Alis, R., Garatachea, N., Pareja-Galeano, H., Santos-Lozano, A., et al. (2016). No evidence of adverse cardiac remodeling in former elite endurance athletes. International Journal of Cardiology, 222, 171–177.

    PubMed  Google Scholar 

  75. 75.

    Merghani, A., Maestrini, V., Rosmini, S., Cox, A. T., Dhutia, H., Bastiaenan, R., et al. (2017). Prevalence of subclinical coronary artery disease in masters endurance athletes with a low atherosclerotic risk profile. Circulation, 136(2), 126–137.

    CAS  PubMed  Google Scholar 

  76. 76.

    Tahir, E., Starekova, J., Muellerleile, K., von Stritzky, A., Münch, J., Avanesov, M., et al. (2018). Myocardial fibrosis in competitive triathletes detected by contrast-enhanced CMR correlates with exercise-induced hypertension and competition history. JACC: Cardiovascular Imaging, 11(9), 1260–1270.

    PubMed  Google Scholar 

  77. 77.

    Mousavi, N., Czarnecki, A., Kumar, K., Fallah-Rad, N., Lytwyn, M., Han, S. Y., et al. (2009). Relation of biomarkers and cardiac magnetic resonance imaging after marathon running. The American Journal of Cardiology, 103(10), 1467–1472.

    PubMed  Google Scholar 

  78. 78.

    O’Hanlon, R., Wilson, M., Wage, R., Smith, G., Alpendurada, F., Wong, J., et al. (2010). Troponin release following endurance exercise: is inflammation the cause? A cardiovascular magnetic resonance study. Journal of Cardiovascular Magnetic Resonance, 12, 38.

    PubMed  PubMed Central  Google Scholar 

  79. 79.

    Oomah, S. R., Mousavi, N., Bhullar, N., Kumar, K., Walker, J. R., Lytwyn, M., et al. (2011). The role of three-dimensional echocardiography in the assessment of right ventricular dysfunction after a half marathon: comparison with cardiac magnetic resonance imaging. Journal of the American Society of Echocardiography, 24(2), 207–213.

    PubMed  Google Scholar 

  80. 80.

    Wilson, M., O’Hanlon, R., Prasad, S., Deighan, A., MacMillan, P., Oxborough, D., et al. (2011). Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. Journal of Applied Physiology, 110(6), 1622–1626.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. 81.

    La Gerche, A., Burns, A. T., Mooney, D. J., Inder, W. J., Taylor, A. J., Bogaert, J., et al. (2012). Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. European Heart Journal, 33(8), 998–1006.

    PubMed  Google Scholar 

  82. 82.

    Erz, G., Mangold, S., Franzen, E., Claussen, C. D., Niess, A. M., Burgstahler, C., & Kramer, U. (2013). Correlation between ECG abnormalities and cardiac parameters in highly trained asymptomatic male endurance athletes: evaluation using cardiac magnetic resonance imaging. The International Journal of Cardiovascular Imaging, 29(2), 325–334.

    PubMed  Google Scholar 

  83. 83.

    Mangold, S., Kramer, U., Franzen, E., Erz, G., Bretschneider, C., Seeger, A., et al. (2013). Detection of cardiovascular disease in elite athletes using cardiac magnetic resonance imaging. Rofo, 185(12), 1167–1174.

    CAS  PubMed  Google Scholar 

  84. 84.

    Franzen, E., Mangold, S., Erz, G., Claussen, C. D., Niess, A. M., Kramer, U., & Burgstahler, C. (2013). Comparison of morphological and functional adaptations of the heart in highly trained triathletes and long-distance runners using cardiac magnetic resonance imaging. Heart and Vessels, 28(5), 626–631.

    PubMed  Google Scholar 

  85. 85.

    Corrado, D., Van Tintelen, J., Mckenna, W., Hauer, R., Anastasakis, A., Asimaki, A., et al. (2019). Arrhythmogenic right ventricular cardiomyopathy: evaluation of the current diagnostic criteria and differential diagnosis. European Heart Journal in press.

  86. 86.

    Pelliccia, A., Corrado, D., Bjã¸rnstad, H. H., Panhuyzen-Goedkoop, N., Urhausen, A., Carre, F., et al. (2006). Recommendations for participation in competitive sport and leisure-time physical activity in individuals with cardiomyopathies, myocarditis and pericarditis. European Journal of Preventive Cardiology, 13(6), 876–885.

    Google Scholar 

  87. 87.

    Maron, B. J., Ackerman, M. J., Nishimura, R. A., Pyeritz, R. E., Towbin, J. A., & Udelson, J. E. (2005). Task Force 4: HCM and other cardiomyopathies, mitral valve prolapse, myocarditis, and Marfan syndrome. Journal of the American College of Cardiology, 45(8), 1340–1345.

    PubMed  Google Scholar 

  88. 88.

    Pelliccia, A., Solberg, E. E., Papadakis, M., Adami, P. E., Biffi, A., Caselli, S., et al. (2019). Recommendations for participation in competitive and leisure time sport in athletes with cardiomyopathies, myocarditis, and pericarditis: position statement of the Sport Cardiology Section of the European Association of Preventive Cardiology (EAPC). European Heart Journal, 40(1), 19–33.

    PubMed  Google Scholar 

  89. 89.

    Maron, B. J., Udelson, J. E., Bonow, R. O., Nishimura, R. A., Ackerman, M. J., Estes, N. A. M., et al. (2015). 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. Journal of the American College of Cardiology, 66(21), 2362–2371.

    PubMed  Google Scholar 

  90. 90.

    Zorzi, A., Susana, A., De Lazzari, M., Migliore, F., Vescovo, G., Scarpa, D., et al. (2018). Diagnostic value and prognostic implications of early cardiac magnetic resonance in survivors of out-of-hospital cardiac arrest. Heart Rhythm, 15(7), 1031–1041.

    PubMed  Google Scholar 

  91. 91.

    Zorzi, A., Rigato, I., Pilichou, K., Marra, M. P., Migliore, F., Mazzotti, E., et al. (2016). Phenotypic expression is a prerequisite for malignant arrhythmic events and sudden cardiac death in arrhythmogenic right ventricular cardiomyopathy. Europace, 18(7), 1086–1094.

    PubMed  Google Scholar 

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Correspondence to Domenico Corrado.

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Vio, R., Zorzi, A. & Corrado, D. Myocarditis in the Athlete: Arrhythmogenic Substrates, Clinical Manifestations, Management, and Eligibility Decisions. J. of Cardiovasc. Trans. Res. 13, 284–295 (2020). https://doi.org/10.1007/s12265-020-09996-1

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Keywords

  • Myocarditis
  • Athletes
  • Sport
  • Ventricular tachycardia
  • Ventricular fibrillation
  • Atrial fibrillation
  • Atrioventricular block
  • Sudden death