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Specific Cardiovascular Diseases and Competitive Sports Participation: Myocarditis and Myocardial Fibrosis

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Textbook of Sports and Exercise Cardiology

Abstract

According to recent epidemiologic studies, myocarditis represents one of the major causes of sudden cardiac death among young competitive athletes. Myocarditis can be caused by infectious agents (with viral myocarditis being the leading cause), systemic auto-immune diseases, medical drugs and toxic agents. Since myocarditis is an acquired disease, systematic screening programs will fail to depict this disease. Nevertheless, an adapted prevention can decrease its incidence in athletes. Information on not to train in case of infection and systemic symptoms and on the potential adverse effects of doping agents and recreational drugs is essential for the prevention of myocarditis in athletes. The diagnosis of myocarditis is challenging, due to the heterogeneity of its clinical presentation. Cardiovascular symptoms, ECG and echocardiographic changes, as well as elevation of troponin are rather unspecific. If these first line examinations are suggestive, cardiac MRI should be performed, and the diagnosis should be based on the Lake Louise Consensus criteria. Endomyocardial biopsy, the gold standard for diagnosis, should be limited to recent-onset, high-risk major clinical syndromes not responding to conventional medical therapy. In case of myocarditis, the treatment is essentially symptomatic and based on the management of arrhythmic and heart failure complications. Sport restriction is of course warranted in order to prevent potential lethal arrhythmias and to decrease the risk of negative ventricular remodelling. Athletes with a diagnosis of myocarditis should be restricted from exercise programs for a period of 3–6 months. Asymptomatic patients might be able to resume training and competition if serum markers of myocardial injury, inflammation, and heart failure have normalized, if ventricular systolic function has returned to the normal range, and if no significant arrhythmia occurs on a 24-h ECG monitoring and during an exercise test.

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References

  1. Bohm P, Scharhag J, Meyer T. Data from a nationwide registry on sports-related sudden cardiac deaths in Germany. Eur J Prev Cardiol. 2016;23(6):649–56.

    Article  PubMed  Google Scholar 

  2. Harmon KG, Asif IM, Maleszewski JJ, Owens DS, Prutkin JM, Salerno JC, et al. Incidence, cause, and comparative frequency of sudden cardiac death in National Collegiate Athletic Association Athletes: a decade in review. Circulation. 2015;132(1):10–9.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Reyes MP, Ho KL, Smith F, Lerner AM. A mouse model of dilated-type cardiomyopathy due to coxsackievirus B3. J Infect Dis. 1981;144(3):232–6.

    Article  CAS  PubMed  Google Scholar 

  4. Rose NR. Myocarditis: infection versus autoimmunity. J Clin Immunol. 2009;29(6):730–7.

    Article  CAS  PubMed  Google Scholar 

  5. Schultheiss HP, Kuhl U, Cooper LT. The management of myocarditis. Eur Heart J. 2011;32(21):2616–25.

    Article  PubMed  Google Scholar 

  6. Caforio AL, Pankuweit S, Arbustini E, Basso C, Gimeno-Blanes J, Felix SB, et al. 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. Eur Heart J. 2013;34(33):2636–48, 48a-48d

    Article  PubMed  Google Scholar 

  7. Rump AF, Theisohn M, Klaus W. The pathophysiology of cocaine cardiotoxicity. Forensic Sci Int. 1995;71(2):103–15.

    Article  CAS  PubMed  Google Scholar 

  8. Montisci M, El Mazloum R, Cecchetto G, Terranova C, Ferrara SD, Thiene G, et al. Anabolic androgenic steroids abuse and cardiac death in athletes: morphological and toxicological findings in four fatal cases. Forensic Sci Int. 2012;217(1-3):e13–8.

    Article  CAS  PubMed  Google Scholar 

  9. Schurer S, Klingel K, Sandri M, Majunke N, Besler C, Kandolf R, et al. Clinical characteristics, histopathological features, and clinical outcome of methamphetamine-associated cardiomyopathy. JACC Heart Fail. 2017;5(6):435–45.

    Article  PubMed  Google Scholar 

  10. Ulrich R, Pope HG Jr, Cleret L, Petroczi A, Nepusz T, Schaffer J, et al. Doping in two elite athletics competitions assessed by randomized-response surveys. Sports Med. 2018;48(1):211–9.

    Article  PubMed  Google Scholar 

  11. Roberts JA. Viral illnesses and sports performance. Sports Med. 1986;3(4):298–303.

    Article  CAS  PubMed  Google Scholar 

  12. Reyes MP, Lerner AM. Interferon and neutralizing antibody in sera of exercised mice with coxsackievirus B-3 myocarditis. Proc Soc Exp Biol Med. 1976;151(2):333–8.

    Article  CAS  PubMed  Google Scholar 

  13. Nieman DC. Is infection risk linked to exercise workload? Med Sci Sports Exerc. 2000;32(7 Suppl):S406–11.

    Article  CAS  PubMed  Google Scholar 

  14. Tomasi TB, Trudeau FB, Czerwinski D, Erredge S. Immune parameters in athletes before and after strenuous exercise. J Clin Immunol. 1982;2(3):173–8.

    Article  CAS  PubMed  Google Scholar 

  15. Primos WA Jr. Sports and exercise during acute illness. Phys Sportsmed. 1996;24(1):44–54.

    Article  PubMed  Google Scholar 

  16. Wesslen L, Pahlson C, Lindquist O, Hjelm E, Gnarpe J, Larsson E, et al. An increase in sudden unexpected cardiac deaths among young Swedish orienteers during 1979-1992. Eur Heart J. 1996;17(6):902–10.

    Article  CAS  PubMed  Google Scholar 

  17. Metz JP. Upper respiratory tract infections: who plays, who sits? Curr Sports Med Rep. 2003;2(2):84–90.

    Article  PubMed  Google Scholar 

  18. Exercise and febrile illnesses. Paediatr Child Health. 2007;12(10):885–92.

    Google Scholar 

  19. Sinagra G, Anzini M, Pereira NL, Bussani R, Finocchiaro G, Bartunek J, et al. Myocarditis in clinical practice. Mayo Clin Proc. 2016;91(9):1256–66.

    Article  PubMed  Google Scholar 

  20. Grani C, Eichhorn C, Biere L, Murthy VL, Agarwal V, Kaneko K, et al. Prognostic value of cardiac magnetic resonance tissue characterization in risk stratifying patients with suspected myocarditis. J Am Coll Cardiol. 2017;70(16):1964–76.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Morgera T, Di Lenarda A, Dreas L, Pinamonti B, Humar F, Bussani R, et al. Electrocardiography of myocarditis revisited: clinical and prognostic significance of electrocardiographic changes. Am Heart J. 1992;124(2):455–67.

    Article  CAS  PubMed  Google Scholar 

  22. Pinamonti B, Alberti E, Cigalotto A, Dreas L, Salvi A, Silvestri F, et al. Echocardiographic findings in myocarditis. Am J Cardiol. 1988;62(4):285–91.

    Article  CAS  PubMed  Google Scholar 

  23. Wu C, Singh A, Collins B, Fatima A, Qamar A, Gupta A, et al. Causes of troponin elevation and associated mortality in young patients. Am J Med. 2018;131(3):284–92. e1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Smith SC, Ladenson JH, Mason JW, Jaffe AS. Elevations of cardiac troponin I associated with myocarditis. Experimental and clinical correlates. Circulation. 1997;95(1):163–8.

    Article  CAS  PubMed  Google Scholar 

  25. Sedaghat-Hamedani F, Kayvanpour E, Frankenstein L, Mereles D, Amr A, Buss S, et al. Biomarker changes after strenuous exercise can mimic pulmonary embolism and cardiac injury—a metaanalysis of 45 studies. Clin Chem. 2015;61(10):1246–55.

    Article  CAS  PubMed  Google Scholar 

  26. Shave R, Baggish A, George K, Wood M, Scharhag J, Whyte G, et al. Exercise-induced cardiac troponin elevation: evidence, mechanisms, and implications. J Am Coll Cardiol. 2010;56(3):169–76.

    Article  CAS  PubMed  Google Scholar 

  27. Mahfoud F, Gartner B, Kindermann M, Ukena C, Gadomski K, Klingel K, et al. Virus serology in patients with suspected myocarditis: utility or futility? Eur Heart J. 2011;32(7):897–903.

    Article  CAS  PubMed  Google Scholar 

  28. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, et al. Cardiovascular magnetic resonance in myocarditis: a JACC white paper. J Am Coll Cardiol. 2009;53(17):1475–87.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Grun S, Schumm J, Greulich S, Wagner A, Schneider S, Bruder O, et al. Long-term follow-up of biopsy-proven viral myocarditis: predictors of mortality and incomplete recovery. J Am Coll Cardiol. 2012;59(18):1604–15.

    Article  PubMed  Google Scholar 

  30. Yilmaz A, Kindermann I, Kindermann M, Mahfoud F, Ukena C, Athanasiadis A, et al. Comparative evaluation of left and right ventricular endomyocardial biopsy: differences in complication rate and diagnostic performance. Circulation. 2010;122(9):900–9.

    Article  PubMed  Google Scholar 

  31. Nadjiri J, Nieberler H, Hendrich E, Greiser A, Will A, Martinoff S, et al. Performance of native and contrast-enhanced T1 mapping to detect myocardial damage in patients with suspected myocarditis: a head-to-head comparison of different cardiovascular magnetic resonance techniques. Int J Cardiovasc Imaging. 2017;33(4):539–47.

    Article  PubMed  Google Scholar 

  32. Radunski UK, Lund GK, Saring D, Bohnen S, Stehning C, Schnackenburg B, et al. T1 and T2 mapping cardiovascular magnetic resonance imaging techniques reveal unapparent myocardial injury in patients with myocarditis. Clin Res Cardiol. 2017;106(1):10–7.

    Article  CAS  PubMed  Google Scholar 

  33. Cooper LT, Baughman KL, Feldman AM, Frustaci A, Jessup M, Kuhl U, et al. The role of endomyocardial biopsy in the management of cardiovascular disease: a scientific statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. Endorsed by the Heart Failure Society of America and the Heart Failure Association of the European Society of Cardiology. J Am Coll Cardiol. 2007;50(19):1914–31.

    Article  PubMed  Google Scholar 

  34. Holzmann M, Nicko A, Kuhl U, Noutsias M, Poller W, Hoffmann W, et al. Complication rate of right ventricular endomyocardial biopsy via the femoral approach: a retrospective and prospective study analyzing 3048 diagnostic procedures over an 11-year period. Circulation. 2008;118(17):1722–8.

    Article  PubMed  Google Scholar 

  35. Baughman KL. Diagnosis of myocarditis: death of Dallas criteria. Circulation. 2006;113(4):593–5.

    Article  PubMed  Google Scholar 

  36. Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JGF, Coats AJS, et al. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: The Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC)Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J. 2016;37(27):2129–200.

    Article  PubMed  Google Scholar 

  37. Priori SG, Blomstrom-Lundqvist C, Mazzanti A, Blom N, Borggrefe M, Camm J, et al. 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). Eur Heart J. 2015;36(41):2793–867.

    Article  PubMed  Google Scholar 

  38. Adler Y, Charron P, Imazio M, Badano L, Baron-Esquivias G, Bogaert J, et al. 2015 ESC Guidelines for the diagnosis and management of pericardial diseases: The Task Force for the Diagnosis and Management of Pericardial Diseases of the European Society of Cardiology (ESC)Endorsed by: The European Association for Cardio-Thoracic Surgery (EACTS). Eur Heart J. 2015;36(42):2921–64.

    Article  PubMed  Google Scholar 

  39. Kiel RJ, Smith FE, Chason J, Khatib R, Reyes MP. Coxsackievirus B3 myocarditis in C3H/HeJ mice: description of an inbred model and the effect of exercise on virulence. Eur J Epidemiol. 1989;5(3):348–50.

    Article  CAS  PubMed  Google Scholar 

  40. Phillips M, Robinowitz M, Higgins JR, Boran KJ, Reed T, Virmani R. Sudden cardiac death in Air Force recruits. A 20-year review. JAMA. 1986;256(19):2696–9.

    Article  CAS  PubMed  Google Scholar 

  41. Maron BJ, Udelson JE, Bonow RO, Nishimura RA, Ackerman MJ, Estes NAM 3rd, 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(21):2362–71.

    Article  PubMed  Google Scholar 

  42. Pelliccia A, Solberg EE, Papadakis M, Adami PE, Biffi A, Caselli S, et al. 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). Eur Heart J. 2019;40(1):19–33.

    Article  PubMed  Google Scholar 

  43. Mewton N, Dernis A, Bresson D, Zouaghi O, Croisille P, Flocard E, et al. Myocardial biomarkers and delayed enhanced cardiac magnetic resonance relationship in clinically suspected myocarditis and insight on clinical outcome. J Cardiovasc Med (Hagerstown). 2015;16(10):696–703.

    Article  CAS  Google Scholar 

  44. van de Schoor FR, Aengevaeren VL, Hopman MT, Oxborough DL, George KP, Thompson PD, et al. Myocardial fibrosis in athletes. Mayo Clin Proc. 2016;91(11):1617–31.

    Article  PubMed  Google Scholar 

  45. Breuckmann F, Mohlenkamp S, Nassenstein K, Lehmann N, Ladd S, Schmermund A, et al. Myocardial late gadolinium enhancement: prevalence, pattern, and prognostic relevance in marathon runners. Radiology. 2009;251(1):50–7.

    Article  PubMed  Google Scholar 

  46. La Gerche A, Burns AT, Mooney DJ, Inder WJ, Taylor AJ, Bogaert J, et al. Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J. 2012;33(8):998–1006.

    Article  PubMed  CAS  Google Scholar 

  47. Wilson M, O’Hanlon R, Prasad S, Deighan A, Macmillan P, Oxborough D, et al. Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol (1985). 2011;110(6):1622–6.

    Article  CAS  Google Scholar 

  48. Kwong RY, Chan AK, Brown KA, Chan CW, Reynolds HG, Tsang S, et al. Impact of unrecognized myocardial scar detected by cardiac magnetic resonance imaging on event-free survival in patients presenting with signs or symptoms of coronary artery disease. Circulation. 2006;113(23):2733–43.

    Article  PubMed  Google Scholar 

  49. Borjesson M, Dellborg M, Niebauer J, LaGerche A, Schmied C, Solberg EE, et al. Recommendations for participation in leisure time or competitive sports in athletes-patients with coronary artery disease: a position statement from the Sports Cardiology Section of the European Association of Preventive Cardiology (EAPC). Eur Heart J. 2019;40(1):13–8.

    Article  PubMed  Google Scholar 

  50. Authors/Task Force members, Elliott PM, Anastasakis A, Borger MA, Borggrefe M, Cecchi F, et al. 2014 ESC Guidelines on diagnosis and management of hypertrophic cardiomyopathy: the Task Force for the Diagnosis and Management of Hypertrophic Cardiomyopathy of the European Society of Cardiology (ESC). Eur Heart J. 2014;35(39):2733–79.

    Article  Google Scholar 

  51. Chan RH, Maron BJ, Olivotto I, Pencina MJ, Assenza GE, Haas T, et al. Prognostic value of quantitative contrast-enhanced cardiovascular magnetic resonance for the evaluation of sudden death risk in patients with hypertrophic cardiomyopathy. Circulation. 2014;130(6):484–95.

    Article  PubMed  Google Scholar 

  52. Rowin EJ, Maron MS. The role of cardiac MRI in the diagnosis and risk stratification of hypertrophic cardiomyopathy. Arrhythm Electrophysiol Rev. 2016;5(3):197–202.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Schnell F, Claessen G, La Gerche A, Bogaert J, Lentz PA, Claus P, et al. Subepicardial delayed gadolinium enhancement in asymptomatic athletes: let sleeping dogs lie? Br J Sports Med. 2016;50(2):111–7.

    Article  PubMed  Google Scholar 

  54. Zorzi A, Perazzolo Marra M, Rigato I, De Lazzari M, Susana A, Niero A, et al. Nonischemic left ventricular scar as a substrate of life-threatening ventricular arrhythmias and sudden cardiac death in competitive athletes. Circ Arrhythm Electrophysiol. 2016;9(7):e004229.

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to François Carré .

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1.1 Questions

  1. 1.

    Regarding different diagnostic tools of myocarditis in athletes, which of the following statements is correct?

    1. (a)

      A slight increase of troponin after intense exercise is always pathological.

    2. (b)

      Pathological ECG changes are always present in myocarditis.

    3. (c)

      Regional wall motion abnormalities on imaging techniques are always present in myocarditis.

    4. (d)

      Late gadolinium enhancement is always present in myocarditis.

    5. (e)

      None of the answers is correct.

  2. 2.

    Which of the following statements are correct? Clearance of athletes regarding competitive sports practice after a myocarditis is possible:

    1. (a)

      If the athlete is asymptomatic.

    2. (b)

      If serum markers of myocardial injury, inflammation, and heart failure have normalized.

    3. (c)

      If LV systolic function has returned to the normal range.

    4. (d)

      If no significant arrhythmia occurs on a 24-h ECG monitoring and exercise test.

    5. (e)

      If there is no more LGE on control CMR.

1.2 Answers

  1. 1.

    (e)

    The diagnosis of myocarditis is difficult. Indeed, except endomyocardial biopsy, none of the diagnostic tools that are at our disposal are specific nor sensitive.

    • Troponin can increase slightly after endurance exercise. Therefore, it is necessary to take previous physical exercise into account when a cardiac emergency is suspected.

    • ECG abnormalities are only present in less than 50% of patients with suspected myocarditis.

    • Regional wall motion abnormalities can be present, and LV global systolic function can range from normal to severely altered, but this is also not always the case.

    • A certain number of patients with biopsy proven myocarditis do not show LGE.

  2. 2.

    (a–d)

    The clinical significance of persistent LGE in an asymptomatic athlete with clinically healed myocarditis is unknown, however, myocardial scar is a potential source of ventricular tachyarrhythmias. At present, it seems reasonable for these athletes to resume training and participate in competitive sport if LV function is preserved and in the absence of frequent or complex repetitive forms of ventricular or supraventricular arrhythmias during maximal exercise and on 24-h ECG monitoring (including a session of training or competition). Asymptomatic athletes with LGE, however, should remain under annual clinical surveillance.

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Schnell, F., Carré, F. (2020). Specific Cardiovascular Diseases and Competitive Sports Participation: Myocarditis and Myocardial Fibrosis. In: Pressler, A., Niebauer, J. (eds) Textbook of Sports and Exercise Cardiology. Springer, Cham. https://doi.org/10.1007/978-3-030-35374-2_19

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