Athletic Training and Arrhythmogenic Right Ventricular Cardiomyopathy

Sara Alcobia Coelho; Filipe Silva; Joana Silva; Natália António

doi:10.1055/a-0750-5848

International Journal of Sports Medicine, Table of Contents

Int J Sports Med 2019; 40(05): 295-304
DOI: 10.1055/a-0750-5848

Review

Athletic Training and Arrhythmogenic Right Ventricular Cardiomyopathy

Sara Alcobia Coelho

¹ACeS Baixo Mondego, USF Mondego, Coimbra, Portugal

²Faculty of Medicine, University of Coimbra, Coimbra, Portugal

,

Filipe Silva

²Faculty of Medicine, University of Coimbra, Coimbra, Portugal

,

Joana Silva

¹ACeS Baixo Mondego, USF Mondego, Coimbra, Portugal

²Faculty of Medicine, University of Coimbra, Coimbra, Portugal

,

Natália António

²Faculty of Medicine, University of Coimbra, Coimbra, Portugal

³Cardiology Department, Coimbra Hospital and Universitary Centre, Coimbra, Portugal

› Author Affiliations

Abstract

Arrhythmogenic right ventricular cardiomyopathy (ARVC) is an inherited cardiomyopathy characterized by ventricular arrhythmias and sudden death in the young and in competitive athletes. The deleterious role of exercise in the natural history of ARVC is clear. Even in the absence of a demonstrated arrhythmogenic substrate, family history or mutations of ARVC, intense physical exercise may in some individuals lead to the development of right ventricular dysfunction and arrhythmogenicity. This led to question the benignity of some adaptive features of the athlete's heart. In fact, there is an overlap between typical aspects of the athlete's heart and pathological changes described in ARVC, being challenging to distinguish the two conditions. The aim of this review is to highlight the aspects that help to distinguish between athlete's heart and ARVC, to review the major findings on exams helping in the differential diagnosis and to determine the implications on eligibility for leisure and competitive sports.

Key words

arrhythmogenic right ventricular dysplasia - athlete’s heart - sudden death - exercise

Full Text

References

References
1 Basso C, Corrado D, Thiene G. Arrhythmogenic right ventricular cardiomyopathy in athletes: Diagnosis, management, and recommendations for sport activity. Cardiol Clin 2007; 25: 415-422
2 Bauce B, Frigo G, Benini G, Michieli P, Basso C, Folino AF, Rigato I, Mazzotti E, Daliento L, Thiene G, Nava A. Differences and similarities between arrhythmogenic right ventricular cardiomyopathy and athlete’s heart adaptations. Br J Sports Med 2010; 44: 148-154
3 Bhella PS, Kelly JP, Peshock R, Levine BD. Delayed enhancement of the intraventricular septum following an extraordinary endurance exercise. BMJ Case Rep 2010 pii: bcr0620103096
4 Calore C, Zorzi A, Sheikh N, Nese A, Facci M, Malhotra A, Zaidi A, Schiavon M, Pelliccia A, Sharma S, Corrado D. Electrocardiographic anterior T-wave inversion in athletes of different ethnicities: Differential diagnosis between athlete’s heart and cardiomyopathy. Eur Heart J 2016; 37: 2515-2527
5 Corrado D, Basso C, Leoni L, Tokajuk B, Bauce B, Frigo G, Tarantini G, Napodano M, Turrini P, Ramondo A, Daliento L, Nava A, Buja G, Iliceto S, Thiene G. Three-dimensional electroanatomic voltage mapping increases accuracy of diagnosing arrhythmogenic right ventricular cardiomyopathy/dysplasia. Circulation. 2005; 111: 3042-3050
6 Corrado D, Basso C, Rizzoli G, Schiavon M, Thiene G. Does sports activity enhance the risk of sudden death in adolescents and young adults?. J Am Coll Cardiol 2003; 42: 1959-1963
7 Corrado D, Link MS, Calkins H. Arrhythmogenic right ventricular cardiomyopathy. N Engl J Med 2017; 376: 1489-1490
8 Corrado D, Wichter T, Link MS, Hauer R, Marchlinski F, Anastasakis A, Bauce B, Basso C, Brunckhorst C, Tsatsopoulou A, Tandri H, Paul M, Schmied C, Pelliccia A, Duru F, Protonotarios N, Estes 3rd NA, McKenna WJ, Thiene G, Marcus FI, Calkins H. Treatment of arrhythmogenic right ventricular cardiomyopathy/dysplasia: An international task force consensus statement. Eur Heart J 2015; 36: 3227-3237
9 D’Ascenzi F, Pisicchio C, Caselli S, Di Paolo FM, Spataro A, Pelliccia ARV. Remodeling in Olympic Athletes. JACC Cardiovasc Imaging 2017; 10: 385-393
10 Denis A, Sacher F, Derval N, Lim HS, Cochet H, Shah AJ, Daly M, Pillois X, Ramoul K, Komatsu Y, Zemmoura A, Amraoui S, Ritter P, Ploux S, Bordachar P, Hocini M, Jaïs P, Haïssaguerre M. Diagnostic value of isoproterenol testing in arrhythmogenic right ventricular cardiomyopathy. Circ Arrhythmia Electrophysiol 2014; 7: 590-597
11 Denis A, Sacher F, Derval N, Martin R, Lim HS, Pambrun T, Massoullie G, Duchateau J, Cochet H, Pillois X, Cheniti G, Frontera A, Takigawa M, Vlachos K, Martin C, Kitamura T, Hocini M, Douard H, Jaïs P, Haïssaguerre M. Arrhythmogenic response to isoproterenol testing vs. exercise testing in arrhythmogenic right ventricular cardiomyopathy patients. Europace 2018; 20: f30-f36
12 Finocchiaro G, Papadakis M, Dhutia H, Zaidi A, Malhotra A, Fabi E, Cappelletto C, Brook J, Papatheodorou E, Ensam B, Miles CJ, Bastiaenen R, Attard V, Homfray T, Sharma R, Tome M, Carr-White G, Merlo M, Behr ER, Sinagra G, Sharma S. Electrocardiographic differentiation between ‘benign T-wave inversion’ and arrhythmogenic right ventricular cardiomyopathy. Europace 2019; 21: 332-338
13 Galderisi M, Cardim N, D'Andrea A, Bruder O, Cosyns B, Davin L, Donal E, Edvardsen T, Freitas A, Habib G, Kitsiou A, Plein S, Petersen SE, Popescu BA, Schroeder S, Burgstahler C, Lancellotti P. The multi-modality cardiac imaging approach to the Athlete’s heart: An expert consensus of the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 2015; 16: 353
14 Hariharan V, Asimaki A, Michaelson JE, Plovie E, MacRae CA, Saffitz JE, Huang H. Arrhythmogenic right ventricular cardiomyopathy mutations alter shear response without changes in cell-cell adhesion. Cardiovasc Res 2014; 104: 280-289
15 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 Update. Int J Sports Med 2017; 38: 1126-1131
16 Haugaa KH, Basso C, Badano LP, Bucciarelli-Ducci C, Cardim N, Gaemperli O, Galderisi M, Habib G, Knuuti J, Lancellotti P, McKenna W, Neglia D, Popescu BA, Edvardsen T. EACVI Scientific Documents Committee, EACVI Board members and external reviewers; EACVI Scientific Documents Committee, EACVI Board members and external reviewers . Comprehensive multi-modality imaging approach in arrhythmogenic cardiomyopathy-an expert consensus document of the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 2017; 18: 237-253
17 Heidbüchel H, Hoogsteen J, Fagard R, Vanhees L, Ector H, Willems R, Van Lierde J. High prevalence of right ventricular involvement in endurance athletes with ventricular arrhythmias: Role of an electrophysiologic study in risk stratification. Eur Heart J 2003; 24: 1473-1480
18 Heidbüchel H, La Gerche A. The right heart in athletes: Evidence for exercise-induced arrhythmogenic right ventricular cardiomyopathy. Herzschrittmacherther Elektrophysiol 2012; 23: 82-86
19 Inciardi RM, Rossi A, Pesarini G, Clemenza F, Vassanelli C. Cardiovascular imaging in arrhythmogenic right ventricular dysplasia/cardiomyopathy. Int J Cardiol 2015; 190: 329-331
20 James CA, Bhonsale A, Tichnell C, Murray B, Russell SD, Tandri H, Tedford RJ, Judge DP, Calkins H. Exercise increases age-related penetrance and arrhythmic risk in arrhythmogenic right ventricular dysplasia/cardiomyopathy-associated desmosomal mutation carriers. J Am Coll Cardiol 2013; 62: 1290-1297
21 Khan AA, Safi L, Wood M. Cardiac Imaging In Athletes. Methodist Debakey Cardiovasc J 2016; 12: 86-92
22 King G, Wood MJ. The right ventricle of the elite high end endurance athlete cannot be underestimated. J Am Soc Echocardiogr 2012; 25: 272-273
23 Kirchhof P, Fabritz L, Zwiener M, Witt H, Schäfers M, Zellerhoff S, Paul M, Athai T, Hiller KH, Baba HA, Breithardt G, Ruiz P, Wichter T, Levkau B. Age- and training-dependent development of arrhythmogenic right ventricular cardiomyopathy in heterozygous plakoglobin-deficient mice. Circulation 2006; 114: 1799-1806
24 Kjaergaard J. Assessment of right ventricular systolic function by tissue Doppler echocardiography. Dan Med J 2012; 59: B4409
25 Kushwaha SS, Grupper A. Suspected ARVC in the athlete: Do T-wave findings really help in diagnosis?. J Am Coll Cardiol 2015; 65: 2712-2713
26 La Gerche A. Defining the interaction between exercise and arrhythmogenic right ventricular cardiomyopathy. Eur J Heart Fail 2015; 17: 128-131
27 La Gerche A, Burns AT, D’Hooge J, MacIsaac AI, Heidbüchel H, Prior DL. Exercise strain rate imaging demonstrates normal right ventricular contractile reserve and clarifies ambiguous resting measures in endurance athletes. J Am Soc Echocardiogr 2012; 25: 253-262
28 La Gerche A, Burns AT, Mooney DJ, Inder WJ, Taylor AJ, Bogaert J, Macisaac AI, Heidbüchel H, Prior DL. Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J 2012; 33: 998-1006
29 La Gerche A, Heidbüchel H, Burns AT, Mooney DJ, Taylor AJ, Pfluger HB, Inder WJ, Macisaac AI, Prior DL. Disproportionate exercise load and remodeling of the athlete’s right ventricle. Med Sci Sports Exerc 2011; 43: 974-981
30 La Gerche A, Robberecht C, Kuiperi C, Nuyens D, Willems R, de Ravel T, Matthijs G, Heidbüchel H. Lower than expected desmosomal gene mutation prevalence in endurance athletes with complex ventricular arrhythmias of right ventricular origin. Heart 2010; 96: 1268-1274
31 La Gerche A, Taylor AJ, Prior DL. Athlete’s heart: The Potential for multimodality imaging to address the critical remaining questions. JACC Cardiovasc Imaging 2009; 2: 350-363
32 Malhotra A, Dhutia H, Gati S, Yeo TJ, Dores H, Bastiaenen R, Narain R, Merghani A, Finocchiaro G, Sheikh N, Steriotis A, Zaidi A, Millar L, Behr E, Tome M, Papadakis M, Sharma S. Anterior T-wave inversion in young white athletes and nonathletes: prevalence and significance. J Am Coll Cardiol 2017; 69: 1-9
33 Marcus FI, Edson S, Towbin JA. Genetics of arrhythmogenic right ventricular cardiomyopathy: A practical guide for physicians. J Am Coll Cardiol 2013; 61: 1945-1948
34 Marcus FI, McKenna WJ, Sherrill D, Basso C, Bauce B, Bluemke DA, Calkins H, Corrado D, Cox MG, Daubert JP, Fontaine G, Gear K, Hauer R, Nava A, Picard MH, Protonotarios N, Saffitz JE, Sanborn DM, Steinberg JS, Tandri H, Thiene G, Towbin JA, Tsatsopoulou A, Wichter T, Zareba W. Diagnosis of arrhythmogenic right ventricular cardiomyopathy/Dysplasia: Proposed modification of the task force criteria. Circulation 2010; 121: 1533-1541
35 Marcus FI, Zareba W, Calkins H, Towbin JA, Basso C, Bluemke DA, Estes 3rd NA, Picard MH, Sanborn D, Thiene G, Wichter T, Cannom D, Wilber DJ, Scheinman M, Duff H, Daubert J, Talajic M, Krahn A, Sweeney M, Garan H, Sakaguchi S, Lerman BB, Kerr C, Kron J, Steinberg JS, Sherrill D, Gear K, Brown M, Severski P, Polonsky S, McNitt S. Arrhythmogenic right ventricular cardiomyopathy/dysplasia clinical presentation and diagnostic evaluation: Results from the North American Multidisciplinary Study. Heart Rhythm 2009; 6: 984-992
36 Maron BJ, Pelliccia A. The heart of trained athletes: Cardiac remodeling and the risks of sports, including sudden death. Circulation 2006; 114: 1633-1644
37 Maron BJ, Udelson JE, Bonow RO, Nishimura RA, Ackerman MJ, Estes NAM, Cooper LT, Link MS, Maron MS. Eligibility and Disqualification Recommendations for Competitive Athletes with Cardiovascular Abnormalities: Task Force 3: Hypertrophic Cardiomyopathy, Arrhythmogenic Right Ventricular Cardiomyopathy and Other Cardiomyopathies, and Myocarditis. J Am Coll Cardiol 2015; 66: 2362-2371
38 Marra MP, Leoni L, Bauce B, Corbetti F, Zorzi A, Migliore F, Silvano M, Rigato I, Tona F, Tarantini G, Cacciavillani L, Basso C, Buja G, Thiene G, Iliceto S, Corrado D. Imaging study of ventricular scar in arrhythmogenic right ventricular cardiomyopathy: comparison of 3D standard electroanatomical voltage mapping and contrast-enhanced cardiac magnetic resonance. Circ Arrhythm Electrophysiol 2012; 5: 91-100
39 McKenna WJ, Thiene G, Nava A, Fontaliran F, Blomstrom-Lundqvist C, Fontaine G, Camerini F. Diagnosis of arrhythmogenic right ventricular dysplasia/cardiomyopathy. Task Force of the Working Group Myocardial and Pericardial Disease of the European Society of Cardiology and of the Scientific Council on Cardiomyopathies of the International Society and Federation of Cardiology. Br Heart J 1994; 71: 215-218
40 Pelliccia A, Fagard R, Bjørnstad HH, Anastassakis A, Arbustini E, Assanelli D, Biffi A, Borjesson M, Carrè F, Corrado D, Delise P, Dorwarth U, Hirth A, Heidbuchel H, Hoffmann E, Mellwig KP, Panhuyzen-Goedkoop N, Pisani A, Solberg EE, van-Buuren F, Vanhees L, Blomstrom-Lundqvist C, Deligiannis A, Dugmore D, Glikson M, Hoff PI, Hoffmann A, Hoffmann E, Horstkotte D, Nordrehaug JE, Oudhof J, McKenna WJ, Penco M, Priori S, Reybrouck T, Senden J, Spataro A, Thiene G. Study Group of Sports Cardiology of the Working Group of Cardiac Rehabilitation and Exercise Physiology; Working Group of Myocardial and Pericardial Diseases of the European Society of Cardiology . Recommendations for competitive sports participation in athletes with cardiovascular disease: a consensus document from the Study Group of Sports Cardiology of the Working Group of Cardiac Rehabilitation and Exercise Physiology and the Working Group of Myocardial and Pericardial Diseases of the European Society of Cardiology. Eur Heart J 2005; 26: 1422-1445
41 Perrin MJ, Angaran P, Laksman Z, Zhang H, Porepa LF, Rutberg J, James C, Krahn AD, Judge DP, Calkins H, Gollob MH. Exercise testing in asymptomatic gene carriers exposes a latent electrical substrate of arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol 2013; 62: 1772-1779
42 Platonov PG, Calkins H, Hauer RN, Corrado D, Svendsen JH, Wichter T, Biernacka EK, Saguner AM, Te Riele AS, Zareba W. High interobserver variability in the assessment of epsilon waves: Implications for diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia. Heart Rhythm 2016; 13: 208-216
43 Poh KK, Ton-Nu TT, Neilan TG, Tournoux FB, Picard MH, Wood MJ. Myocardial adaptation and efficiency in response to intensive physical training in elite speedskaters. Int J Cardiol 2008; 126: 346-351
44 Prakken NH, Velthuis BK, Bosker AC, Mosterd A, Teske AJ, Mali WP, Cramer MJ. Relationship of ventricular and atrial dilatation to valvular function in endurance athletes. Br J Sports Med 2011; 45: 178-184
45 Qasem M, Utomi V, George K, Somauroo J, Zaidi A, Forsythe L. A meta-analysis for the echocardiographic assessment of right ventricular structure and function in ARVC: a Study by the Research and Audit Committee of the British Society of Echocardiography. Echo Res Pract 2016; 3: 95-104
46 Ruwald AC, Marcus F, Estes 3rd NA, Link M, McNitt S, Polonsky B, Calkins H, Towbin JA, Moss AJ, Zareba W. Association of competitive and recreational sport participation with cardiac events in patients with arrhythmogenic right ventricular cardiomyopathy: Results from the North American multidisciplinary study of arrhythmogenic right ventricular cardiomyopath. Eur Heart J 2015; 36: 1735-1743
47 Saberniak J, Hasselberg NE, Borgquist R, Platonov PG, Sarvari SI, Smith HJ, Ribe M, Holst AG, Edvardsen T, Haugaa KH. Vigorous physical activity impairs myocardial function in patients with arrhythmogenic right ventricular cardiomyopathy and in mutation positive family members. Eur J Heart Fail 2014; 16: 1337-1344
48 Schnell F, Riding N, O'Hanlon R, Axel Lentz P, Donal E, Kervio G, Matelot D, Leurent G, Doutreleau S, Chevalier L, Guerard S, Wilson MG, Carré F. Recognition and significance of pathological T-wave inversions in athletes. Circulation 2014; 131: 165-173
49 Sen-Chowdhry S, Lowe MD, Sporton SC, McKenna WJ. Arrhythmogenic right ventricular cardiomyopathy: Clinical presentation, diagnosis, and management. Am J Med 2004; 117: 685-695
50 Sen-Chowdhry S, Syrris P, Ward D, Asimaki A, Sevdalis E, McKenna WJ. Clinical and genetic characterization of families with arrhythmogenic right ventricular dysplasia/cardiomyopathy provides novel insights into patterns of disease expression. Circulation 2007; 115: 1710-1720
51 Sharma S, Zaidi A. Exercise-induced arrhythmogenic right ventricular cardiomyopathy: Fact or fallacy?. Eur Heart J 2012; 33: 938-940
52 Tahir E, Starekova J, Muellerleile K, von Stritzky A, Münch J, Avanesov M, Weinrich JM, Stehning C, Bohnen S, Radunski UK, Freiwald E, Blankenberg S, Adam G, Pressler A, Patten M, Lund GK. Myocardial fibrosis in competitive triathletes detected by contrast-enhanced CMR correlates with exercise-induced hypertension and competition history. JACC Cardiovasc Imaging 2018; 11: 1260-1270
53 Tandri H, Bomma C, Calkins H, Bluemke DA. Magnetic resonance and computed tomography imaging of arrhythmogenic right ventricular dysplasia. J Magn Reson Imaging 2004; 19: 848-858
54 Teske AJ, Cox MG, De Boeck BW, Doevendans PA, Hauer RN, Cramer MJ. Echocardiographic tissue deformation imaging quantifies abnormal regional right ventricular function in arrhythmogenic right ventricular dysplasia/cardiomyopathy. J Am Soc Echocardiogr 2009; 22: 920-927
55 Vitarelli A, Cortes Morichetti M, Capotosto L, De Cicco V, Ricci S, Caranci F, Vitarelli M. Utility of strain echocardiography at rest and after stress testing in arrhythmogenic right ventricular dysplasia. Am J Cardiol 2013; 111: 1344-1350
56 Wilson M, O'Hanlon R, Prasad S, Deighan A, Macmillan P, Oxborough D, Godfrey R, Smith G, Maceira A, Sharma S, George K, Whyte G. Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol 2011; 110: 1622-1626
57 Yoerger DM, Marcus F, Sherrill D, Calkins H, Towbin JA, Zareba W, Picard MH. Multidisciplinary Study of Right Ventricular Dysplasia Investigators . Echocardiographic findings in patients meeting task force criteria for arrhythmogenic right ventricular dysplasia: New insights from the multidisciplinary study of right ventricular dysplasia. J Am Coll Cardiol 2005; 45: 860-865
58 Zaidi A, Ghani S, Sheikh N, Gati S, Bastiaenen R, Madden B, Papadakis M, Raju H, Reed M, Sharma R, Behr ER, Sharma S. Clinical significance of electrocardiographic right ventricular hypertrophy in athletes: Comparison with arrhythmogenic right ventricular cardiomyopathy and pulmonary hypertension. Eur Heart J 2013; 34: 3649-3656
59 Zaidi A, Sheikh N, Jongman JK, Gati S, Panoulas VF, Carr-White G, Papadakis M, Sharma R, Behr ER, Sharma S. Clinical differentiation between physiological remodeling and arrhythmogenic right ventricular cardiomyopathy in athletes with marked electrocardiographic repolarization anomalies. J Am Coll Cardiol 2015; 65: 2702-2711
60 Zorzi A, ElMaghawry M, Rigato I, Cardoso Bianchini F, Crespi Ponta G, Michieli P, Migliore F, Perazzolo Marra M, Bauce B, Basso C, Schiavon M, Thiene G, Iliceto S, Corrado D. Exercise-induced normalization of right precordial negative T waves in arrhythmogenic right ventricular cardiomyopathy. Am J Cardiol 2013; 112: 411-415