Right heart structural and functional remodeling in athletes

Echocardiography

Volumn 32, Issue S1, 2015, Pages 11-22

  D'Andrea, Antonello ^a   La Gerche, Andrè ^b   Golia, Enrica ^a   Teske, Arco J ^c   Bossone, Eduardo ^d   Russo, Maria Giovanna ^a   Calabrò, Raffaele ^a   Baggish, Aaron L ^e  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d IRCCS POLICLINICO SAN DONATO   (Italy)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

athlete's heart; echocardiography; exercise; right ventricle; strain imaging; tissue Doppler

Indexed keywords

ADAPTATION; ARTICLE; ATHLETE; COLOR ULTRASOUND FLOWMETRY; DIASTOLE; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAM; ENDURANCE TRAINING; HEART FUNCTION; HEART RIGHT BUNDLE BRANCH BLOCK; HEART RIGHT VENTRICLE; HEART RIGHT VENTRICLE DYSPLASIA; HEART RIGHT VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MORPHOLOGY; PRIORITY JOURNAL; SYSTOLE; ANATOMY AND HISTOLOGY; DOPPLER ECHOCARDIOGRAPHY; ENDURANCE; FEMALE; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; HEART VENTRICLE; MALE; PHYSICAL EDUCATION; PHYSIOLOGY; PROCEDURES; SPORT; STATISTICS AND NUMERICAL DATA;

ADAPTATION, PHYSIOLOGICAL; ATHLETES; ECHOCARDIOGRAPHY, DOPPLER, COLOR; FEMALE; HEART VENTRICLES; HUMANS; MALE; PHYSICAL EDUCATION AND TRAINING; PHYSICAL ENDURANCE; SPORTS; STROKE VOLUME; VENTRICULAR FUNCTION, LEFT; VENTRICULAR FUNCTION, RIGHT; VENTRICULAR REMODELING;

EID: 84921686196     PISSN: 07422822     EISSN: 15408175     Source Type: Journal    
DOI: 10.1111/echo.12226     Document Type: Article

References (81)

1. Morganroth J, Maron BJ, Henry WL, et al. Comparative left ventricular dimensions in trained athletes. Ann Intern Med 1975; 82: 521-524.
2. Rost R, Hollmann W,: Athlete's heart. A review of its historical assessment and new aspects. Int J Sports Med 1983; 4: 147-165.
3. D'Andrea A, Limongelli G, Caso P, et al. Association between left ventricular structure and cardiac performance during effort in two morphological forms of athlete's heart. Int J Cardiol 2002; 86: 177-184.
4. George KP, Warburton DE, Oxborough D, et al. Upper limits of physiological cardiac adaptation in ultramarathon runners. J Am Coll Cardiol 2011; 57: 754-755.
5. D'Andrea A, Galderisi M, Sciomer S, et al. Echocardiographic evaluation of the athlete's heart: From morphological adaptations to myocardial function. G Ital Cardiol (Rome) 2009; 10: 533-544.
6. Maron BJ,: Structural features of the athlete heart as defined by echocardiography. J Am Coll Cardiol 1986; 7: 190-203.
7. Pelliccia A, Maron BJ, Spataro A, et al. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl J Med 1991; 324: 295-301.
8. Spirito P, Pelliccia A, Proschan MA, et al. Morphology of the "athlete's heart" assessed by echocardiography in 947 elites athletes rapresenting 27 sports. Am J Cardiol 1994; 74: 802-806.
9. Pelliccia A, Culasso F, Di Paolo F, et al. Physiologic left ventricular cavity dilation in elite athletes. Ann Intern Med 1999; 130: 23-31.
10. Fisman EZ, Embon P, Pines A, et al. Comparison of left ventricular function using isometric exercise Doppler echocardiography in competitive runners and weightlifters versus sedentary individuals. Am J Cardiol 1997; 79: 355-359.
11. Pluim BM, Zwinderman AH, van der Laarse A, et al. The athlete's heart. A meta-analysis of cardiac structure and function. Circulation 2000; 101: 336-342.
12. Pelliccia A, Maron BJ, De Luca R, et al. Remodeling of left ventricular hypertrophy in elite athletes after long-term deconditioning. Circulation 2002; 105: 944-949.
13. Sciomer S, Vitarelli A, Penco M, et al. Anatomico-functional changes in the right ventricle of the athlete. Cardiologia 1998; 43: 1215-1220.
14. Douglas PS, O'Toole ML, Hiller WDB, et al. Different effects of prolonged exercise on the right and left ventricles. J Am Coll Cardiol 1990; 15: 64-69.
15. Rudski LG, Lai WW, Afilalo J, et al. Guidelines for the echocardiographic assessment of the right heart in adults: A report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 2010; 23: 685-713.
16. Corrado D, Pelliccia A, Heidbuchel H, et al. Recommendations for interpretation of 12-lead electrocardiogram in the athlete. Eur Heart J 2010; 31: 243-259.
17. Uberoi A, Stein R, Perez MV, et al. Interpretation of the electrocardiogram of young athletes. Circulation 2011; 124: 746-757.
18. Baggish AL, Wood MJ,: Athlete's heart and cardiovascular care of the athlete: Scientific and clinical update. Circulation 2011; 123: 2723-2735.
19. Noseworthy PA, Weiner R, Kim J, et al. Early repolarization pattern in competitive athletes: Clinical correlates and the effects of exercise training. Circ Arrhythm Electrophysiol 2011; 4: 432-440.
20. Weiner RB, Hutter AM, Wang F, et al. Performance of the 2010 European Society of cardiology criteria for ECG interpretation in athletes. Heart 2011; 97: 1573-1577.
21. Corrado D, Basso C, Buja G, et al. Right bundle branch block, right precordial st-segment elevation, and sudden death in young people. Circulation 2001; 103: 710-717.
22. Nakamoto K,: Electrocardiograms of 25 marathon runners before and after 100 meter dash. Jpn Circ J 1969; 33: 105-128.
23. Venerando A, Rulli V,: Frequency morphology and meaning of the electrocardiographic anomalies found in olympic marathon runners and walkers. J Sports Med Phys Fitness 1964; 50: 135-141.
24. Pelliccia A, Culasso F, Di Paolo FM, et al. Prevalence of abnormal electrocardiograms in a large, unselected population undergoing pre-participation cardiovascular screening. Eur Heart J 2007; 28: 2006-2010.
25. Pelliccia A, Maron BJ, Culasso F, et al. Clinical significance of abnormal electrocardiographic patterns in trained athletes. Circulation 2000; 102: 278-284.
26. Baggish AL, Hutter AM Jr, Wang F, et al. Cardiovascular screening in college athletes with and without electrocardiography: A cross-sectional study. Ann Intern Med 2010; 152: 269-275.
27. Kim JH, Noseworthy PA, McCarty D, et al. Significance of electrocardiographic right bundle branch block in trained athletes. Am J Cardiol 2011; 107: 1083-1089.
28. Foale RA, Nihoyannopoulos P, Mc Kenna W,: Echocardiographic measurement of normal adult right ventricle. Br Heart J 1986; 56: 33-44.
29. Kaul S, Tei C, Hopkins JM, et al. Assessment of right ventricular function using two-dimensonal echocardiography. Am Heart J 1984; 128: 301-307.
30. Hauser AM, Dressendorfer RH, Vos M, et al. Symmetric cardiac enlargement in highly trained endurance athletes: A two-dimensional echocardiographic study. Am Heart J 1985; 109: 1038-1044.
31. Henriksen E, Landelius J, Kangro T, et al. An echocardiographic study of right and left ventricular adaptation to physical exercise in elite female orienteers. Eur Heart J 1999; 20: 309-316.
32. Baggish AL, Yared K, Weiner RB, et al. Differences in cardiac parameters among elite rowers and subelite rowers. Med Sci Sports Exerc 2010; 42: 1215-1220.
33. D'Andrea A, Caso P, Sarubbi B, et al. Right ventricular myocardial adaptation to different training protocols in top-level athletes. Echocardiography 2003; 20: 329-336.
34. Raymond RJ, Hinderliter AL, Willis PW, et al. Echocardiographic predictors of adverse outcomes in primary pulmonary hypertension. J Am Coll Cardiol 2002; 39: 1214-1219.
35. Zeppilli P, Vannicelli R, Santini C, et al. Echocardiographic size of conductance vessels in athletes and sedentary people. Int J Sports Med 1995; 16: 38-44.
36. Goldhammer E, Mesnick N, Abinader EG, et al. Dilated inferior vena cava: A common echocardiographic finding in highly trained elite athletes. J Am Soc Echocardiogr 1999; 12: 988-993.
37. Oxboruogh D, Sharma S, Shave R, et al. The right ventricle of the endurance atlete: The relationship between morphology and deformation. J Am Soc Echocardiogr 2012; 25: 263-271.
38. Pollak SJ, McMillan SA, Knopff WD, et al. Cardiac evaluation of women distance runners by echocardiographic Doppler flow mapping. J Am Coll Cardiol 1988; 11: 89-93.
39. D'Andrea A, Naeije R, D'Alto M, et al. Range in pulmonary artery systolic pressure among highly trained athletes. Chest 2011; 139: 788-794.
40. La Gerche A, MacIsaac AI, Burns AT, et al. Pulmonary transit of agitated contrast is associated with enhanced pulmonary vascular reserve and right ventricular function during exercise. J Appl Physiol 2010; 109: 1307-1317.
41. Eldridge MW, Dempsey JA, Haverkamp HC, et al. J Appl Physiol 2004; 97: 797-805.
42. Stickland MK, Welsh RC, Haykowsky MJ, et al. Intra-pulmonary shunt and pulmonary gas exchange during exercise in humans. J Physiol 2004; 561: 321-329.
43. Sharma S, Zaidi A,: Exercise-induced arrhythmogenic right ventricular cardiomyopathy: Fact or fallacy? Eur Heart J 2012; 33: 938-940.
44. Shave R, Baggish A, George K, et al. Exercise-induced cardiac troponin elevation: Evidence, mechanisms, and implications. J Am Coll Cardiol 2010; 56: 169-176.
45. La Gerche A, Burns AT, Mooney DJ, et al. Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J, 2012; 33: 998-1006.
46. Heidbuchel H, Prior DL, Gerche AL,: Ventricular arrhythmias associated with long-term endurance sports: What is the evidence? Br J Sports Med 2012; 46 (Suppl 1): i44-i50.
47. Mont L,: Arrhythmias and sport practice. Heart 2010; 96: 398-405.
48. Shave R, George K, Whyte G, et al. Postexercise changes in left ventricular function: The evidence so far. Med Sci Sports Exerc, 2008; 40: 1393-1399.
49. La Gerche A, Connelly KA, Mooney DJ, et al. Biochemical and functional abnormalities of left and right ventricular function after ultra-endurance exercise. Heart, 2008; 94: 860-866.
50. Oxborough D, Shave R, Warburton D, et al. Dilatation and dysfunction of the right ventricle immediately after ultraendurance exercise: Exploratory insights from conventional two-dimensional and speckle tracking echocardiography. Circ Cardiovasc Imaging 2011; 4: 253-263.
51. Neilan TG, Januzzi JL, Lee-Lewandrowski E, et al. Myocardial injury and ventricular dysfunction related to training levels among nonelite participants in the Boston marathon. Circulation, 2006; 114: 2325-2333.
52. Neilan TG, Yoerger DM, Douglas PS, et al. Persistent and reversible cardiac dysfunction among amateur marathon runners. Eur Heart J, 2006; 27: 1079-1084.
53. La Gerche A, Jurcut R, Voigt JU,: Right ventricular function by strain echocardiography. Curr Opin Cardiol 2010; 22: 430-436.
54. Mousavi N, Czarnecki A, Kumar K, et al. Relation of biomarkers and cardiac magnetic resonance imaging after marathon running. Am J Cardiol 2009; 103: 1467-1472.
55. Trivax JE, Franklin BA, Goldstein JA, et al. Acute cardiac effects of marathon running. J Appl Physiol 2010; 108: 1148-1153.
56. La Gerche A, Heidbüchel H, Burns AT, et al. Disproportionate Exercise Load and Remodeling of the Athlete's Right Ventricle. Med Sci Sports Exerc, 2011; 43: 974-981.
57. Kovacs G, Berghold A, Scheidl S, et al. Pulmonary arterial pressure during rest and exercise in healthy subjects: A systematic review. Eur Respir J 2009; 34: 888-894.
58. Reeves JT, Groves BM, Cymerman A, et al. Operation Everest II: Cardiac filling pressures during cycle exercise at sea level. Respir Physiol, 1990; 80: 147-154.
59. Reeves JT, Dempsey JA, Grover RF,: Pulmonary circulation during exercise. In, Weir EK, Reeves JT, (eds): Pulmonary Vascular Physiology and Physiopathology, New York: Marcel Dekker, 1989, pp. 107-133.
60. La Gerche A, Burns AT, D'Hooge J, et al. 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 e1.
61. Pelliccia A, Maron BJ, Spataro A, et al. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl J Med 1991; 31: 295-301.
62. Teske AJ, Prakken NH, De Boeck BW, et al. Echocardiographic tissue deformation imaging of right ventricular systolic function in endurance athletes. Eur Heart J 2009; 30: 969-977.
63. Kasikcioglu E, Oflaz H, Akhan H, et al. Right ventricular myocardial performance index and exercise capacity in athletes. Heart Vessels 2005; 20: 147-152.
64. Prakken NH, Velthuis BK, Teske AJ, et al. Cardiac MRI reference values for athletes and nonathletes corrected for body surface area, training hours/week and sex. Eur J Cardiovasc Prev Rehabil 2010; 17: 198-203.
65. Kowalski M, Kukulski T, Jamal F, et al. Can natural strain and strain rate quantify regional myocardial deformation? A study in healthy subjects. Ultrasound Med Biol 2001; 27: 1087-1097.
66. Teske AJ, De Boeck BWL, Olimulder M, et al. Echocardiographic Assessment of Regional Right Ventricular Function: A Head-to-head Comparison Between 2-Dimensional and Tissue Doppler-derived Strain Analysis. J Am Soc Echocardiogr 2008; 21: 275-283.
67. Carlsson M, Ugander M, Heiberg E, et al. The quantitative relationship between longitudinal and radial function in left, right, and total heart pumping in humans. Am J Physiol Heart Circ Physiol 2007; 293: H636-H644.
68. Baggish AL, Wang F, Weiner RB, et al. Training-specific changes in cardiac structure and function: A prospective and longitudinal assessment of competitive athletes. J Appl Physiol 2008; 104: 1121-1128.
69. Caso P, D'Andrea A, Galderisi M, et al. Pulsed Doppler tissue imaging in endurance athletes: Relation between left ventricular preload and myocardial regional diastolic function. The American Journal of Cardiology 2000; 85: 1131-1136.
70. Erol MK, Karakelleoglu S,: Assessment of right heart function in the athlete's heart. Heart Vessels 2002; 16: 175-180.
71. Caso P, Galderisi M, D'Andrea A, et al. Analysis by Doppler tissue imaging of ventricular interaction in long-distance competitive swimmers. Am J Cardiol 2002; 90: 193-197.
72. Vitale G, Galderisi M, Colao A, et al. Circulating insulin-like growth factor-I levels are associated with increased biventricular contractility in top level rowers. Clin Endocrinol 2008; 69: 231-236.
73. Santamore WP, Dell'Italia LJ,: Ventricular interdependence: Significant left ventricular contributions to right ventricular systolic function. Progr Cardiovasc Dis 1998; 40: 289-308.
74. Teske Arco J, Prakken Niek H, De Boeck BW, et al. Effect of long term and intensive endurance training in athletes on the age related decline in left and right ventricular diastolic function as assessed by Doppler echocardiography. Am J Cardiol 2009; 104: 1145-1151.
75. Maron BJ, Pelliccia A,: The Heart of Trained Athletes: Cardiac Remodeling and the Risks of Sports. Including Sudden Death. Circulation 2006; 114: 1633-1644.
76. Marcus FI, McKenna WJ, Sherrill D, et al. Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia: Proposed modification of the task force criteria. Circulation 2010; 121: 1533-1541.
77. Severino S, Caso P, Cicala S, et al. Involvement of right ventricle in left ventricular hypertrophic cardiomyopathy: Analysis by pulsed tissue imaging. Eur J Echocardiogr 2000; 1: 281-288.
78. Vinereanu D, Florescu N, Schulthorpe N, et al. Differentiation between pathologic and physiologic left ventricular hypertrophy by tissue Doppler assessment of long-axis function in patients with hypertrophic cardiomyopathy or systemic hypertension and in athletes. Am J Cardiol 2001; 88: 53-58.
79. Cicala S, Galderisi M, Caso P, et al. Right ventricular diastolic dysfunction in arterial systemic hypertension:analysis by pulsed tissue Doppler. Eur J Echocardiogr 2002; 3: 135-142.
80. D'Andrea A, Caso P, Bossone E, et al. Right ventricular myocardial involvement in either physiological or pathological left ventricular hypertrophy: An ultrasound speckle- tracking two-dimensional strain analysis. Eur J Echocardiogr 2010; 11: 492-500.
81. Morner S, Lindqvist P, Waldenstrom A, et al. Right ventricular dysfunction in hypertrophic cardiomyopathy as evidenced by the myocardial performance index. Int J Cardiol 2008; 124: 57-63.