The endurance athletes heart: acute stress and chronic adaptation

The impact of endurance exercise training on the heart has received significant research and clinical attention for well over a century. Despite this, many issues remain controversial and clinical interpretation can be complex of biomarkers of cardiomyocyte insult. This review assesses the current state of knowledge related to two areas of research where problems with clinical decision making may arise: (1) the impact of chronic endurance exercise training on cardiac structure, function and electrical activity to the point where the athletic heart phenotype may be similar to the expression of some cardiac pathologies (a diagnostic dilemma referred to as the ‘grey-zone’) and (2) the impact of acute bouts of prolonged exercise on cardiac function and the presentation of biomarkers and cardiomyocyte insult in the circulatory system. The combination of acute endurance exercise stress on the heart and prolonged periods of training are considered together in the final section.

[1]  J. Mitchell,et al.  Classification of sports. , 1994, Medicine and science in sports and exercise.

[2]  N. Secher,et al.  β‐Adrenergic receptor desensitization in man: insight into post‐exercise attenuation of cardiac function , 2006, The Journal of physiology.

[3]  W. Roberts,et al.  Causes of sudden death in competitive athletes. , 1986, Journal of the American College of Cardiology.

[4]  G. Whyte,et al.  Myocardial fibrosis in an veteran endurance athlete , 2009, BMJ Case Reports.

[5]  K. George,et al.  Treat the patient not the blood test: the implications of an increase in cardiac troponin after prolonged endurance exercise , 2007, British Journal of Sports Medicine.

[6]  W. Mckenna,et al.  Electrocardiographic changes in 1000 highly trained junior elite athletes. , 1999, British journal of sports medicine.

[7]  G. Kervio,et al.  The prevalence, distribution, and clinical outcomes of electrocardiographic repolarization patterns in male athletes of African/Afro-Caribbean origin. , 2011, European heart journal.

[8]  K. Connelly,et al.  Biochemical and functional abnormalities of left and right ventricular function after ultra-endurance exercise , 2007, Heart.

[9]  B. Maron,et al.  Relation between training-induced left ventricular hypertrophy and risk for ventricular tachyarrhythmias in elite athletes. , 2008, The American journal of cardiology.

[10]  K. George,et al.  Exercise-induced cardiac troponin T release: a meta-analysis. , 2007, Medicine and science in sports and exercise.

[11]  B. Maron,et al.  Remodeling of Left Ventricular Hypertrophy in Elite Athletes After Long-Term Deconditioning , 2002, Circulation.

[12]  P. Baxter,et al.  Prevalence and prognosis of electrocardiographic findings in middle-aged men. , 1978, British heart journal.

[13]  H. Saner,et al.  Atrial remodeling, autonomic tone, and lifetime training hours in nonelite athletes. , 2011, The American journal of cardiology.

[14]  K. George,et al.  “Exercise‐Induced Cardiac Fatigue”—A Review of the Echocardiographic Literature , 2010, Echocardiography.

[15]  K. George,et al.  Post-Exercise Cardiac Troponin Release is Related to Exercise Training History , 2012, International Journal of Sports Medicine.

[16]  K. George,et al.  A depression in left ventricular diastolic filling following prolonged strenuous exercise is associated with changes in left atrial mechanics. , 2010, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[17]  M. Murayama,et al.  New upper limit of physiologic cardiac hypertrophy in Japanese participants in the 100-km ultramarathon. , 2003, Journal of the American College of Cardiology.

[18]  K. George,et al.  Does the Human Heart Fatigue Subsequent to Prolonged Exercise? , 2003, Sports medicine.

[19]  G. Whyte.  Clinical significance of cardiac damage and changes in function after exercise. , 2008, Medicine and science in sports and exercise.

[20]  J. Brugada,et al.  Cardiac Arrhythmogenic Remodeling in a Rat Model of Long-Term Intensive Exercise Training , 2011, Circulation.

[21]  D. Warburton,et al.  Mechanisms underpinning exercise-induced changes in left ventricular function. , 2008, Medicine and science in sports and exercise.

[22]  K. George,et al.  Evidence of increased electro-mechanical delay in the left and right ventricle after prolonged exercise , 2009, European Journal of Applied Physiology.

[23]  K. George,et al.  Dilatation and Dysfunction of the Right Ventricle Immediately After Ultraendurance Exercise: Exploratory Insights From Conventional Two-Dimensional and Speckle Tracking Echocardiography , 2011, Circulation. Cardiovascular imaging.

[24]  K. George,et al.  Cardiac electromechanical delay is increased during recovery from 40 km cycling but is not mediated by exercise intensity , 2013, Scandinavian journal of medicine & science in sports.

[25]  H. Arnesen,et al.  Mortality and cardiovascular morbidity among long‐term endurance male cross country skiers followed for 28–30 years , 2011, Scandinavian journal of medicine & science in sports.

[26]  H. Calkins,et al.  Echocardiographic findings in patients meeting task force criteria for arrhythmogenic right ventricular dysplasia: new insights from the multidisciplinary study of right ventricular dysplasia. , 2005, Journal of the American College of Cardiology.

[27]  W. Mckenna,et al.  Left Ventricular Morphology and Function in Female Athletes: A Meta-Analysis , 2004, International journal of sports medicine.

[28]  J. Ganame,et al.  Reduced right ventricular ejection fraction in endurance athletes presenting with ventricular arrhythmias: a quantitative angiographic assessment. , 2007, European heart journal.

[29]  Wilfried Kindermann,et al.  Athlete's heart: right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging. , 2002, Journal of the American College of Cardiology.

[30]  K. George,et al.  A prospective randomised longitudinal MRI study of left ventricular adaptation to endurance and resistance exercise training in humans , 2011, The Journal of physiology.

[31]  C. Wren,et al.  Cardiovascular pre-participation screening of young competitive athletes for prevention of sudden death: proposal for a common European protocol. , 2005, European heart journal.

[32]  K. George,et al.  Postexercise changes in left ventricular function: the evidence so far. , 2008, Medicine and science in sports and exercise.

[33]  A. Boland,et al.  Training-specific changes in cardiac structure and function: a prospective and longitudinal assessment of competitive athletes. , 2008, Journal of applied physiology.

[34]  B. Maron,et al.  Hypertrophic cardiomyopathy compatible with successful completion of the marathon. , 1984, American Journal of Cardiology.

[35]  K. George,et al.  Cardiac adaptation to acute and chronic participation in endurance sports , 2011, Heart.

[36]  J. Brugada,et al.  Endurance sport practice as a risk factor for atrial fibrillation and atrial flutter , 2008, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[37]  G. Thiene,et al.  Differences and similarities between arrhythmogenic right ventricular cardiomyopathy and athlete’s heart adaptations , 2008, British Journal of Sports Medicine.

[38]  G. Di Salvo,et al.  Range of right heart measurements in top-level athletes: the training impact. , 2013, International journal of cardiology.

[39]  G. Limongelli,et al.  Left atrial myocardial function in either physiological or pathological left ventricular hypertrophy: a two-dimensional speckle strain study , 2007, British Journal of Sports Medicine.

[40]  K. George,et al.  Upper limits of physiological cardiac adaptation in ultramarathon runners. , 2011, Journal of the American College of Cardiology.

[41]  G. Whyte,et al.  Ethnic Differences in Physiological Cardiac Adaptation to Intense Physical Exercise in Highly Trained Female Athletes , 2010, Circulation.

[42]  N. Terrados,et al.  Prevalence and upper limit of cardiac hypertrophy in professional cyclists , 2004, European Journal of Applied Physiology and Occupational Physiology.

[43]  M Santini,et al.  Ventricular arrhythmias and athlete's heart. Role of signal-averaged electrocardiography. , 1996, European heart journal.

[44]  K. George,et al.  Exercise-induced cardiac troponin elevation: evidence, mechanisms, and implications. , 2010, Journal of the American College of Cardiology.

[45]  K. George,et al.  Exercise-associated increases in cardiac biomarkers. , 2008, Medicine and science in sports and exercise.

[46]  B. Maron,et al.  Reduction in left ventricular wall thickness after deconditioning in highly trained Olympic athletes. , 1993, British heart journal.

[47]  Jan Bogaert,et al.  Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. , 2012, European heart journal.

[48]  A H Zwinderman,et al.  The athlete's heart. A meta-analysis of cardiac structure and function. , 2000, Circulation.

[49]  H. Quinney,et al.  Left ventricular morphology in junior and master resistance trained athletes. , 2000, Medicine and science in sports and exercise.

[50]  E. Ashley,et al.  Interpretation of the Electrocardiogram of Young Athletes , 2011, Circulation.

[51]  E. E. van der Wall,et al.  Myocardial adaptation in different endurance sports: an echocardiographic study , 2004, The International Journal of Cardiovascular Imaging.

[52]  M. Proschan,et al.  The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. , 1991, The New England journal of medicine.

[53]  B. Maron,et al.  Patterns of ventricular tachyarrhythmias associated with training, deconditioning and retraining in elite athletes without cardiovascular abnormalities. , 2011, The American journal of cardiology.

[54]  B. Maron,et al.  Clinical significance of abnormal electrocardiographic patterns in trained athletes. , 2000, Circulation.

[55]  J. Nielsen,et al.  Is the risk of atrial fibrillation higher in athletes than in the general population? A systematic review and meta-analysis. , 2009, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[56]  D. Warburton,et al.  Prolonged strenuous exercise alters the cardiovascular response to dobutamine stimulation in male athletes , 2005, The Journal of physiology.

[57]  D. Low,et al.  Cardiac troponin I is released following high-intensity short-duration exercise in healthy humans. , 2010, International journal of cardiology.

[58]  B. Maron,et al.  Long-term clinical consequences of intense, uninterrupted endurance training in olympic athletes. , 2010, Journal of the American College of Cardiology.

[59]  K. George,et al.  Diverse Patterns of Myocardial Fibrosis in Lifelong, Veteran Endurance Athletes , 2011, Journal of applied physiology.

[60]  G. De Backer,et al.  Prognostic value of ischemic electrocardiographic findings for cardiovascular mortality in men and women. , 1998, Journal of the American College of Cardiology.

[61]  K. Jöckel,et al.  Myocardial late gadolinium enhancement: prevalence, pattern, and prognostic relevance in marathon runners. , 2009, Radiology.

[62]  W. Gonyea,et al.  Echocardiographic left ventricular masses in distance runners and weight lifters. , 1980, Journal of applied physiology: respiratory, environmental and exercise physiology.

[63]  F. Katsukawa,et al.  Unusual left ventricular dilatation without functional or biochemical impairment in normotensive extremely overweight Japanese professional sumo wrestlers. , 2003, The American journal of cardiology.

[64]  Mathew G. Wilson,et al.  Hypertrophic cardiomyopathy and ultra-endurance running - two incompatible entities? , 2011, Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance.

[65]  J. Brugada,et al.  Long-term endurance sport practice increases the incidence of lone atrial fibrillation in men: a follow-up study. , 2008, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[66]  J. Ménard,et al.  Serial left ventricular adaptations in world-class professional cyclists: implications for disease screening and follow-up. , 2004, Journal of the American College of Cardiology.

[67]  W. Henry,et al.  Comparative left ventricular dimensions in trained athletes. , 1975, Annals of internal medicine.

[68]  A. Sahlén,et al.  Predisposing factors and consequences of elevated biomarker levels in long-distance runners aged >or=55 years. , 2009, The American journal of cardiology.

[69]  Richard B Devereux,et al.  Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardio , 2005, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[70]  S. Solomon,et al.  GUIDELINES AND STANDARDS , 2010 .

[71]  B. Saltin,et al.  CIRCULATORY RESPONSE TO PROLONGED SEVERE EXERCISE. , 1964, Journal of applied physiology.

[72]  Barry J Maron,et al.  Recommendations for interpretation of 12-lead electrocardiogram in the athlete. , 2009, European heart journal.

[73]  B. Maron,et al.  Outcomes in athletes with marked ECG repolarization abnormalities. , 2008, The New England journal of medicine.

[74]  J. D’hooge,et al.  Exercise strain rate imaging demonstrates normal right ventricular contractile reserve and clarifies ambiguous resting measures in endurance athletes. , 2012, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[75]  K. George,et al.  Cardiac troponin T release is stimulated by endurance exercise in healthy humans. , 2008, Journal of the American College of Cardiology.

[76]  H. Calkins,et al.  Arrhythmogenic right ventricular dysplasia/cardiomyopathy (ARVD/C): a multidisciplinary study: design and protocol. , 2003, Circulation.

[77]  D. Corrado,et al.  Controversies in cardiovascular medicine Risk of sports : do we need a pre-participation screening for competitive and leisure athletes ? , 2011 .

[78]  J. Manson,et al.  Body weight and mortality. A 27-year follow-up of middle-aged men. , 1993, JAMA.

[79]  A. Mosterd,et al.  Cardiac MRI reference values for athletes and nonathletes corrected for body surface area, training hours/week and sex , 2010, European journal of cardiovascular prevention and rehabilitation : official journal of the European Society of Cardiology, Working Groups on Epidemiology & Prevention and Cardiac Rehabilitation and Exercise Physiology.

[80]  K. George,et al.  Left ventricular function immediately following prolonged exercise: A meta-analysis. , 2006, Medicine and science in sports and exercise.

[81]  S. Caselli,et al.  Three-dimensional echocardiographic characterization of left ventricular remodeling in Olympic athletes. , 2011, The American journal of cardiology.

[82]  Lippincott Williams Wilkins,et al.  Coronary artery surgery study (CASS): a randomized trial of coronary artery bypass surgery. Survival data. , 1983, Circulation.

[83]  D. Warburton,et al.  The effects of prolonged strenuous exercise on left ventricular function: a brief review. , 2002, Heart & lung : the journal of critical care.

[84]  M. Sheppard,et al.  Post-mortem evidence of idiopathic left ventricular hypertrophy and idiopathic interstitial myocardial fibrosis: is exercise the cause? , 2007, British Journal of Sports Medicine.

[85]  J. Marshall,et al.  Persistent and reversible cardiac dysfunction among amateur marathon runners. , 2006, European heart journal.

[86]  K. George,et al.  171 The right ventricle of the endurance athlete: the relationship between morphology and deformation , 2011, Heart.

[87]  S. Tanguy,et al.  β-Adrenergic receptors desensitization is not involved in exercise-induced cardiac fatigue: NADPH oxidase-induced oxidative stress as a new trigger. , 2011, Journal of applied physiology.

[88]  W. Rodney,et al.  The athletic heart syndrome. , 1985, The New England journal of medicine.

[89]  H. Heidbuchel,et al.  High prevalence of right ventricular involvement in endurance athletes with ventricular arrhythmias. Role of an electrophysiologic study in risk stratification. , 2003, European heart journal.

[90]  J. Brugada,et al.  Long-lasting sport practice and lone atrial fibrillation. , 2002, European heart journal.

[91]  N. Prakken,et al.  Echocardiographic tissue deformation imaging of right ventricular systolic function in endurance athletes. , 2008, European heart journal.

[92]  Hein Heidbüchel,et al.  Disproportionate exercise load and remodeling of the athlete's right ventricle. , 2011, Medicine and science in sports and exercise.

[93]  H. Heidbuchel,et al.  Long-term endurance sport is a risk factor for development of lone atrial flutter , 2011, Heart.

[94]  K. Teo,et al.  Effects of 16 weeks of resistance training on left ventricular morphology and systolic function in healthy men >60 years of age. , 2000, The American journal of cardiology.