Review Article

Atrial Fibrillation in Athletes Christos A. Goudis, MD, MSc,* Ioannis V. Ntalas, MD,† and Dimitrios G. Ketikoglou, MD, PhD‡

Abstract: Atrial fibrillation is the most common arrhythmia in athletes and may be associated with endurance sport practice. Atrial ectopic beats, chronic systemic inflammation, autonomic system alterations, anatomic adaptation, myocardial injury and illicit drugs seem to be implicated in the increased prevalence of atrial fibrillation in athletes, but clear evidence is lacking. Treatment of the arrhythmia is a challenging issue, as atrial fibrillation may impair athletic performances and deteriorate athletes’ quality of life. This review focuses on the epidemiology, possible pathophysiological mechanisms, and management of atrial fibrillation in athletes. Key Words: atrial fibrillation, athletes, endurance sport practice (Cardiology in Review 2015;23: 247–251)

A

trial fibrillation is the most common arrhythmia in clinical practice and is associated with increased cardiovascular morbidity and mortality.1,2 The prevalence increases with age, ranging from 0.5% at 40–50 years to 5–15% at 80 years.3,4 Several cardiac and extracardiac diseases, including structural heart disease, atrial septal defects, coronary artery disease, hypertension, diabetes mellitus, hyperthyroidism, and obesity are associated with atrial fibrillation.5 However, in a subset of patients younger than 60 years, atrial fibrillation occurs in the absence of structural heart disease, as determined by physical examination, electrocardiography, chest radiography, and echocardiography (lone atrial fibrillation).6 The prevalence of lone atrial fibrillation ranges from 2% to 10% in the general population to 30% in studies performed in patients with paroxysmal atrial fibrillation, who seek medical attention.7,8 Even though the benefits of regular physical activity in controlling cardiovascular risk factors have been extensively proved,9–12 numerous studies have demonstrated that endurance exercise may increase the risk of developing atrial fibrillation in middle-aged ­athletes.13–22 A competitive athlete is defined as one who participates in an organized team or individual sport that requires regular competition against others as a central component, places a high premium on excellence and achievement, and requires some form of systematic (and usually intense) training.23 This review provides epidemiological data regarding atrial fibrillation in competitive athletes, and describes the possible pathophysiological mechanisms and therapeutic options of atrial fibrillation in this special population.

EPIDEMIOLOGY OF ATRIAL FIBRILLATION IN ATHLETES Prevalence of atrial fibrillation in athletes has been variable in recent studies. Furlanello et al24 reported that the prevalence of atrial

From the *Department of Cardiology, General Hospital of Grevena, Grevena, Greece; †Department of Cardiology, University Hospital of Ioannina, Ioannina, Greece; and ‡Department of Cardiology, Interbalkan Medical Center, Thessaloniki, Greece. Disclosure: The authors have no conflicts of interest to report. Correspondence: Christos A. Goudis, MD, MSc, Department of Cardiology, General Hospital of Grevena 51100, Grevena, Greece. E-mail:[email protected]. Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 1061-5377/15/2305-0247 DOI: 10.1097/CRD.0000000000000049

fibrillation was 0.2% in a population of 5000 athletes, and Pelliccia et al25 reported 0.3% in a study involving 1777 athletes. However, these studies included younger athletes with relatively fewer years of training, unlike the later reports. In a retrospective analysis, Mont et al26 concluded that the proportion of regular sport practice among men with lone atrial fibrillation was much higher than among men from the general population (63% versus 15%). Elosua et al14 reported that the proportion of patients with lone atrial fibrillation, who reported current sport practice (31%) was higher than that observed in controls (14%). In the logistic regression, the current practice of sport was associated with a higher prevalence of lone atrial fibrillation [odds ratio (OR), 3.13; 95% confidence interval (CI), 1.39–7.05]. Of note, the association of current sport practice with lone atrial fibrillation was observed at more than 1500 lifetime hours of sport practice (OR, 2.87; 95% CI, 1.20–6.91), suggesting the existence of a threshold point.14 Gender also seems to play a role in atrial fibrillation vulnerability among athletes. Grimsmo et al sought to determine not only the prevalence but also the possible predictors of lone atrial fibrillation in male long-term endurance cross-country skiers. They reported a high prevalence of lone atrial fibrillation (12.8%) and concluded that long PQ interval time in the electrocardiogram, bradycardia, and left atrial enlargement seem to be important risk factors for the initiation of the arrhythmia.18 The high prevalence of atrial fibrillation was probably due to the fact that the study included athletes from three different age groups.18 Wilhelm et al reported that for a comparable amount of training and performance, male athletes showed a more pronounced atrial remodeling, a concentric type of ventricular remodeling, an altered diastolic function, a higher blood pressure at rest and during exercise, and a higher sympathetic tone. The prevalence of atrial fibrillation was 3.3% and the authors concluded that atrial remodeling might facilitate the occurrence of atrial fibrillation.27 In a recent meta-analysis, Abdulla and Nielsen reported a fivefold increased risk of atrial fibrillation in middle-aged endurance athletes with a striking male predominance.28 Mortality data in athletes with atrial fibrillation are scarce and inconsistent. Karjalainen et al13 found significantly lower mortality in athletes compared with controls, but this finding was not confirmed by Baldesberger et al.15

PATHOPHYSIOLOGY OF ATRIAL FIBRILLATION IN ATHLETES The pathophysiological mechanisms responsible for the increased risk of atrial fibrillation in athletes remain speculative. Atrial ectopic beats, chronic systemic inflammation, autonomic system alterations, anatomic adaptation, myocardial injury, and illicit drugs have been proposed.

Atrial Ectopic Beats Atrial ectopic beats, in particular those originating from pulmonary veins, have been shown to be the triggers in most episodes of paroxysmal atrial fibrillation.29 Because atrial ectopy is increased as a consequence of physical activity,30,31 it was proposed that increased atrial ectopy could explain the increased risk of atrial fibrillation associated with sport practice. However, these findings were not confirmed by Baldesberger et al15 who did not find an increased incidence of atrial ectopy in former professional cyclists.

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Autonomic Nervous System Several observations suggest that autonomic nervous system plays an important role in the initiation and perpetuation of atrial fibrillation. Autonomic changes have been shown to precede the onset of paroxysmal atrial fibrillation.32 In patients with organic heart diseases, episodes of paroxysmal atrial fibrillation seem more sympathetically dependent.33 On the contrary, increased vagal activity can facilitate induction of paroxysmal atrial fibrillation by shortening the atrial refractory period in young patients without heart disease.34,35 Most of the available data in athletes implicate increased vagal tone as the principal mechanism of atrial fibrillation initiation. The origin of atrial fibrillation was vagal in 70% of patients in the Grup Integrat de Recerca en Fibril-laciό Auricular (GIRAFA) study.17 Grimsmo et al18 found that bradycardia and long PQ time were predictors for the occurrence of lone atrial fibrillation. Swanson et al36 suggested that gastroesophageal reflux may be a stimulus link between autonomic nervous system and exercise-induced atrial fibrillation. Wilhelm et al evaluated the impact of lifetime training hours of endurance athletes on signal-averaged P-wave duration and modifying factors. They found that in the high training group, vagal tone was significantly increased and premature atrial complexes were more frequent.27 These premature atrial complexes may serve as a trigger to initiate paroxysmal atrial fibrillation.29

Inflammation Inflammation may also play a role in the development of atrial fibrillation in athletes. Several studies have examined the acute phase response to strenuous exercise.37–42 Interleukin(IL)-1, IL-6 and tumor necrosis factor-alpha are involved in the acute phase response. These cytokines, with the possible exception of tumor necrosis factoralpha, temporarily increase during and shortly after prolonged exercise.43,44 IL-6 stimulates hepatic C-reactive protein (CRP) synthesis and increases as much as 100-fold after strenuous exercise.45–47 This increase in IL-6 is the earliest and most prominent of the cytokine responses to exercise.47 Other studies have related an increase in CRP and ILs in both paroxysmal and persistent atrial fibrillation.48,49 Psychari et al found CRP to be an independent predictor of atrial fibrillation. Both CRP and IL-6 were positively related to left atrial diameter and negatively related to left ventricular function, and IL-6 was also positively related to the duration of atrial fibrillation.50 In a recent study, Wilhelm et al51 demonstrated a transient increase in the levels of high-sensitivity CRP, proinflammatory cytokines, total leucocytes, and neutrophil granulocytes in elite marathon runners. However, despite these findings, the possible association among exercise, inflammation, and atrial fibrillation has not been confirmed yet.

Atrial Remodeling Morphologic adaptations in athletes’ hearts include increased atrial size and ventricular mass, and altered diastolic function. Even though left atrial remodeling in competitive athletes is assumed to be a physiologic adaptation to exercise conditioning, it may create a favorable substrate for atrial fibrillation. Atrial remodeling may be the consequence of long-standing volume and/or pressure overload. Endurance sports increase preload, which increases atrial pressure. In experimental models, increased atrial pressure shortens atrial refractory period and increases dispersion of atrial refractoriness, thereby favoring atrial fibrillation.52 Pelliccia et al25 reported that 20% of endurance sport athletes had larger left atrial dimensions compared with sedentary controls. Wilhelm et al27,53 found that in nonelite male athletes and professional soccer players, lifetime training hours and early repolarization pattern on the ECG respectively, were associated with increased left atrial volume. In addition, Wilhelm et al54 measured pro-atrial natriuretic peptide levels in marathon and nonmarathon runners, and concluded that marathon running was associated with progressive left and right atrial remodeling possibly induced by repetitive episodes of atrial stretching. Grimsmo et al18 reported that 248  |  www.cardiologyinreview.com

in endurance-trained athletes, left atrial diameter and left atrial area were larger in the atrial fibrillation group and left atrial size was associated with lone atrial fibrillation. Atrial fibrosis is a hallmark of atrial structural remodeling and predisposes to arrhythmogenicity and development of atrial fibrillation,55 but in endurance athletes, data regarding histological and biochemical remodeling are scarce. In an experimental study, Benito et al showed that male Wistar rats which were conditioned to run vigorously for 4, 8, and 16 weeks developed eccentric hypertrophy and diastolic dysfunction together with atrial dilation. Protein expression of fibrosis markers in both the atria and right ventricle were significantly greater in exercise rats than sedentary control rats.56 In a case– control study, Lindsay and Dunn analyzed the presence of humoral markers of fibrosis in veteran athletes compared with sedentary subjects. Veteran athletes showed an increase in serum collagen markers (C-terminal propeptide of procollagen type I[PICP], C-terminal telopeptide of collagen type I[CITP], and tissue inhibitor of matrix metalloproteinase 1[TIMP-1]), suggesting that long-term sport practice may provoke fibrosis as part of the hypertrophic process.57 Further studies are needed to correlate atrial fibrosis with atrial fibrillation in athletes.

Myocardial Injury The release of troponin T (TnT) and TnI has been demonstrated in several small studies after endurance exercise, suggesting that strenuous physical exertion may result in myocardial injury.58–62 Rifai et al59 concluded that ultraendurance exercise may cause myocardial damage based on plasma cardiac TnT (cTNT) and cTnI measurements, quantitative echocardiographic wall-motion analysis and ejection fraction measurements in athletes who participated in the Hawaii Ironman Triathlon. A meta-analysis by Shave et al63 demonstrated that exercise-induced cTnT release is apparent in almost half of the endurance athletes, and that detection of cTnT is not affected by age. It also showed that postexercise cTnT decreases slightly with mean body mass decrease and event duration increase. However, the exact mechanisms responsible for postexercise cTnT release and the kinetics of cTnT release after exercise are not clear, and whether postexercise cTnT release is related to microinjury of the myocardium remains to be elucidated. Magnetic resonance imaging allows definition of abnormal processes occurring at the tissue level, including myocardial edema, fatty infiltration, and importantly myocardial fibrosis.64 Breuckmann et al65 demonstrated that marathon participants exhibited late gadolinium enhancement (LGE) of the left ventricular myocardium three times more often than their age-matched controls. They also noted different patterns of LGE within the marathon participant group and suggested that the noncoronary artery disease pattern with small focal midmyocardial spots of LGE may develop from ischemic myocardial damage subsequent to coronary microembolization, or may be due to hypertensive cardiomyopathy or residual myocarditis.65 Wilson et al66 reported an unexpectedly high prevalence of myocardial fibrosis in healthy, asymptomatic, lifelong veteran male athletes compared with age-matched veteran controls and young athletes, suggesting a link between lifelong endurance exercise and myocardial fibrosis. On the contrary, several other studies did not demonstrate any evidence of LGE of the left ventricular myocardium, suggesting that true myocardial necrosis does not occur.67–72 Gaudreault et al evaluated recreational marathon runners before and after the marathon run. No myocardial necrosis was observed, but repeated acute edema and decreased perfusion associated with decreased function could contribute to explain the transient increase in cardiac risk previously reported during strenuous exercise.71 Karlstedt et al systematically evaluated the presence of occult coronary artery disease using cardiac computed tomography, as a potential cause of myocardial fibrosis in marathon athletes over the age of 50. They concluded that the presence of myocardial fibrosis in older marathon athletes is infrequent, © 2015 Wolters Kluwer Health, Inc. All rights reserved.

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but when present, it may be due to underlying occult coronary artery disease.72 Recreational marathon runners presenting with myocardial LGE were found to have higher coronary artery calcification scores, supporting a pathophysiological link between epicardial subclinical plaque burden and myocardial damage in marathon runners, thus increasing the awareness of coronary artery disease in this patient population.73 More studies, including athletes from all ages, will help to define the prevalence of silent coronary artery disease in marathon participants.

Drugs Several illicit drugs or substances banned by the World AntiDoping Agency may cause atrial fibrillation in athletes.74 These drugs include anabolic steroids, erythropoiesis-stimulating agents, growth hormone, insulin-like growth factor-1, stimulants (amphetamines, ephedrine, adrenaline, pseudoephedrine, methylphenidate), β2 agonists (salbutamol, formoterol, and salmeterol), alcohol, cannabinoids, ketamine, cocaine, ecstasy, and diuretics.75 There is increasing concern about the supraphysiological doses of anabolic steroids used among athletes for improving muscle mass and physical performance. In a recent meta-analysis and meta-regression analysis, the global lifetime prevalence rate of anabolic-androgenic steroid use was 3.3%, and the prevalence rate was significantly higher for males than for females (6.4% versus 1.6%).76 Common cardiovascular adverse effects of anabolic steroid abuse include left ventricular hypertrophy, hypertension, dyslipidemia, and thrombus formation.77,78 There are few published data with only two case reports of atrial fibrillation related to anabolic steroid abuse, one with moderate left atrial hypertrophy79 and another with a structurally normal heart.80 Left ventricular hypertrophy and altered baro-reflex81 and autonomic function82 may be possible pathophysiological mechanisms, but the role of anabolic steroids in the development of the arrhythmia remains obscure.

MANAGEMENT OF ATRIAL FIBRILLATION IN ATHLETES Sport Activity Reduction It is of outmost importance to recognize if atrial fibrillation episodes are attributed to excessive sport activity or not. In such cases, the initial approach is reduction of physical activity. Furlanello et al24 described a good response to sport abstinence in top-level athletes with atrial fibrillation. Hoogsteen et al20 showed that up to 30% of athletes experienced fewer episodes of atrial fibrillation by reducing sport activity. Further studies are needed to prove that limitation of sports activities can have favorable outcomes in athletes with atrial fibrillation.

Drug Therapy Angiotensin-converting enzyme inhibitors and angiotensin receptor blockers may prevent atrial fibrillation recurrences after ablation or cardioversion.83,84 According to the World Anti-Doping Agency, beta-blockers are not prohibited in endurance sports (prohibition is in force in specific sports’ competition including archery, automobile, billiards, darts, golf, shooting, skiing/snowboarding in ski jumping, freestyle aerials/halfpipe and snowboard halfpipe/ big air).85 However, the therapeutic goal of rate control is difficult to achieve in athletes, because beta-blockers are not well tolerated and digoxin or calcium antagonists alone will not be potent enough to slow the heart rate during exertional atrial fibrillation.86 In some athletes with paroxysmal atrial fibrillation, class I antiarrhythmic agents can be used only for acute reconversion therapy (pill-in-the pocket approach).87 Even though these drugs may prevent atrial fibrillation recurrences, atrial fibrillation can be converted to atrial flutter.88,89 In these cases, prophylactic ablation of the flutter circuit © 2015 Wolters Kluwer Health, Inc. All rights reserved.

Atrial Fibrillation

must be considered.86 Amiodarone is more efficient in preventing atrial fibrillation recurrences, but the potential side-effects limit its use.5 In young athletes with no underlying structural heart disease, the risk for thromboembolism is low without treatment. For athletes with nonvalvular atrial fibrillation and a CHA2DS2-VASc score of 0, it is reasonable to omit antithrombotic therapy.90 Antiplatelet agents or oral anticoagulants may be necessary depending on the presence of risk factors for thromboembolic events.90 It is also noteworthy that anticoagulation therapy excludes athletes from sports with risk of bodily collision or trauma.86

Direct-Current Cardioversion Direct-current cardioversion is indicated in athletes with atrial fibrillation, who require emergency cardioversion, caused by hemodynamic instability.90 In these cases, the initiation of anticoagulation should not delay interventions to stabilize the patient. If atrial fibrillation duration is ≤48 h, it is common practice to perform a cardioversion without transesophageal echocardiogram (TEE) or antecedent anticoagulation.90 If atrial fibrillation duration is ≥48 h or the duration is unknown, cardioversion can be attempted only with therapeutic anticoagulation for at least 3 weeks prior and continued for at least 4 weeks after. For athletes with atrial fibrillation of 48-h duration or longer or of unknown duration who have not been anticoagulated for the preceding 3 weeks, it is reasonable to perform a TEE before cardioversion and proceed with cardioversion if no left atrial (LA) thrombus is identified, including the left atrial appendage (LAA), provided that anticoagulation is achieved before TEE and maintained after cardioversion for at least 4 weeks.90

Catheter Ablation Over the past decade, catheter ablation of atrial fibrillation has emerged from being a novel, largely unproven procedure to a very commonly performed procedure for treatment of patients with symptomatic atrial fibrillation.91 Recent studies have showed that catheter ablation is also effective and safe for athletes suffering from atrial fibrillation. Furlanello et al92 described a highly successful ablation, with 90% success after a mean of two ablation procedures in a series of 20 athletes, without major complications. Calvo et al93 proved that the probability of remaining free of atrial fibrillation recurrences after a single circumferential pulmonary vein ablation was similar in athletes compared with controls, and that left atrial diameter and long-standing atrial fibrillation are the only independent predictors of recurrence. Koopman et al94 showed that in patients with documented focal induction of nonpermanent atrial fibrillation and the absence of large atrial size, pulmonary vein isolation is as effective in endurance athletes as in other patients, concluding that there is no reason to withhold ablation therapy from such athletes with atrial fibrillation.

RECOMMENDATIONS FOR ATHLETES WITH ATRIAL FIBRILLATION Guidelines for athletic participation are needed to reduce the risk for arrhythmia-related morbidity or mortality. Task Force 7 of the 36th Bethesda Conference recommends that athletes with asymptomatic atrial fibrillation in the absence of structural heart disease who maintain a ventricular rate that increases and slows appropriately and is comparable to that of a normal sinus response in relation to the level of activity, while receiving no therapy or therapy with AV nodal blocking drugs, can participate in all competitive sports.95 Athletes without structural heart disease who have elimination of atrial fibrillation by an ablation technique, including surgery, may participate in all competitive sports after 4 to 6 weeks without a recurrence or after an electrophysiologic study has confirmed noninducibility.95 www.cardiologyinreview.com  |  249

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CONCLUSION Endurance exercise training increases the risk for recurrent atrial fibrillation. Atrial morphologic adaptations and autonomic nervous system alterations seem to be implicated, but the exact pathophysiological mechanisms remain to be elucidated. Reduction of sports activities should be considered as part of the therapeutic advice to minimize the risk of atrial fibrillation development. Class I antiarrhythmic drugs can be used for acute conversion of paroxysmal atrial fibrillation and prevention of recurrences. Antiplatelet or anticoagulant administration depends on the presence of risk factors for thromboembolic events. Catheter ablation of atrial fibrillation has proven to be as effective and safe as in the general population and should be recommended in highly symptomatic drug-refractory endurance athletes. REFERENCES 1. Stewart S, Hart CL, Hole DJ, et al. A population-based study of the longterm risks associated with atrial fibrillation: 20-year follow-up of the Renfrew/ Paisley study. Am J Med. 2002;113:359–364. 2. Benjamin EJ, Wolf PA, D’Agostino RB, et al. Impact of atrial fibrillation on the risk of death: the Framingham Heart Study. Circulation. 1998;98:946–952. 3. Stewart S, Hart CL, Hole DJ, et al. Population prevalence, incidence, and predictors of atrial fibrillation in the Renfrew/Paisley study. Heart. 2001;86:516–521. 4. Go AS, Hylek EM, Phillips KA, et al. Prevalence of diagnosed atrial fibrillation in adults: national implications for rhythm management and stroke prevention: the AnTicoagulation and Risk Factors in Atrial Fibrillation (ATRIA) Study. JAMA. 2001;285:2370–2375. 5. Camm AJ, Kirchhof P, Lip GY, et al. Guidelines for the management of atrial fibrillation: the Task Force for the Management of Atrial Fibrillation of the European Society of Cardiology (ESC). Europace. 2010;12:1360–1420. 6. Chugh SS, Blackshear JL, Shen WK, et al. Epidemiology and natural history of atrial fibrillation: clinical implications. J Am Coll Cardiol. 2001;37:371–378. 7. Planas F, Romero-Menor C, Vazquez-Oliva G, et al. Natural history of and risk factors for idiopathic atrial fibrillation recurrence (FAP Registry). Rev Esp Cardiol. 2006;59:1106–1112. 8. Lévy S, Maarek M, Coumel P, et al. Characterization of different subsets of atrial fibrillation in general practice in France: the ALFA study. The College of French Cardiologists. Circulation. 1999;99:3028–3035. 9. Morris JN, Everitt MG, Pollard R, et al. Vigorous exercise in leisure-time: protection against coronary heart disease. Lancet. 1980;2:1207–1210. 10. Kujala UM, Kaprio J, Taimela S, et al. Prevalence of diabetes, hypertension, and ischemic heart disease in former elite athletes. Metabolism. 1994;43:1255–1260. 11. Blair SN, Kampert JB, Kohl HW 3rd, et al. Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA. 1996;276:205–210. 12. Thompson PD, Buchner D, Pina IL, et al. Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease: a statement from the Council on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity). Circulation. 2003;107:3109–3116. 13. Karjalainen J, Kujala UM, Kaprio J, et al. Lone atrial fibrillation in vigorously exercising middle aged men: case-control study. BMJ. 1998;316:1784–1785. 14. Elosua R, Arquer A, Mont L, et al. Sport practice and the risk of lone atrial fibrillation: a case-control study. Int J Cardiol. 2006;108:332–337. 15. Baldesberger S, Bauersfeld U, Candinas R, et al. Sinus node disease and arrhythmias in the long-term follow-up of former professional cyclists. Eur Heart J. 2008;29:71–78. 16. Molina L, Mont L, Marrugat J, et al. Long-term endurance sport practice increases the incidence of lone atrial fibrillation in men: a follow-up study. Europace. 2008;10:618–623. 17. Mont L, Tamborero D, Elosua R, et al; on behalf of the GIRAFA Investigators. Physical activity, height and left atrial size are independent risk factors for lone atrial fibrillation in middle-aged healthy individuals. Europace. 2008;10:15–20. 18. Grimsmo J, Grundvold I, Maehlum S, et al. High prevalence of atrial fibrillation in long-term endurance cross-country skiers: echocardiographic findings and possible predictors–a 28-30 years follow-up study. Eur J Cardiovasc Prev Rehabil. 2010;17:100–105. 19. Hood S, Northcote RJ. Cardiac assessment of veteran endurance athletes: a 12 year follow up study. Br J Sports Med. 1999;33:239–243.

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Cardiology in Review  •  Volume 23, Number 5, September/October 2015

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Atrial Fibrillation

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Atrial Fibrillation in Athletes.

Atrial fibrillation is the most common arrhythmia in athletes and may be associated with endurance sport practice. Atrial ectopic beats, chronic syste...
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