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Int J Sports Med 2016; 37(10): 792-798
DOI: 10.1055/s-0035-1569348
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Does Deep Bradycardia Increase the Risk of Arrhythmias and Syncope in Endurance Athletes?

D. Matelot
1   LTSI, Inserm UMR 1099, Rennes, F-35000
,
F. Schnell
2   Sport Medicine Department, University Hospital of Rennes, Rennes, France
,
N. Khodor
1   LTSI, Inserm UMR 1099, Rennes, F-35000
,
N. Endjah
2   Sport Medicine Department, University Hospital of Rennes, Rennes, France
,
G. Kervio
3   CIC-IT, Inserm Rennes 804, Rennes, F-35000
,
G. Carrault
1   LTSI, Inserm UMR 1099, Rennes, F-35000
,
N. Thillaye du Boullay
1   LTSI, Inserm UMR 1099, Rennes, F-35000
,
F. Carre
2   Sport Medicine Department, University Hospital of Rennes, Rennes, France
› Author Affiliations
Further Information

Publication History



accepted after revision 30 November 2015

Publication Date:
10 June 2016 (online)

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Abstract

The aim of this study was to evaluate whether endurance athletes who exhibit deep bradycardia are more prone to arrhythmias and reflex syncope than their non-bradycardic peers. 46 healthy men (ages 19–35) were divided into 3 groups based on whether they were sedentary (SED,<2 h/week) or endurance trained (ET,>6 h/week), and non-bradycardic (NB, resting heart rate (HR)≥60 bpm) or bradycardic (B, resting HR<50 bpm). Resting HR was lower in ETB vs. ETNB and SED (43.8±3.1, 61.3±3.3, 66.1±5.9 bpm, respectively; p<0.001). Thus, 16 SED, 13 ETNB and 17 ETB underwent resting echocardiography, maximal exercise test, tilt test (TT) and 24 h-Holter ECG. Subjects were followed-up during 4.7±1.1 years for training, syncope and cardiac events. Our results showed that incidence of arrhythmias and hypotensive susceptibility did not differ between groups. During follow-up, no episode of syncope or near-syncope was reported. However, cardio-inhibitory syncope occurrence tended to be higher in ETB. Left ventricular end-diastolic diameter index was increased in ETB vs. ETNB and was correlated with resting HR (r=− 0.64; p<0.001). As a result, athletes with deep bradycardia do not present more arrhythmias and more hypotensive susceptibility than their non-bradycardic peers. Cardiac enlargement and autonomic alteration both seem to be involved in an athlete’s bradycardia.

Key words

athlete’s heart - bradycardia - arrhythmias - syncope
 

  • References

  • 1 Barbier J, Ville N, Kervio G, Walther G, Carre F. Sports-specific features of athlete’s heart and their relation to echocardiographic parameters. Herz 2006; 31: 531-543
    CrossrefPubMedGoogle Scholar
  • 2 Biffi A, Maron BJ, Di Giacinto B, Porcacchia P, Verdile L, Fernando F, Spataro A, Culasso F, Casasco M, Pelliccia A. Relation between training-induced left ventricular hypertrophy and risk for ventricular tachyarrhythmias in elite athletes. Am J Cardiol 2008; 101: 1792-1795
    CrossrefPubMedGoogle Scholar
  • 3 Biffi A, Maron BJ, Verdile L, Fernando F, Spataro A, Marcello G, Ciardo R, Ammirati F, Colivicchi F, Pelliccia A. Impact of physical deconditioning on ventricular tachyarrhythmias in trained athletes. J Am Coll Cardiol 2004; 44: 1053-1058
    CrossrefPubMedGoogle Scholar
  • 4 Billman GE. The effect of heart rate on the heart rate variability response to autonomic interventions. Front Physiol 2013; 4: 222
    PubMedGoogle Scholar
  • 5 Calvo N, Brugada J, Sitges M, Mont L. Atrial fibrillation and atrial flutter in athletes. Br J Sports Med 2012; 46 (Suppl. 01) i37-i43
    CrossrefPubMedGoogle Scholar
  • 6 Carter JB, Banister EW, Blaber AP. Effect of endurance exercise on autonomic control of heart rate. Sports Med 2003; 33: 33-46
    CrossrefPubMedGoogle Scholar
  • 7 Carter R, Hinojosa-Laborde C, Convertino VA. Heart rate variability in patients being treated for dengue viral infection: new insights from mathematical correction of heart rate. Front Physiol 2014; 5: 46
    PubMedGoogle Scholar
  • 8 Convertino VA. Endurance exercise training: conditions of enhanced hemodynamic responses and tolerance to LBNP. Med Sci Sports Exerc 1993; 25: 705-712
    PubMedGoogle Scholar
  • 9 Coote JH, White MJ. CrossTalk proposal: Bradycardia in the trained athlete is attributable to high vagal tone. J Physiol 2015; 593: 1745-1747
    CrossrefPubMedGoogle Scholar
  • 10 Crawford MH. Physiologic consequences of systematic training. Cardiol Clin 1992; 10: 209-218
    PubMedGoogle Scholar
  • 11 D’Souza A, Sharma S, Boyett MR. CrossTalk opposing view: Bradycardia in the trained athlete is attributable to a downregulation of a pacemaker channel in the sinus node. J Physiol 2015; 593: 1749-1751
    CrossrefPubMedGoogle Scholar
  • 12 Deharo JC, Jego C, Lanteaume A, Djiane P. An implantable loop recorder study of highly symptomatic vasovagal patients: the heart rhythm observed during a spontaneous syncope is identical to the recurrent syncope but not correlated with the head-up tilt test or adenosine triphosphate test. J Am Coll Cardiol 2006; 47: 587-593
    CrossrefPubMedGoogle Scholar
  • 13 Douglas PS, Garcia MJ, Haines DE, Lai WW, Manning WJ, Patel AR, Picard MH, Polk DM, Ragosta M, Ward RP, Weiner RB. Appropriate Use Criteria for Echocardiography. J Am Coll Cardiol 2011; 57: 1126-1166
    CrossrefPubMedGoogle Scholar
  • 14 Dumont Ast J, Hernandez AI, Carrault G. Improving ECG beats delineation with an evolutionary optimization process. IEEE Trans Biomed Eng 2010; 57: 607-615
    CrossrefPubMedGoogle Scholar
  • 15 Durnin JV, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr 1974; 32: 77-97
    CrossrefPubMedGoogle Scholar
  • 16 Erz G, Mangold S, Franzen E, Claussen CD, Niess AM, Burgstahler C, Kramer U. Correlation between ECG abnormalities and cardiac parameters in highly trained asymptomatic male endurance athletes: evaluation using cardiac magnetic resonance imaging. Int J Cardiovasc Imaging 2013; 29: 325-334
    CrossrefPubMedGoogle Scholar
  • 17 Fadel PJ, Stromstad M, Hansen J, Sander M, Horn K, Ogoh S, Smith ML, Secher NH, Raven PB. Arterial baroreflex control of sympathetic nerve activity during acute hypotension: effect of fitness. Am J Physiol 2001; 280: H2524-H2532
    PubMedGoogle Scholar
  • 18 Forleo C, Guida P, Iacoviello M, Resta M, Monitillo F, Sorrentino S, Favale S. Head-up tilt testing for diagnosing vasovagal syncope: A meta-analysis. Int J Cardiol 2013; 168: 27-35
    CrossrefPubMedGoogle Scholar
  • 19 Giada F, Biffi A, Cannom DS, Cappato R, Capucci A, Corrado D, Delise P, Drezner JA, El-Sherif N, Estes 3rd M, Furlanello F, Heidbuchel H, Inama G, Lindsay BD, Maron BJ, Maron MS, Mont L, Olshansky B, Pelliccia A, Thiene G, Viskin S, Zeppilli P, Natale A, Raviele A. Sports and arrhythmias: a report of the International Workshop Venice Arrhythmias 2009. Eur J Cardiovasc Prev Rehabil 2010; 17: 607-612
    CrossrefPubMedGoogle Scholar
  • 20 Gratze G, Fortin J, Holler A, Grasenick K, Pfurtscheller G, Wach P, Schonegger J, Kotanko P, Skrabal F. A software package for non-invasive, real-time beat-to-beat monitoring of stroke volume, blood pressure, total peripheral resistance and for assessment of autonomic function. Comput Biol Med 1998; 28: 121-142
    CrossrefPubMedGoogle Scholar
  • 21 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2016 update. Int J Sports Med 2015; 36: 1121-1124
    Google Scholar
  • 22 Hastings JL, Levine BD. Syncope in the athletic patient. Prog Cardiovasc Dis 2012; 54: 438-444
    CrossrefPubMedGoogle Scholar
  • 23 Hedman K, Tamas E, Henriksson J, Bjarnegard N, Brudin L, Nylander E. Female athlete’s heart: Systolic and diastolic function related to circulatory dimensions. Scand J Med Sci Sports 2015; 25: 372-381
    CrossrefPubMedGoogle Scholar
  • 24 Heinonen I, Kudomi N, Kemppainen J, Kiviniemi A, Noponen T, Luotolahti M, Luoto P, Oikonen V, Sipila HT, Kopra J, Mononen I, Duncker DJ, Knuuti J, Kalliokoski KK. Myocardial blood flow and its transit time, oxygen utilization, and efficiency of highly endurance-trained human heart. Basic Res Cardiol 2014; 109: 413
    CrossrefPubMedGoogle Scholar
  • 25 Jardine DL. Vasovagal syncope: new physiologic insights. Cardiol Clin 2013; 31: 75-87
    CrossrefPubMedGoogle Scholar
  • 26 Katritsis DG, Camm AJ. Nonsustained ventricular tachycardia: where do we stand?. Eur Heart J 2004; 25: 1093-1099
    CrossrefPubMedGoogle Scholar
  • 27 Lampert R. Evaluation and management of arrhythmia in the athletic patient. Prog Cardiovasc Dis 2012; 54: 423-431
    CrossrefPubMedGoogle Scholar
  • 28 Levine BD. Regulation of central blood volume and cardiac filling in endurance athletes: the Frank-Starling mechanism as a determinant of orthostatic tolerance. Med Sci Sports Exerc 1993; 25: 727-732
    PubMedGoogle Scholar
  • 29 Levine BD, Buckey JC, Fritsch JM, Yancy CWJ, Watenpaugh DE, Snell PG, Lane LD, Eckberg DL, Blomqvist CG. Physical fitness and cardiovascular regulation: mechanisms of orthostatic intolerance. J Appl Physiol 1991; 70: 112-122
    PubMedGoogle Scholar
  • 30 Levine BD, Lane LD, Buckey JC, Friedman DB, Blomqvist CG. Left ventricular pressure-volume and Frank-Starling relations in endurance athletes. Implications for orthostatic tolerance and exercise performance. Circulation 1991; 84: 1016-1023
    CrossrefPubMedGoogle Scholar
  • 31 Lewis SF, Nylander E, Gad P, Areskog NH. Non-autonomic component in bradycardia of endurance trained men at rest and during exercise. Acta Physiol Scand 1980; 109: 297-305
    CrossrefPubMedGoogle Scholar
  • 32 Matelot D, Schnell F, Kervio G, Thillaye du Boullay N, Carre F. Athlete’s bradycardia may be a multifactorial mechanism. J Appl Physiol 2013; 114: 1755-1756
    CrossrefPubMedGoogle Scholar
  • 33 Mehlsen J, Kaijer MN, Mehlsen AB. Autonomic and electrocardiographic changes in cardioinhibitory syncope. Europace 2008; 10: 91-95
    PubMedGoogle Scholar
  • 34 Mellingsaeter MR, Wyller TB, Ranhoff AH, Wyller VB. Fit elderly men can also stand: orthostatic tolerance and autonomic cardiovascular control in elderly endurance athletes. Aging Clin Exp Res 2015; 27: 499-505
    CrossrefPubMedGoogle Scholar
  • 35 Mignot A, Donal E, Zaroui A, Reant P, Salem A, Hamon C, Monzy S, Roudaut R, Habib G, Lafitte S. Global longitudinal strain as a major predictor of cardiac events in patients with depressed left ventricular function: a multicenter study. J Am Soc Echocardiogr 2010; 23: 1019-1024
    CrossrefPubMedGoogle Scholar
  • 36 Millet GP, Vleck VE, Bentley DJ. Physiological differences between cycling and running: lessons from triathletes. Sports Med 2009; 39: 179-206
    CrossrefPubMedGoogle Scholar
  • 37 Mont L, Elosua R, Brugada J. Endurance sport practice as a risk factor for atrial fibrillation and atrial flutter. Europace 2009; 11: 11-17
    PubMedGoogle Scholar
  • 38 Mont L, Tamborero D, Elosua R, Molina I, Coll-Vinent B, Sitges M, Vidal B, Scalise A, Tejeira A, Berruezo A, Brugada J. Investigators G . 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
    CrossrefPubMedGoogle Scholar
  • 39 Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelisa A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr 2009; 10: 165-193
    CrossrefPubMedGoogle Scholar
  • 40 Negrao CE, Janot de Matos LD, Braga VA, Coote JH, Souza HD. Commentaries on Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone?. Journal of applied physiology 2013; 114: 1356-1357
    CrossrefPubMedGoogle Scholar
  • 41 Pelliccia A, Maron BJ, Culasso F, Di Paolo FM, Spataro A, Biffi A, Caselli G, Piovano P. Clinical significance of abnormal electrocardiographic patterns in trained athletes. Circulation 2000; 102: 278-284
    CrossrefPubMedGoogle Scholar
  • 42 Petersen ME, Williams TR, Gordon C, Chamberlain-Webber R, Sutton R. The normal response to prolonged passive head up tilt testing. Heart 2000; 84: 509-514
    CrossrefPubMedGoogle Scholar
  • 43 Predel HG. Marathon run: cardiovascular adaptation and cardiovascular risk. Eur Heart J 2014; 35: 3091-3098
    CrossrefPubMedGoogle Scholar
  • 44 Raven PB, Pawelczyk JA. Chronic endurance exercise training: a condition of inadequate blood pressure regulation and reduced tolerance to LBNP. Med Sci Sports Exerc 1993; 25: 713-721
    PubMedGoogle Scholar
  • 45 Sacha J. Why should one normalize heart rate variability with respect to average heart rate. Front Physiol 2013; 4: 306
    PubMedGoogle Scholar
  • 46 Sacha J, Sobon J, Sacha K, Barabach S. Heart rate impact on the reproducibility of heart rate variability analysis. Int J Cardiol 2013; 168: 4257-4259
    CrossrefPubMedGoogle Scholar
  • 47 Serra-Grima R, Puig T, Donate M, Gich I, Ramon J. Long-term follow-up of bradycardia in elite athletes. Int J Sports Med 2008; 29: 934-937
    Article in Thieme ConnectPubMedGoogle Scholar
  • 48 Shi X, Stevens GH, Foresman BH, Stern SA, Raven PB. Autonomic nervous system control of the heart: endurance exercise training. Med Sci Sports Exerc 1995; 27: 1406-1413
    PubMedGoogle Scholar
  • 49 Stegemann J, Meier U, Skipka W, Hartlieb W, Hemmer B, Tibes U. Effects of a multi-hour immersion with intermittent exercise on urinary excretion and tilt table tolerance in athletes and nonathletes. Aviat Space Environ Med 1975; 46: 26-29
    PubMedGoogle Scholar
  • 50 Stein R, Medeiros CM, Rosito GA, Zimerman LI, Ribeiro JP. Intrinsic sinus and atrioventricular node electrophysiologic adaptations in endurance athletes. J Am Coll Cardiol 2002; 39: 1033-1038
    CrossrefPubMedGoogle Scholar
  • 51 Sutton R, Brignole M. Twenty-eight years of research permit reinterpretation of tilt-testing: hypotensive susceptibility rather than diagnosis. Eur Heart J 2014; 35: 2211-2212
    CrossrefPubMedGoogle Scholar
  • 52 Task Force . Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 1996; 93: 1043-1065
    CrossrefPubMedGoogle Scholar
  • 53 Task Force for the D, Management of S, European Society of C, European Heart Rhythm A, Heart Failure A, Heart Rhythm S . Moya A, Sutton R, Ammirati F, Blanc JJ, Brignole M, Dahm JB, Deharo JC, Gajek J, Gjesdal K, Krahn A, Massin M, Pepi M, Pezawas T, Ruiz Granell R, Sarasin F, Ungar A, van Dijk JG, Walma EP, Wieling W. Guidelines for the diagnosis and management of syncope (version 2009). Eur Heart J 2009; 30: 2631-2671
    CrossrefPubMedGoogle Scholar
  • 54 Thompson PD. Cardiovascular adaptations to marathon running: the marathoner's heart. Sports Med 2007; 37: 444-447
    CrossrefPubMedGoogle Scholar
  • 55 van Lieshout JJ. Exercise training and orthostatic intolerance: a paradox?. J Physiol 2003; 551: 401
    CrossrefPubMedGoogle Scholar
  • 56 Voice RA, Lurie KG, Sakaguchi S, Rector TS, Benditt DG. Comparison of tilt angles and provocative agents (edrophonium and isoproterenol) to improve head-upright tilt-table testing. Am J Cardiol 1998; 81: 346-351
    CrossrefPubMedGoogle Scholar
  • 57 Wasserman K, Hansen J, Sue D, Casaburi R, Whipp B. Principles of exercise testing and interpretation. Third edition Lippincott & Wilkins; 1999
    Google Scholar
  • 58 Wilhelm M. Atrial fibrillation in endurance athletes. Eur J Prevent Cardiol 2014; 21: 1040-1048
    PubMedGoogle Scholar
  • 59 Winker R, Barth A, Bidmon D, Ponocny I, Weber M, Mayr O, Robertson D, Diedrich A, Maier R, Pilger A, Haber P, Rudiger HW. Endurance exercise training in orthostatic intolerance: a randomized, controlled trial. Hypertension 2005; 45: 391-398
    CrossrefPubMedGoogle Scholar
  • 60 Xhyheri B, Manfrini O, Mazzolini M, Pizzi C, Bugiardini R. Heart rate variability today. Prog Cardiovasc Dis 2012; 55: 321-331
    CrossrefPubMedGoogle Scholar
  • 61 Yamamoto K, Miyachi M, Saitoh T, Yoshioka A, Onodera S. Effects of endurance training on resting and post-exercise cardiac autonomic control. Med Sci Sports Exerc 2001; 33: 1496-1502
    CrossrefPubMedGoogle Scholar