Commentaries on Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone?
2013; American Physiological Society; Volume: 114; Issue: 9 Linguagem: Inglês
10.1152/japplphysiol.00270.2013
ISSN8750-7587
AutoresCarlos Eduardo Negrão, Luciana Diniz Nagem Janot de Matos, Valdir A. Braga, John H. Coote, Hugo Celso Dutra de Souza,
Tópico(s)Heart rate and cardiovascular health
ResumoViewpointCommentaries on Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone?Published Online:01 May 2013https://doi.org/10.1152/japplphysiol.00270.2013MoreSectionsPDF (37 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations CHANGES IN PACEMAKER CELLS DETERMINE RESTING BRADYCARDIA AFTER EXERCISE TRAININGCarlos Eduardo NegraoFull Professor and Luciana D. N. Janot de MatosHeart Institute.to the editor: Resting bradycardia is an unquestionable marker of exercise training adaptation (1) and has been consistently documented in different species (2, 4). The question is whether this cardiac adaptation is due to increased vagal tone, sympathetic tone reduction, or decrease in intrinsic heart rate. In our investigations, exercise training reduces vagal and sympathetic tonus in a similar matter (5), which implies that no change in resting heart rate should be expected. However, we found a reduced resting heart rate, as extensively demonstrated by other investigators. These findings strongly suggest that the bradycardia provoked by exercise training is not simply a result of changes in the vagal and sympathetic balance. In fact, further investigation with double blockade with methylatropine and propranolol showed that intrinsic heart rate was significantly reduced in exercise-training animals compared with untrained animals. Our studies provide no evidence for increased vagal function after exercise training. On the contrary, exercise training virtually decreases vagal function. Baroreflex bradycardia provoked by vasoconstrictor drug, bradycardic responses caused by electrical stimulation of the vagal nerve, and responses to methacholine injection are all depressed after exercise training. These findings lead us to strongly agree with Boyett and collaborators (3) that “resting bradycardia cannot be explained by high vagal tone.” The resting bradycardia is a consequence of pacemaker cell alterations and intrinsic heart rate reduction.REFERENCES1. Badder HS. Resting bradycardia of exercise training: a concept based on currently available data. Recent Adv Stud Cardiac Struct Metab 10: 553–560, 1975.Google Scholar2. Barnard RJ , Corre K , Cho H. Effect of training on the resting heart rate of rats. Eur J Appl Physiol Occup Physiol 35: 285–289, 1976.Crossref | ISI | Google Scholar3. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone?“ J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar4. Hanne-Paparo N , Drory Y , Schoenfeld Y , Shapira Y , Kellermann JJ. Common ECG changes in athletes. Cardiology 61: 267–278, 1976.Crossref | ISI | Google Scholar5. Negrao CE , Moreira ED , Santos MC , Farah VM , Krieger EM. Vagal function impairment after exercise training. J Appl Physiol 72: 1749–1753, 1992.Link | ISI | Google ScholarREFERENCES1. Badder HS. Resting bradycardia of exercise training: a concept based on currently available data. Recent Adv Stud Cardiac Struct Metab 10: 553–560, 1975.Google Scholar2. Barnard RJ , Corre K , Cho H. Effect of training on the resting heart rate of rats. Eur J Appl Physiol Occup Physiol 35: 285–289, 1976.Crossref | ISI | Google Scholar3. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone?“ J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar4. Hanne-Paparo N , Drory Y , Schoenfeld Y , Shapira Y , Kellermann JJ. Common ECG changes in athletes. Cardiology 61: 267–278, 1976.Crossref | ISI | Google Scholar5. Negrao CE , Moreira ED , Santos MC , Farah VM , Krieger EM. Vagal function impairment after exercise training. J Appl Physiol 72: 1749–1753, 1992.Link | ISI | Google ScholarRESTING BRADYCARDIA IN ATHLETES: COULD THE CURRENT TECHNIQUES LEAD TO MISINTERPRETATION?Valdir A. Braga.Author AffiliationsDirector Biotechnology Center - Federal University of Paraiba.to the editor: Trained athletes have been reported to have resting bradycardia, which was initially attributed to increases in cardiac vagal tone (2). More recently, this hypothesis has been questioned based on experimental evidences that shifted the focus to the sinoatrial node suggesting a reduction in the intrinsic heart rate (3). In their Viewpoint, Dr. Boyett and colleagues (1) took a critical look at the two lines of evidence favoring the high cardiac vagal tone hypothesis: 1) little or no change in the intrinsic heart rate in athletes and 2) an increase in heart rate variability in athletes. Although authors suggest that intrinsic remodeling of the sinoatrial node would play a major role in the bradycardia seen in athletes, we believe that the limitations of the currently employed techniques, such as drug-induced autonomic blockade with propranolol and atropine as well as heart rate variability, for indirect measuring cardiac vagal activity, compromised the conclusions and could lead to misassumptions. Therefore, we believe that combining direct recording of the cardiac vagal tone in athletes and/or experimental animals to cellular approaches ranging from enzymes and other cellular mediators to electrophysiological properties of the sinoatrial none cells would help to unravel the precise role played by the parasympathetic activity and by the cells in the sinoatrial node in producing resting bradycardia in trained athletes. However, there is still need for refining the experimental approaches to investigate such mechanisms.REFERENCES1. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar2. Smith M , Hudson D , Graitzer H , Raven P. Exercise training bradycardia: the role of autonomic balance. Med Sci Sports Exert 21: 40–44, 1989.Crossref | PubMed | ISI | Google Scholar3. Stein R , Medeiros CM , Rosito GA , Zimerman LI , Ribeiro JP. Intrinsic sinus and atrioventricular node electrophysiologic adaptations in endurance athletes. J Am Coll Cardiol 39: 1033–1038, 2002.Crossref | PubMed | ISI | Google ScholarREFERENCES1. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar2. Smith M , Hudson D , Graitzer H , Raven P. Exercise training bradycardia: the role of autonomic balance. Med Sci Sports Exert 21: 40–44, 1989.Crossref | PubMed | ISI | Google Scholar3. Stein R , Medeiros CM , Rosito GA , Zimerman LI , Ribeiro JP. Intrinsic sinus and atrioventricular node electrophysiologic adaptations in endurance athletes. J Am Coll Cardiol 39: 1033–1038, 2002.Crossref | PubMed | ISI | Google ScholarA STALKING HORSE FOR RESTING HEART RATE IN ATHLETESJohn H. Coote.Author AffiliationsProfessor Emeritus University of Birmingham UK.to the editor: The paper by Boyett et al. (3) makes an argument in a theoretical analysis for a decrease in intrinsic pacemaker rate. This idea is not new. Boyett et al. (3) provide some further “food for thought.” I have some criticisms of this analysis. It is poor science to cross-compare data between the studies in parallel groups 2–11 (Table 1) that are not biologically similar. This is only valid in a longitudinal study such as one in which the conclusion could be different to that of Boyett's. The arguments take no account of changes in the vagal mediated baro-heart rate reflex sensitivity following training in animal and human that also have been shown to be protective against ventricular fibrillation (5). Appraisal of heart rate variability (HVR) is superficial and there is no comment on its vagal dependence. Al-Ani et al. (1) based conclusions on several indices and did not use SDNN. Their data of HF peak in PSA and the larger initial changes in R-R interval in response to muscle contraction in trained vs. untrained subject are well proven indices of vagal tone (2, 4). Changes in peripheral signaling involving nNOS are not considered. I accept that long-term exercise is likely to result in a remodeling of pacemaker currents but the influence of autonomic innervation should not be dismissed.REFERENCES1. Al-Ani M , Munir SM , White M , Townend J , Coote JH. Changes in R-R variability before and after endurance training measured by power spectral analysis and by the effect of isometric muscle contraction. Eur J Appl Physiol Occup Physiol 74: 397–403, 1996.Crossref | PubMed | ISI | Google Scholar2. Al-Ani M , Robins K , al-Khalidi AH , Vaile J , Townend J , Coote JH. Isometric contraction of arm flexor muscles as a method of evaluating cardiac vagal tone in man. Clin Sci (Lond) 92: 175–180, 1997.Crossref | ISI | Google Scholar3. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar4. Eckberg DL. Human sinus arrhythmia as an index of vagal cardiac outflow. J Appl Physiol 54: 961–966, 1983.Link | ISI | Google Scholar5. Schwartz PJ , Vanoli E , Stramba-Badiale M , De Ferrari GM , Billman GE , Foreman RD. Autonomic mechanisms and sudden death. New insights from analysis of baroreceptor reflexes in conscious dogs with and without a myocardial infarction. Circulation 78: 969–979, 1988.Crossref | PubMed | ISI | Google ScholarREFERENCES1. Al-Ani M , Munir SM , White M , Townend J , Coote JH. Changes in R-R variability before and after endurance training measured by power spectral analysis and by the effect of isometric muscle contraction. Eur J Appl Physiol Occup Physiol 74: 397–403, 1996.Crossref | PubMed | ISI | Google Scholar2. Al-Ani M , Robins K , al-Khalidi AH , Vaile J , Townend J , Coote JH. Isometric contraction of arm flexor muscles as a method of evaluating cardiac vagal tone in man. Clin Sci (Lond) 92: 175–180, 1997.Crossref | ISI | Google Scholar3. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar4. Eckberg DL. Human sinus arrhythmia as an index of vagal cardiac outflow. J Appl Physiol 54: 961–966, 1983.Link | ISI | Google Scholar5. Schwartz PJ , Vanoli E , Stramba-Badiale M , De Ferrari GM , Billman GE , Foreman RD. Autonomic mechanisms and sudden death. New insights from analysis of baroreceptor reflexes in conscious dogs with and without a myocardial infarction. Circulation 78: 969–979, 1988.Crossref | PubMed | ISI | Google ScholarCOMMENT ON “IS THE RESTING BRADYCARDIA IN ATHLETES THE RESULT OF REMODELING OF THE SINOATRIAL NODE RATHER THAN HIGH VAGAL TONE?”Hugo D. Souza.Author AffiliationsProfessor University of Sao Paulo.to the editor: The basal heart rate (HR) has always been considered an indirect index of fitness, often used as a parameter in individuals undergoing physical training. However, where was discussed the origin of prominent bradycardia at rest observed in trained individuals, especially in high level athletes? The study by Boyett et al. (1) makes a systematic review of the findings of several authors, both clinical and experimental, and discusses the possible mechanisms responsible for bradycardia, with a focus on cardiac autonomic control and reduction of intrinsic HR (iHR). In fact, the autonomic nervous system has been touted as a major contributor to the bradycardia at rest. This bradycardia was due to adjustments in cardiac autonomic balance characterized by increased vagal autonomic drive and/or reduction of sympathetic autonomic drive (2). In this case, these adjustments may result from central or peripheral adaptations of structures involved with autonomic nervous system, i.e., afferent, central nuclei, efferent, and cardiac autonomic receptors. However, in experimental studies with rats, the reduction in basal HR, due to the physical training, seems to depend on the two mechanisms, i.e., reduction in iHR and adaptations in cardiac autonomic balance (3, 4). Moreover, the study of Tezini et al. (4) also shows that the bradycardia at rest in young animals is more dependent on iHR reduction, whereas in older animals it is more dependent on the autonomic balance adjustments. Finally, studies in humans are needed to confirm these findings.REFERENCES1. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar2. Smith ML , Hudson DL , Graitzer HM , Raven PB. Exercise training bradycardia: the role of autonomic balance. Med Sci Sports Exerc 21: 40–44, 1989.Crossref | PubMed | ISI | Google Scholar3. Stein R , Medeiros CM , Rosito GA , Zimenman LI , Ribeiro JP. Intrinsic sinus and atrioventricular node electrophysiologic adaptations in endurance athletes. J Am Coll Cardiol 39: 1033–1038, 2002.Crossref | PubMed | ISI | Google Scholar4. Tezini GC , Dias DP , Souza HC. Aerobic physical training has little effect on cardiovascular autonomic control in aging rats subjected to early menopause. Exp Gerontol 48: 147–153, 2013.Crossref | PubMed | ISI | Google ScholarREFERENCES1. Boyett MR , D'Souza A , Zhang H , Morris GM , Dobrzynski H , Monfredi O. Viewpoint: Is the resting bradycardia in athletes the result of remodeling of the sinoatrial node rather than high vagal tone? J Appl Physiol; doi:10.1152/japplphysiol.01126.2012.ISI | Google Scholar2. Smith ML , Hudson DL , Graitzer HM , Raven PB. Exercise training bradycardia: the role of autonomic balance. Med Sci Sports Exerc 21: 40–44, 1989.Crossref | PubMed | ISI | Google Scholar3. Stein R , Medeiros CM , Rosito GA , Zimenman LI , Ribeiro JP. Intrinsic sinus and atrioventricular node electrophysiologic adaptations in endurance athletes. J Am Coll Cardiol 39: 1033–1038, 2002.Crossref | PubMed | ISI | Google Scholar4. Tezini GC , Dias DP , Souza HC. Aerobic physical training has little effect on cardiovascular autonomic control in aging rats subjected to early menopause. Exp Gerontol 48: 147–153, 2013.Crossref | PubMed | ISI | Google Scholar Download PDF Previous Back to Top FiguresReferencesRelatedInformation Cited BySystolic blood pressure but not electrocardiogram QRS duration is associated with heart rate variability (HRV): a cross-sectional study in rural Australian non-diabetics2 May 2017 | Clinical Hypertension, Vol. 23, No. 1Aerobic physical training increases contractile response and reduces cardiac fibrosis in rats subjected to early ovarian hormone deprivationAna Carolina S. Felix, Sabrina G. V. Dutra, Geisa C. S. V. Tezini, Marcus Vinicius Simões, and Hugo Celso Dutra de Souza15 May 2015 | Journal of Applied Physiology, Vol. 118, No. 10 More from this issue > Volume 114Issue 9May 2013Pages 1356-1357 Copyright & PermissionsCopyright © 2013 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00270.2013PubMed23785129History Published online 1 May 2013 Published in print 1 May 2013 Metrics
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