Effects of aerobic training on heart rate

is an important factor to re- duce the indexes of cardiovascular and all causes morbi- mortality. However, there is, apparently, additional and in- dependent benefits of the regular practice of physical exercise and the improvement of the level of aerobic con- dition. Heart rate ( HR) is mediated primarily by the direct activity of the autonomic nervous system ( ANS), specifi- cally through the sympathetic and parasympathetic branch- es activities over the sinus node autorhythmicity, with pre- dominance of the vagal activity (parasympathetic) at rest, that is progressively inhibited since the onset of the exer- cise. The HR behavior has been widely studied during dif- ferent conditions and protocols associated to the exercise. A reduction of the cardiac vagal tone (parasympathetic function) and consequently a diminished HR variability in rest, independently of the protocol of measurement used, is related to an autonomic dysfunction, chronic-degenera- tive diseases and increased mortality risk. Individuals with high levels of aerobic condition have a lower resting HR, along with a larger parasympathetic activity or smaller sym- pathetic activity, but it is not necessarily a direct conse- quence of the exercise training, as long as other

independently of the protocol of measurement used, is related to an autonomic dysfunction, chronic-degenera- tive diseases and increased mortality risk. Individuals with high levels of aerobic condition have a lower resting HR, along with a larger parasympathetic activity or smaller sym- pathetic activity, but it is not necessarily a direct conse- quence of the exercise training, as long as other inherent adaptations to the aerobic conditioning can influence the resting HR. The HR response in the onset of the exercise represents the integrity of the vagus nerve, and the HR re- covery on the post-exercise transient also denotes impor- tant prognostic information; by the way, individuals that have a slow HR recovery in the first minute post-exercise have increased mortality risk. In conclusion, the physio-

114 Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003 the effect of pharmacological block 20-22 , and is almost ex- clusively mediated by vagal inhibition, with no significant sympathetic role 20 , partly from different times of latency from the two branches to this physiological stress. HR variability was originally studied by Hon and Lee 23 in newborns, and has been the target of many researches over the past few years. At a search with the key word “heart rate variability” on MedLine, there were over 6,000 refer- ences, 32% between the years 1999 and 2002, showing a raising interest on the theme within the academic/scientif- ic fields. HR variations or variability can be measured within the time and frequency domains, with specific protocols for each domain 24-30 , even with specificity enough for an isolated assessment of cardiac vagal tone (parasympathet- ic branch) in the transition from rest to dynamic exercise 20 . A reduction of the cardiac vagal tone, thus of HR vari- ability, regardless of the measuring protocol, is related to autonomic dysfunction, chronic-degenerative diseases, and increased mortality risk 31-37 , thus representing an impor- tant indicator of health status 38,39 . An isolated decrease of HR variability reflects a two- to five-fold increase in the relative mortality risk due to a cardiac event 33,40 ; when as- sociated to a significant decrease of baroreflex sensitivity (< 3 ms/mmHg), this relative risk may reach a 7-fold in- crease 33 . On the other hand, in individuals with congestive heart failure, even small increases in HR variability indi- ces, such as standard-deviation of normal RR intervals (time domain), may decrease mortality risk in up to 20% 32 . For this reason, and for its predominance on resting, cardiac vagal activity has been addressed in a number of trials, especially when it relates to physical activity. Today, at the light of science, one cannot deny that aero- bic training leads to improvement in the maximum oxygen uptake 15,41,42 , due to, at least in part, an increase of cardiac output from an increase in the

predominance on resting, cardiac vagal activity has been addressed in a number of trials, especially when it relates to physical activity. Today, at the light of science, one cannot deny that aero- bic training leads to improvement in the maximum oxygen uptake 15,41,42 , due to, at least in part, an increase of cardiac output from an increase in the systolic volume. Maximal HR does not tend to change, whereas somewhat smaller values may be seen in rest and, especially, during submax- imal exercise 43 , and are probably related to mechanisms such as increase of venous return and myocardial contrac- tility 44 . Furthermore, maximum O 2 uptake, both absolute, and gender and age-related, is an important longevity fac- tor, i.e., the higher the aerobic conditions of an individual, the smaller his/her mortality risk 3,45,46 (table 1). These ad- justments of HR behavior from aerobic training may also be due to changes in the sympathetic-vagal balance or in- trinsic adaptations, such as improvement in the atrioven- tricular conduction system 47 . Some studies suggest that the mere practice of physical exercises is not enough to effec- tively decrease mortality risk, being necessary that the train- ing program be capable of promoting adjustments in both, the individual’s aerobic condition 3,45,46 and the autonomic function 48 . It remains unclear if the improvement of the aerobic con- dition from training enhances cardiac vagal tone, thus rest- ing- HR variability. Therefore, the purpose of this review is to discuss the effects of aerobic training on the autonomic nervous system to control resting HR, and in the initial and Fig. 1 – Heart rate autonomic control at rest and at exercise. Parasym- pathetic role decreases when intensity of exercise is increased, and the opposite happens with the sympathetic role. TABLE 1 Mortality relative risk according to aerobic condition Aerobic RR condition* (CI 95%) Laukkanen et al., 2001 > 10.6 1.0 (ref) (asymptomatic individuals) 9.3-10.6 0.71-3.01 7.9-9.2 1.44-5.39 < 7.9 2.02-7.32 Kavanagh et al., 2002 < 4.2 1.0 (ref) (individual with 4.2-6.3 0.54-0.71 cardiovascular disease) > 6.3 0.33-0.47 Myers et al., 2002 1.0-5.9 3.0-6.8

opposite happens with the sympathetic role. TABLE 1 Mortality relative risk according to aerobic condition Aerobic RR condition* (CI 95%) Laukkanen et al., 2001 > 10.6 1.0 (ref) (asymptomatic individuals) 9.3-10.6 0.71-3.01 7.9-9.2 1.44-5.39 < 7.9 2.02-7.32 Kavanagh et al., 2002 < 4.2 1.0 (ref) (individual with 4.2-6.3 0.54-0.71 cardiovascular disease) > 6.3 0.33-0.47 Myers et al., 2002 1.0-5.9 3.0-6.8 (asymptomatic individuals) 6.0-7.9 1.5-3.8 8.0-9.9 1.1-2.8 10.0-12.9 0.7-2.2 > 13.0 1.0 (ref) Myers et al., 2002 1.0-4.9 3.3-5.2 (individuals with 5.0-6.4 2.4-3.7 cardiovascular conditions) 6.5-8.2 1.7-2.8 8.3-10.6 1.4-2.2 > 10.7 1.0 (ref) * Aerobic condition measured in METs. RR: Relative risk for cardiovascular mortality. ref.: Value of reference. Heart Rate Rest Maximal Exercise Parasympathe tic Symp atheti c Submaximal Exercise ...

Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003 115 final exercise transients, i.e., the potential of aerobic train- ing in inducing physiological changes of the cardiac vagal tone. This review was based primarily on original studies in humans of different medical and physical conditions (lev- els of physical activity) ranging from individuals with se- vere heart conditions, even heart-transplanted subjects, to healthy, but sedentary individuals to high-performance ath- letes. EFFECTS ON RESTING-HR A low resting HR reflects a good health condition, where- as higher values are apparently related to a higher mortal- ity risk 49 . A mistake often made in sports area is to use resting- HR as an indicator of the degree of aerobic condi- tioning, since the association between low resting- HR and maximal aerobic power is quite modest, and may be due to higher resting vagal activity 50 , reducing diastolic depolar- ization rate and prolonging duration of the cardiac cycle, primarily on account of a proportionally longer diastole 13 . However, can training induce higher resting vagal activity, and therefore be accountable for lower resting- HR? Studies suggest that well-trained or physically well-fit (aerobically) individuals present a lower resting- HR, sug- gestive of higher parasympathetic activity 51-55 or lower sym- pathetic activity 56 . However, except for the later, a cross- sectional analysis does not allow us to conclude that training was responsible for such adjustment on the ANS. These stud- ies did not take into consideration the level of aerobic con- ditioning and the autonomic function of athletes prior to training; by knowing that there is an important genetic in- fluence in determining HR variability 57 , one could specu- late that those individuals could have better cardiovascular adjustment upon training for having a better prior cardiac vagal tone 58 . Uusitalo et al. 59 and Bonaduce et al. 60 , after longitudinal studies, noted a reduction of resting- HR, even though significant changes in autonomic indicators were not seen. Exercise-induced bradycardia can also be due to intrinsic adaptation of the sinus node 61 . A lower resting- HR can

training for having a better prior cardiac vagal tone 58 . Uusitalo et al. 59 and Bonaduce et al. 60 , after longitudinal studies, noted a reduction of resting- HR, even though significant changes in autonomic indicators were not seen. Exercise-induced bradycardia can also be due to intrinsic adaptation of the sinus node 61 . A lower resting- HR can also be consequence of other factors derived from a training program 60 , such as the in- crease of venous return and systolic volume. With the im- provement of the venous return, there is an increase in the systolic volume, and according to Frank-Starling law, when there is an increase in the volume of blood in its cavities, there is an increase in heart contractility 62 . To keep resting- heart output constant, there is a decrease of HR in response to a higher systolic volume, and these adaptations are ex- pected in individuals with better aerobic conditioning 62 , re- gardless of their autonomic function. However, will train- ing effects on cardiorespiratory variables also modify ANS? EFFECTS ON EXERCISE-HR As previously discussed, HR behavior during the exer- cise is mediated by ANS. HR variability is the oscillation in time between consecutive myocardial contractions (systo- les) 23 . Studies with selective pharmacological block 22 showed the exclusive role of the vagus nerve in HR response at the initial transient of the exercise 20,21 , with predominance of the vagal activity at rest that is gradually inhibited at sub- maximal exercise 63 both active and passive 64-66 , up to the maximum level of exercise, when parasympathetic activi- ty is apparently totally inhibited 67 , causing smaller or ab- sence of HR variability. In the initial seconds of the exercise, HR increases due to inhibition of vagal activity, which not only increases atria contractility, but also conduction velocity of the ventricle depolarization wave from AV node 62 , regardless of the lev- el of intensity of the exercise 68,69 and aerobic conditioning of healthy individuals 70,71 . On other hand, an individual who does not elevate significantly his/her HR in the

increases due to inhibition of vagal activity, which not only increases atria contractility, but also conduction velocity of the ventricle depolarization wave from AV node 62 , regardless of the lev- el of intensity of the exercise 68,69 and aerobic conditioning of healthy individuals 70,71 . On other hand, an individual who does not elevate significantly his/her HR in the beginning of the exercise, may be signalizing an impaired vagal ac- tivity 72 . After this initial stage, as one goes on exercising, HR increases again, due to adrenergic overstimulation on sinus node, or due to increase of serum norepinephrine, or atrial mechanics distention and therefore, sinus node dis- tention due to a higher venous return, and the increase in body’s temperature and blood’s acidity 73 . While Tulppo et al. 74 and Goldsmith et al. 75 relate de- crease of HR variability to age, in face of decreased physi- cal fitness from aging, and that this could be reverted by maintaining or improving aerobic physical condition, re- sults from Migliaro et al. 76 and Byrne et al. 77 suggest that age alone could be the main factor to decrease autonomic modulation, regardless of aerobic fitness. The increase in maximal O 2 uptake through aerobic train- ing can lessen the age-related decrease of baroreflex sensi- tivity 78,79 . A program of mild-intensity exercises would be enough to show some improvement in the autonomic func- tion of healthy adults 80 or those with chronic heart fail- ure 81 , even without direct training supervision 82 ; changes on vagal activity caused by physical training would be cen- tral, possibly directly on baroreflex, whereas the sympa- thetic activity would be primarily related to peripheral changes (vasoconstriction) 82 . These changes can be seen already in the first weeks of training in individuals with coronary heart disease 83 and post-myocardial infarction ( MI) 84,85 . Even though Seals et al. 86 have suggested that such improvements should be further evidenced in individuals with abnormal cardiac function, believing that aerobic train- ing would have a smaller impact on HR variability of healthy individuals, Melanson

seen already in the first weeks of training in individuals with coronary heart disease 83 and post-myocardial infarction ( MI) 84,85 . Even though Seals et al. 86 have suggested that such improvements should be further evidenced in individuals with abnormal cardiac function, believing that aerobic train- ing would have a smaller impact on HR variability of healthy individuals, Melanson and Freedson 87 , Stein et al. 88 , Al-

116 Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003 Ani et al. 89 , and Gallo Jr et al. 90 reached significant out- comes with training on autonomic markers of healthy in- dividuals, and Levy et al. 91 further suggest that these gains would not be age-dependent. In spite of the different meth- odologies used, and the fact that time of effective training had ranged from six weeks to 12 months, the results were consonant, showing an increase in vagal activity due to an exercise program, or even a decrease in resting sympathet- ic activity, which aid to hemodynamic improvements 56,92 . Duru et al. 93 were not successful in investigating posi- tive effects of the regular physical exercises in the auto- nomic function of post- MI individuals when compared to sedentary matches, as, although resting- HR being lower after training, variability indices (in frequency domain) are not significantly altered. On the other hand, in the control group, there was a significant decrease of these indices, showing an advanced stage of autonomic imbalance in favor of a sympathetic preponderance in individuals with post- MI left ventricular dysfunction. These results can be interpreted in another way: the regular practice of physical exercises can, at least, maintain sympatho-vagal balance under para- sympathetic predominance in post- MI individuals, where- as sedentarism tends to increase sympathetic influence, even at rest. Other studies also failed in finding differentiated adaptations of ANS to a program of exercises. Loimaala et al. 94 did not find differences on variability indices of ap- parently healthy sedentary individuals with age ranging from 35 to 55 years, after 5 months of training, even at night, when sympathetic activity is quite decreased and there is less interference of other variables, with improve- ment on resting- HR only, probably due to intrinsic adapta- tions. On the other hand, another interesting aspect is that Boutcher and Stein 58 have observed that individuals with better cardiac vagal tone respond better to an aerobic train- ing, with higher gains in maximum oxygen uptake, and further decreasing resting- HR. Confirming the last studies,

other variables, with improve- ment on resting- HR only, probably due to intrinsic adapta- tions. On the other hand, another interesting aspect is that Boutcher and Stein 58 have observed that individuals with better cardiac vagal tone respond better to an aerobic train- ing, with higher gains in maximum oxygen uptake, and further decreasing resting- HR. Confirming the last studies, Uusitalo et al. 59 e Bonaduce et al. 60 , after investigating ef- fects of high aerobic performance training on autonomic modulations of young athletes, did not find differences, neither for males nor females. It is possible that some chang- es in ANS activity, due to training, are observed only as a response to a stimulus, such as changes in posture or dur- ing exercise, but not in rest 85,90 , as in most protocols. One cannot state that failure in finding differences in autonom- ic functions due to training is due to measuring in rest, without taking into account the possibility of a ceiling-ef- fect of ANS activities, which could justify the mere main- taining of the magnitude of sympathetic and parasympa- thetic influences on HR variability after training period in athletes or physically very well-fit individuals. EFFECTS ON HR POST-EXERCISE RECOVERY Another very important aspect addressed by the litera- ture over the last few years is post-exercise, maximal 95-97 and submaximal 98-100 HR recovery. HR behavior at the final transient of the exercise is another indicator of vagus nerve integrity. HR fall at the end of the exercise does not replace other measurements of cardiac autonomic activity, but it is a remarkable complement to a medical and/or physical as- sessment of an individual 101 . At the end of the exercise, special attention should be paid to HR behavior, as its lowering less than 12 beats per minute (bpm) if return to rest is active 97 or 18 bpm if pas- sive, in the supine position 102 , at the first recovery minute after a maximum-exercise test, represents an unfavorable prognosis for relative-risk of cardiovascular mortality in asymptomatic individuals and cardiopaths 95,97,102 , i.e., for both initial and

This review discusses the effects of aerobic training on heart rate and autonomic nervous system control.