Content uploaded by Claudio Gil Araujo
Author content
All content in this area was uploaded by Claudio Gil Araujo on Feb 01, 2014
Content may be subject to copyright.
Available via license: CC BY-NC 4.0
Content may be subject to copyright.
Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003 113
REVIEW
ARTICLE
logical mechanisms modulating HR during or after an ex-
ercise program are not totally clear, and further studies are
needed.
Key words: Training. Heart rate. Autonomic nervous system. Exer-
cise.
INTRODUCTION
The regular practice of physical exercises is an impor-
tant factor to reduce morbidity and mortality rates of car-
diovascular and all other conditions1,2; there also seems to
have further and independent benefits from the practice of
physical exercises and improvement of the aerobic condi-
tion3-6, which speaks for their being practiced more and
more frequently. The American Heart Association recom-
mends individuals to practice physical exercises in most
days of the week, every day if possible, with intensity rang-
ing from moderate to strenuous, according to their physi-
cal capability, for a period of 30 minutes or more7.
Even though moderate exercises enhance health condi-
tions, there are recent and consistent evidences that high
intensity or strenuous exercises have even more significant
positive effects on lipid profile8, reducing up to two times
mortality rates over a decade9-12.
Acute and chronic effects of physical exercises on the
human body have been targeted by many researches over
the last few decades13-18, and are identified as responses to
exercise, such as higher HR at the initial transient of the
exercise, and adjustments to training, with a lower HR for
the same intensity of submaximal exercise, respectively.
Because it is easy to measure, heart rate (HR) behavior
has been extensively studied under different exercise-re-
lated types and conditions. HR is primarily controlled by
direct activity of the autonomic nervous system (ANS),
through actions on its sympathetic and parasympathetic
branches on the sinus node autorhytmicity, especially rest-
ing vagal activity (parasympathetic), which is progressive-
ly inhibited since the exercise was started19, and sympa-
thetic when exercise intensity is further incremented (figure
1). Different mechanisms act to adjust HR at different mo-
ments of a physical exercise. For instance, the mechanism
through which HR raises on the first four seconds of a phys-
ical exercise has been extensively studied, including under
Effects of aerobic training on heart rate
Marcos B. Almeida1 and Claudio Gil S. Araújo1,2
1. Programa de Pós-Graduação em Educação Física da Universidade Gama
Filho – Rio de Janeiro, RJ.
2. Clinimex – Clínica de Medicina do Exercício – Rio de Janeiro, RJ.
Received in 27/11/02
Approved in 14/3/03
Correspondence to:
Dr. Claudio Gil S. Araújo
Clínica de Medicina do Exercício – Clinimex (www.clinimex.com.br)
Rua Siqueira Campos, 93/101
22031-070 – Rio de Janeiro, RJ
E-mail: cgaraujo@iis.com.br
ABSTRACT
Regular physical exercise 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 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-
ENGLISH VERSION
114 Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003
the effect of pharmacological block20-22, and is almost ex-
clusively mediated by vagal inhibition, with no significant
sympathetic role20, partly from different times of latency
from the two branches to this physiological stress.
HR variability was originally studied by Hon and Lee23
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 domain24-30, even with specificity enough for an
isolated assessment of cardiac vagal tone (parasympathet-
ic branch) in the transition from rest to dynamic exercise20.
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 risk31-37, thus representing an impor-
tant indicator of health status38,39. An isolated decrease of
HR variability reflects a two- to five-fold increase in the
relative mortality risk due to a cardiac event33,40; when as-
sociated to a significant decrease of baroreflex sensitivity
(< 3 ms/mmHg), this relative risk may reach a 7-fold in-
crease33. 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
uptake15,41,42, 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 exercise43, and are probably related to mechanisms
such as increase of venous return and myocardial contrac-
tility44. Furthermore, maximum O2 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 risk3,45,46 (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 system47. 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 condition3,45,46 and the autonomic
function48.
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
(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
Paras
y
mpathetic
S
y
mpathetic
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 risk49. 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 activity50, reducing diastolic depolar-
ization rate and prolonging duration of the cardiac cycle,
primarily on account of a proportionally longer diastole13.
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 activity51-55 or lower sym-
pathetic activity56. 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 variability57, one could specu-
late that those individuals could have better cardiovascular
adjustment upon training for having a better prior cardiac
vagal tone58. 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 node61.
A lower resting-HR can also be consequence of other
factors derived from a training program60, 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 contractility62. 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 conditioning62, 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 block22 showed
the exclusive role of the vagus nerve in HR response at the
initial transient of the exercise20,21, with predominance of
the vagal activity at rest that is gradually inhibited at sub-
maximal exercise63 both active and passive64-66, up to the
maximum level of exercise, when parasympathetic activi-
ty is apparently totally inhibited67, 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 node62, regardless of the lev-
el of intensity of the exercise68,69 and aerobic conditioning
of healthy individuals70,71. 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-
tivity72. 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 acidity73.
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 O2 uptake through aerobic train-
ing can lessen the age-related decrease of baroreflex sensi-
tivity78,79. A program of mild-intensity exercises would be
enough to show some improvement in the autonomic func-
tion of healthy adults80 or those with chronic heart fail-
ure81, even without direct training supervision82; 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 disease83 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 Freedson87, 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 improvements56,92.
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 Stein58 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 rest85,90, 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, maximal95-97
and submaximal98-100 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 individual101.
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 active97 or 18 bpm if pas-
sive, in the supine position102, at the first recovery minute
after a maximum-exercise test, represents an unfavorable
prognosis for relative-risk of cardiovascular mortality in
asymptomatic individuals and cardiopaths95,97,102, i.e., for
both initial and final transient, the smaller the HR varia-
tion, the higher the relative risk.
This stage of the exercise has been intensively investi-
gated over the last few years, but results still differ as to
the necessary time for total restore to post-exercise ANS
resting levels. The time for HR to fall to resting levels de-
pends on the interaction among autonomic functions, the
level of physical fitness103,104, and also on the intensity of
the exercise68,105. Recovery can take one hour after light or
moderate exercise105, four hours after long-duration aero-
bic exercise106, and even up to 24 hours after intense or
maximal exercise107. The mechanisms responsible for such
discrepancies as to the time needed for total HR post-exer-
cise recovery are not fully clear, and the following expla-
nations are currently considered as the most plausible: de-
creased vagal activity105,108-110, sympathetic overactivity107,111
or even increase in the activity of both ANS branches, re-
covering balance with slight vagal predominance25. Five
minutes after a moderate to intense exercise session, se-
rum norepinephrine is still higher than when in rest 110, sug-
gesting higher sympathetic activity at this stage. However,
one must take into account a latency time of about 2.5 min-
utes for serum norepinephrine to reach its peak112, leading
us to wonder that the five-minute recovery time of this study
could be too short. It seems that with aging, the time to
norepinephrine be removed from the blood is slower, and
cardiac rhythm remains faster for a longer time after the
exercise. The decrease of post-exercise norepinephrine con-
centration comes along HR decrease, but there is indica-
tion that at the beginning of recovery, vagal modulation is
primarily responsible for HR fall69,110.
Heart-transplanted individuals have a significantly slower
HR recovery at the first minute post-exercise when com-
pared to apparently healthy individuals113, endorsing the
Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003 117
idea from Perini et al.110. Physical training can increase the
delta between HR at the end of the exercise and at the be-
ginning of recovery, and eight weeks of training would be
enough to augment this difference within the first 30 sec-
onds post-exercise114, with no differences in outcome for
gender or age group115; however, such adaptation may be
lost in few weeks without training79,114. In children, recov-
ery may be faster than in young adults due to their higher
central cholinergic modulation116; there are differences for
elders as well, in whom decrease of post-exercise serum
norepinephrine takes longer117. Apparently, the time for total
restoration of ANS activities is inversely related to the max-
imum level of O2 uptake55,106, in spite of Arai et al.63 not
having found evidences in their results that indicated dif-
ferences in variables such as: gender63,118, position of sub-
ject on recovery (seated or supine), and level of physical
activity among healthy individuals63. When healthy indi-
viduals were compared to heart-failure or heart-transplanted
individuals, the former required shorter time for post-max-
imal exercise HR recovery; notwithstanding, HR variability
measured under frequency domain at the peak of the exer-
cise did not show differences among the groups, probably
a sign of complete inhibition of vagal activity at this stage67.
The groups of heart-failure and heart-transplanted individ-
uals had reduced their HR less than 10 bpm at the begin-
ning of the recovery stage, which is compatible to a prob-
able autonomic dysfunction and related to a high mortality
risk95-97.
CONCLUSIONS
As discussed in this review, HR variability has been stud-
ied at a number of trials over the last few years, especially
its relation to a higher risk of cardiovascular mortality, a
common finding in many of these trials. Vagal nerve activ-
ity (parasympathetic branch) is considered to be a cardio-
vascular protection factor; therefore, ANS dysfunction, par-
ticularly reduction of the cardiac vagal tone, translates in a
significant increase of cardiovascular mortality risk. It is
not clear if the regular practice of physical exercise can
significantly increase ANS function, as shown by some ev-
idences. Perhaps some of the changes that take place in
HR control at rest and at exercise submaximal levels are
consequence of intrinsic adaptations of the sinus node, or
derived from other physiological changes, such as the in-
crease of venous return and systolic volume, and improved
myocardial contractility; or peripheral, such as improved
oxygen extraction (oxygen arteriovenous difference) or en-
hanced O2 use to generate more work (mechanical efficien-
cy), causing HR to reduce to those (submaximal) required
levels.
Apparently, aerobically well-fit individuals present a
more effective autonomic activity than sedentary ones, and
there is indication that individuals with better cardiac va-
gal tone have a better response to aerobic training, which
lead us to question whether aerobically well-fit athletes have
a higher cardiac vagal tone due to training or those indi-
viduals with genetically higher cardiac vagal tone have a
higher potential to become elite athletes if properly trained.
Certainly, the large variety of HR measuring methods,
and the features and peculiarities of the samples and the
outlines used in each trial, have added to differences among
the results and their interpretations as to the effects of ex-
ercise and training on parasympathetic ANS and HR con-
trol.
In spite of the need of other studies on immediate and
late acute effects, and chronic effects of physical exercise
on the autonomic nervous system, especially of the para-
sympathetic component, identifying possible changes on
the cardiac vagal tone, some conclusions could be reached.
REFERENCES
1. Blair SN, Kohl 3rd HW, Barlow CE, Paffenbarger RS, Gibbons LW, Mac-
era CA. Changes in physical fitness and all-cause mortality. A prospec-
tive study of healthy and unhealthy men. JAMA 1995;273:1093-8.
2. Centers for Disease Control. Coronary heart disease attributable to sed-
entary life-style – selected states, 1988. JAMA 1990;264:1390-2.
3. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Ex-
ercise capacity and mortality among men referred for exercise testing. N
Engl J Med 2002;346:793-801.
4. Willians PT. Physical fitness and activity as separate heart disease risk
factors: a meta-analysis. Med Sci Sports Exerc 2001;5:754-61.
5. Erikssen G, Liestol K, Bjornholt J, Thaulow E, Sandvik L, Erikssen J.
Changes in physical fitness and changes in mortality. Lancet 1998;352:
759-62.
6. McGinnis JM, Foege WH. Actual causes of death in the United States.
JAMA 1993;270:2207-12.
7. Pearson TA, Blair SN, Daniels SR, Eckel RH, Fair JM, Fortmann SP, et
al. AHA guidelines for primary prevention of cardiovascular disease and
stroke: 2002 update. Consensus panel guide to comprehensive risk re-
duction for adult patients without coronary or other atherosclerotic vas-
cular diseases. Circulation 2002;106:388-91.
8. Kraus WE, Houmard JA, Duscha BD, Knetzger KJ, Wharton MB, Mc-
Cartney JS, et al. Effects of the amount and intensity of exercise on
plasma lipoproteins. N Engl J Med 2002;347:1483-92.
9. Paffenbarger RS, Lee IM. Physical activity and fitness for health and
longevity. Res Q Exerc Sport 1996;67:11-28.
10. Manson JE, Hu FB, Rich-Edwards JW, Colditz GA, Stampfer MJ, Wil-
lett WC, et al. A prospective study of walking as compared with vigor-
ous exercise in the prevention of coronary heart disease in women. N
Engl J Med 1999;341:650-8.
11. Manson JE, Greenland P, LaCroix AZ, Stefanick ML, Mouton CP, Ober-
man A, et al. Walking compared with vigorous exercise for the preven-
tion of cardiovascular events in women. N Engl J Med 2002;347:716-
25.
118 Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003
12. Tanasescu M, Leitzmann MF, Rimm EB, Willet WC, Stampfer MJ, Hu
FB. Exercise type and intensity in relation to coronary disease in men.
JAMA 2002;288:1994-2000.
13. Nottin S, Vinet A, Stecken F, N’Guyen LD, Ounissi F, Lecoq AM, Obert
P. Central and peripheral cardiovascular adaptations to exercise in en-
durance-trained children. Acta Physiol Scand 2002;175:85-92.
14. McGuirre DK, Levine BD, Williamson JW, Snell PG, Blomqvist CG,
Saltin B, et al. A 30-year follow-up of the Dallas Bed Rest and Training
Study. The effect of age on the cardiovascular response to exercise. Cir-
culation 2001;104:1350-7.
15. McGuirre DK, Levine BD, Williamson JW, Snell PG, Blomqvist CG,
Saltin B, et al. A 30-year follow-up of the Dallas Bed Rest and Training
Study. The effect of age on the cardiovascular adaptation to exercise.
Circulation 2001;104:1358-66.
16. Stratton JR, Levy WC, Cerqueira MD, Schwartz RS, Abrass IB. Cardio-
vascular responses to exercise. Effects of aging and exercise training in
healthy men. Circulation 1994;89:1648-55.
17. Nóbrega ACL, Williamson JW, Araújo CGS, Friedman DB. Heart rate
and blood pressure responses at the onset of dynamic exercise: effect of
Valsalva manoeuvre. Eur J Appl Physiol 1994;68:336-40.
18. Ekblom B, Astrand PO, Saltin B, Stenberg J, Wallstrom B. Effect of
training on circulatory response to exercise. J Appl Physiol 1968;24:
518-28.
19. Ekblom B, Hermansen L. Cardiac output in athletes. J Appl Physiol 1968;
25:619-25.
20. Araújo CGS, Nóbrega ACL, Castro CLB. Heart rate responses to deep
breathing and 4-seconds of exercise before and after pharmacological
blockade with atropine and propranolol. Clin Auton Res 1992;2:35-40.
21. Maciel BC, Gallo L Jr, Marin Neto JA, Lima Filho EC, Martins LE.
Autonomic nervous control of the heart rate during dynamic exercise in
normal man. Clin Sci (Colch) 1986;71:457-60.
22. Jose AD. Effect of combined sympathetic and parasympathetic block-
ade on heart rate and function in man. Am J Cardiol 1966;18:476-8.
23. Hon EH, Lee ST. Electronic evaluations of the fetal heart rate patterns
preceding fetal death: further observations. Am J Obstet Gynecol 1965;
87:814-826.
24. Moraes RS, Ferlin EL, Polanczyk CA, Rohde LE, Zaslavski L, Gross
JL, Ribeiro JP. Three-dimensional return map: a new tool for quantifica-
tion of heart rate variability. Auton Neurosci 2000;83:90-9.
25. Oida E, Moritani T, Yamori Y. Tone-entropy analysis on cardiac recov-
ery after dynamic exercise. J Appl Physiol 1997;82:1794-801.
26. European Society of Cardiology. 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 Electrophysiology. Circulation 1996;93:1043-65.
27. Marfella R, Guigliano D, di Maro G, Acampora R, Giunta R, D’Onofrio
F. The squatting test. A useful tool to assess both parasympathetic and
sympathetic involvement of the cardiovascular autonomic neuropathy
in diabetes. Diabetes 1994;43:607-12.
28. Castro CLB, Nóbrega ACL, Araújo CGS. Testes autonômicos cardio-
vasculares. Uma revisão crítica. Parte I. Arq Bras Cardiol 1992;59:75-
85.
29. Castro CLB, Nóbrega ACL, Araújo CGS. Testes autonômicos cardio-
vasculares. Uma revisão crítica. Parte II. Arq Bras Cardiol 1992;59:151-
8.
30. Wieling W, Borst C, Karemaker JM, Dunning AJ. Testing for autonomic
neuropathy: initial heart rate response to active and passive changes of
posture. Clin Physiol 1985;5: S5-23-7.
31. Tapanainen J, Thomsen P, Kober L, Torp-Pedersen C, Makikallio T, Still
A, et al. Fractal analysis of heart rate variability and mortality after an
acute myocardial infarction. Am J Cardiol 2002;90:347.
32. Bilchick KC, Fetics B, Djoukeng R, Fisher SG, Fletcher RD, Singh SN,
et al. Prognostic value of heart rate variability in chronic congestive heart
failure (Veterans Affairs’ Survival Trial of Antiarrhythmic Therapy in
Congestive Heart Failure). Am J Cardiol 2002;90:24-8.
33. La Rovere MT, Pinna GD, Hohnloser SH, Marcus FI, Mortara A, Noha-
ra R, et al. Baroreflex sensitivity and heart rate variability in the identi-
fication of patients at risk for life-threatening arrhythmias. Implications
for clinical trials. Circulation 2001;103:2072-7.
34. Colhoun HM, Francis DP, Rubens MB, Underwood SR, Fuller JH. The
association of heart rate variability with cardiovascular risk factors and
coronary artery calcification. A study in type 1 diabetic patients and the
general population. Diabetes Care 2001;24:1108-14.
35. Ribeiro AL, Moraes RS, Ribeiro JP, Ferlin EL, Torres RM, Oliveira E,
Rocha MO. Parasympathetic dysautonomia precedes left ventricular sys-
tolic dysfunction in Chagas disease. Am Heart J 2001;141:260-5.
36. Nolan J, Batin PD, Andrews R, Lindsay SJ, Brooksby P, Mullen M, et
al. Prospective study of heart rate variability and mortality in chronic
heart failure. Results of the United Kingdom Heart Failure Evaluation
Assessment of Risk Trial (UK-Heart). Circulation 1998;98:1510-6.
37. Singh JP, Larson MG, Tsuji H, Evans JC, O’Donnell CJ, Levy D. Re-
duced heart rate variability and new-onset hypertension. Insights into
pathogenesis of hypertension: The Framingham Heart Study. Hyperten-
sion 1998;32:293-7.
38. Kikuya M, Hozawa A, Ohokubo T, Tsuji I, Michimata M, Matsubara M,
et al. Prognostic significance of blood pressure and heart rate variabili-
ties. The Ohasama Study. Hypertension 2000;36:901-6.
39. Moser M, Lehofer M, Sedminek A, Lux M, Zapotoczky HG, Kenner T,
et al. Heart rate variability as a prognostic tool in cardiology. A contri-
bution to the problem from a theoretical point of view. Circulation 1994;
90:1078-82.
40. La Rovere MT, Bigger Jr JT, Marcus FI, Mortara A, Schwartz PJ, for the
ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction)
investigators. Baroreflex sensitivity and heart rate variability in predic-
tion of total cardiac mortality after myocardial infarction. Lancet 1998;
351:478-84.
41. Seal DR, Chase PB. Influence of physical training on heart rate variabil-
ity and baroreflex circulatory control. J Appl Physiol 1989;66:1886-95.
42. Blomqvist CG, Saltin B. Cardiovascular adaptations to physical train-
ing. Ann Rev Ph ysiol 1983;45:169-89.
43. Fox EL, Bartels RL, Billings CE, O’Brien R, Bason R, Mathews DK.
Frequency and duration of interval programs and changes in aerobic
power. J Appl Physiol 1975;38:481-4.
44. Yoshiga CC, Higuchi M. Heart rate is lower during ergometer rowing
than during treadmill running. Eur J Appl Physiol 2002;87:97-100.
45. Kavanagh T, Mertens DJ, Hamm LF, Beyene J, Kennedy J, Corey P, et
al. Prediction of long-term prognosis in 12169 men referred for cardiac
rehabilitation. Circulation 2002;106:666-71.
46. Laukkanen JA, Lakka TA, Rauramaa R, Kuhanen R, Venäläinen JM,
Salonen R, et al. Cardiovascular fitness as a predictor of mortality in
men. Arch Intern Med 2001;161:825-31.
47. Stein R, Moraes RS, Cavalcanti AV, Ferlin EL, Zimerman LI, Ribeiro
JP. Atrial automaticity and atrioventricular conduction in athletes: con-
tribution of autonomic regulation. Eur J Appl Physiol 2000;82:155-7.
48. La Rovere MT, Bersano C, Gnemmi M, Specchia G, Schwartz PJ. Exer-
cise-induced increase in baroreflex sensitivity predicts improved prog-
nosis after myocardial infarction. Circulation 2002;106:945-9.
49. Greenland P, Daviglus ML, Dyer AR, Liu K, Huang CF, Goldberger JJ,
et al. Resting heart rate is a risk factor for cardiovascular and noncardio-
vascular mortality: the Chicago Heart Association Detection Project in
Industry. Am J Epidemiol 1999;149:853-62.
Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003 119
50. Jensen-Urstad K, Saltin B, Ericson M, Storck N, Jensen-Urstad M. Pro-
nounced resting bradycardia in male elite runners is associated with high
heart variability. Scand J Med Sci Sports 1997;7:274-8.
51. Aubert AE, Beckers F, Ramaekers D. Short-term heart rate variability in
young athletes. J Cardiol 2001;37: S85-8.
52. Spalding TW, Jeffers LS, Porges SW, Hatfield BD. Vagal and cardiac
reactivity to psychological stressors in trained and untrained men. Med
Sci Sports Exerc 2000;32:581-91.
53. Shin K, Minamitani H, Onishi S, Yamazaki H, Lee M. Autonomic dif-
ferences between athletes and nonathletes: spectral analysis approach.
Med Sci Sports Exerc 1997;29:1482-90.
54. Shin K, Minamitani H, Onishi S, Yamazaki H, Lee M. The power spec-
tral analysis of heart rate variability in athletes during dynamic exercise
– part I. Clin Cardiol 1995;18:583-6.
55. Dixon E, Kamath MV, McCartney N, Fallen E. Neural regulation of the
heart rate in endurance athletes and sedentary controls. Cardiovasc Res
1992;26:713-9.
56. Chacon-Mikahil MPT, Forti VAM, Catai AM, Szrajer JS, Golfetti R,
Martins LEB, et al. Cardiorespiratory adaptations induced by aerobic
training in middle-age men: the importance of a decrease in sympathetic
stimulation for the contribution of dynamic exercise tachycardia. Bra-
zilian J Med Biol Res 1998;31:705-12.
57. Singh JP, Larson MG, O’Donnell CJ, Tsuji H, Evans JC, Levy D. Heri-
tability of the heart rate variability. The Framingham Heart Study. Cir-
culation 1999;99:2251-4.
58. Boutcher SH, Stein P. Association between heart rate variability and train-
ing response in sedentary middle-aged men. Eur J Appl Physiol 1995;
70:75-80.
59. Uusitalo ALT, Uusitalo AJ, Ruscko HK. Exhaustive endurance training
for 6-9 weeks did not change in intrinsic heart rate and cardiac autonom-
ic modulation in female athletes. Int J Sports Med 1998;19:532-40.
60. Bonaduce D, Petretta M, Cavallaro V, Apicella C, Ianniciello A, Ro-
mano M, et al. Intensive training and cardiac autonomic control in high
level athletes. Med Sci Sports Exerc 1998;30:691-6.
61. Catai AM, Chacon-Mikahil MP, Martinelli FS, Forti VAM, Silva E,
Golfetti R, et al. Effects of aerobic exercise training on heart rate vari-
ability during wakefulness and sleep and cardiorespiratory responses of
young and middle-age healthy men. Brazilian J Med Biol Res 2002;35:
741-52.
62. Clausen JP. Effect of physical training on cardiovascular adjustments to
exercise in man. Physiol Rev 1977;57:779-815.
63. Arai Y, Saul JP, Albrecht P, Hartley LH, Lilly LS, Cohen RJ, Colucci
WS. Modulation of cardiac autonomic activity during and immediately
after exercise. Am J Physiol 1989;256:H132-41.
64. Nurhayati Y, Boutcher SH. Cardiovascular response to passive cycle
exercise. Med Sci Sports Exerc 1998;30:234-8.
65. Nóbrega ACL, Williamson JW, Friedman DB, Araújo CGS, Mitchell
JH. Cardiovascular responses to active and passive cycling movements.
Med Sci Sports Exerc 1994;26:709-14.
66. Nóbrega ACL, Araújo CGS. Heart rate transient at the onset of active
and passive dynamic exercise. Med Sci Sports Exerc 1993;25:37-41.
67. Alonso DO, Forjaz CLM, Rezende LO, Braga AMFW, Barretto ACP,
Negrão CE, et al. Comportamento da freqüência cardíaca e da sua varia-
bilidade durante as diferentes fases do exercício físico progressivo. Arq
Bras Cardiol 1998;71:787-92.
68. Baum K, Ebfeld D, Leyk D, Stegemann J. Blood pressure and heart rate
during rest-exercise and exercise-rest transitions. Eur J Appl Physiol 1992;
64:134-8.
69. Araújo CGS. Fast “on” and “off” heart rate transients at different bicy-
cle exercise levels. Int J Sports Med 1985;6:68-73.
70. Araújo CGS, Nóbrega ACL, Castro CLB. Vagal activity: effect of age,
sex and physical pattern. Brazilian J Med Biol Res 1989;22:909-11.
71. Borst C, Wieling W, van Brederode JFM, Hond A, de Rijk LG, Dunning
AJ. Mechanisms of initial heart rate response to postural change. Am J
Physiol 1982;243:H676-81.
72. Nóbrega ACL, Castro CLB, Araújo CGS. Relative roles of the sympa-
thetic and parasympathetic systems in the 4-s exercise test. Brazilian J
Med Biol Res 1990;23:1259-62.
73. Araújo CGS. Fisiologia do exercício. In: Araújo WB, editor. Ergometria
e cardiologia desportiva. Rio de Janeiro: Medsi, 1986;1-57.
74. Tulppo MP, Mäkikallio TH, Seppänen T, Laukkanen RT, Huikuri HV.
Vagal modulation of heart rate during exercise: effects of age and phys-
ical fitness. Am J Physiol 1998;274:H424-9.
75. Goldsmith RL, Bigger JT, Bloofield DM, Steinman RC. Physical fitness
as a determinant of vagal modulation. Med Sci Sports Exerc 1997;29:
812-7.
76. Migliaro ER, Contreras P, Bech S, Etxagibel A, Castro M, Ricca R, et
al. Relative influence of age, resting heart rate and sedentary life style in
short-term analysis of heart rate variability. Brazilian J Med Biol Res
2001;34:493-500.
77. Byrne EA, Fleg JL, Vaitkevicius PV, Wright J, Porges SW. Role of aer-
obic capacity and body mass index in the age-associated decline in heart
rate variability. J Appl Physiol 1996;81:743-50.
78. Hunt BE, Farquhar WB, Taylor JA. Does reduced vascular stiffening
fully explain preserved cardiovagal baroreflex function in older, physi-
cally active men? Circulation 2001;103:2424-7.
79. Frederiks J, Swenne CA, Bruschke AVG, van der Velde ET, Maan AC,
Tenvoorde BJ, et al. Correlated neurocardiologic and fitness changes in
athletes interrupting training. Med Sci Sports Exerc 2000;32:571-5.
80. Uusitalo ALT, Laitinen T, Väisänen SB, Länsimies E, Rauramaa R. Ef-
fects of endurance training on heart rate and blood pressure variability.
Cli Physiol & Func Im 2002;22:173-9.
81. Malfatto G, Branzi G, Riva B, Sala L, Leonetti G, Facchini M. Recov-
ery of cardiac autonomic responsiveness with low-intensity physical train-
ing in patients with chronic heart failure. Eur J Heart Fail 2002;4:159-
66.
82. Radaelli A, Coats AJ, Leuzzi S, Piepoli M, Meyer TE, Calciati A, et al.
Physical training enhances sympathetic and parasympathetic control of
heart rate and peripheral vessels in chronic heart failure. Clin Sci (Colch)
1996;91: S92-4.
83. Iellamo F, Legramante JM, Massaro M, Raimondi G, Galante A. Effects
of a residential exercise training on baroreflex sensitivity and heart rate
variability in patients with coronary artery disease. A randomized, con-
trolled study. Circulation 2000;102:2588-92.
84. Oya M, Itoh H, Kato K, Tanabe K, Murayama M. Effects of exercise
training on the recovery of the autonomic nervous system and exercise
capacity after acute myocardial infarction. Jpn Circ J 1999;63:843-8.
85. La Rovere MT, Mortara A, Sandrone G, Lombardi F. Autonomic ner-
vous system adaptations to short-term exercise training. Chest 1992;101:
299S-303.
86. Seals DR, Hurley BF, Hagberg JM, Schultz J, Linder BJ, Natter L, et al.
Effects of training on systolic time intervals at rest and during isometric
exercise in men and women 61 to 64 years old. Am J Cardiol 1985;55:
797-800.
87. Melanson EL, Freedson OS. The effect of endurance training on resting
heart rate variability in sedentary adult males. Eur J Appl Physiol 2001;
85:442-9.
88. Stein PK, Ehsani AA, Domitrovich PP, Kleiger RE, Rottman JN. Effect
of exercise training on heart rate variability in healthy older adults. Am
Heart J 1999;138:567-76.
120 Rev Bras Med Esporte _ Vol. 9, Nº 2 – Mar/Abr, 2003
89. Al-Ani M, Munir SM, White M, Towend J, Coote JH. Changes in R-R
variability before and after endurance training measured by power spec-
tral analysis and by the effect of isometric muscle contraction. Eur J
Appl Physiol 1996;74:397-403.
90. Gallo Jr L, Maciel BC, Marin-Neto JA, Martins LEB. Sympathetic and
parasympathetic changes in heart rate control during dynamic exercise
induced by endurance training in man. Brazilian J Med Biol Res 1989;
22:631-43.
91. Levy WC, Cerquera MD, Harp GD, Johannessen KA, Abrass IB,
Schwartz RS, et al. Effect of endurance exercise training on heart rate
variability at rest in healthy young and older men. Am J Cardiol 1998;
82:1236-41.
92. O’Sullivan SE, Bell C. Training reduces autonomic cardiovascular re-
sponses to both exercise-dependent and -independent stimuli in humans.
Auton Neurosci 2001;91:76-84.
93. Duru F, Candinas R, Dziekan G, Goebbels U, Myers J, Dubach P. Ef-
fect of exercise training on heart rate variability in patients with new-
onset left ventricular dysfunction after myocardial infarction. Am Heart
J 2000; 140:157-61.
94. Loimaala A, Huikuri H, Oja P, Pasanen M, Vuori I. Controled 5-mo
aerobic training improves heart rate but not heart rate variability or
baroreflex sensitivity. J Appl Physiol 2000;89:1825-9.
95. Nishime OE, Cole CR, Blackstone EH, Pashkow FJ, Lauer MS. Heart
rate recovery and treadmill exercise score as predictors of mortality in
patients referred for exercise ECG. JAMA 2000;284:1392-8.
96. Pierpont GL, Stolpman DR, Gornick CC. Heart rate recovery as an
index of parasympathetic activity. J Auton Nerv Syst 2000;80:169-74.
97. Cole CR, Blackstone EH, Pashkow FJ, Snader CE, Lauer MS. Heart
rate recovery immediately after exercise as a predictor of mortality. N
Engl J Med 1999;341:1351-7.
98. Morshedi-Meibodi A, Larson MG, Levy D, O’Donnel CJ, Vasan R.
Heart rate recovery after treadmill exercise testing and risk of cardio-
vascular disease events (The Framingham Heart Study). Am J Cardiol
2002;90: 848-52.
99. Cole CR, Foody JM, Blackstone EH, Lauer MS. Heart rate recovery
after submaximal exercise testing as a predictor of mortality in a car-
diovascularly healthy cohort. Ann Intern Med 2000;132:552-5.
100. Lauer MS, Francis GS, Okin PM, Pashkow FJ, Snader CE, Marwick
TH. Impaired chronotropic response to exercise stress testing as a pre-
dictor of mortality. JAMA 1999;281:524-9.
101. Shetler K, Marcus R, Froelicher VF, Vora S, Kalisetti D, Prakash M, et
al. Heart rate recovery: validation and methodologic issues. J Am Coll
Cardiol 2001;38:1980-7.
102. Watanabe J, Thamilarasan M, Blackstone EH, Thomas JD, Lauer MS.
Heart rate recovery immediately after treadmill exercise and left ven-
tricular systolic dysfunction as predictors of mortality. The case of stress
echocardiography. Circulation 2001;104:1991-6.
103. Hatfield BD, Spalding TW, Santa Maria DL, Porges SW, Potts JT, Byr-
ne EA, et al. Respiratory sinus arrhythmia during exercise in aerobical-
ly trained and untrained men. Med Sci Sports Exerc 1998;30:206-14.
104. Darr KC, Bassett DR, Morgan BJ, Thomas DP. Effects of age and train-
ing status on heart rate recovery after peak exercise. Am J Physiol 1988;
254:H340-3.
105. Terziotti P, Schena F, Gulli G, Cevese A. Post-exercise recovery of
autonomic cardiovascular control: a study by spectrum and cross-spec-
trum analysis in humans. Eur J Appl Physiol 2001;84:187-94.
106. Hautala A, Tulppo MP, Mäkikallio TH, Laukkanen R, Nissilä S, Huikuri
HV. Changes in cardiac autonomic regulation after prolonged maximal
exercise. Clin Physiol 2001;21:238-45.
107. Furlan R, Piazza S, Dell’Orto S, Gentile E, Cerutti S, Pagani M, Mal-
liani A. Early and late effects of exercise and athletic training on neural
mechanisms controlling heart rate. Cardiovasc Res 1993;27:482-8.
108. Melanson EL. Resting heart rate variability in men varying in habitual
physical activity. Med Sci Sports Exerc 2000;32:1894-901.
109. Imai K, Sato H, Hori M, Kusuoka H, Ozaki H, Yokoyama H, et al.
Vagally mediated heart rate recovery after exercise is accelerated in
athletes but blunted in patients with chronic heart failure. J Am Coll
Cardiol 1994;24:1529-35.
110. Perini R, Orizio C, Comandè A, Castellano M, Beschi M, Veicsteinas
A. Plasma norepinephrine and heart rate dynamics during recovery from
submaximal exercise in men. Eur J Appl Physiol 1989;58:879-83.
111. Dilaveris PE, Zervopoulos GA, Michaelides AP, Sideris SK, Psomada-
ki ZD, Gialafos EJ, et al. Ischemia-induced reflex sympathoexcitation
during the recovery period after maximal treadmill exercise testing.
Clin Cardiol 1998;21:585-90.
112. Watson RDS, Hamilton CA, Jones DH, Reid JL, Stallard TJ, Littler
WA. Sequential changes in plasma noradrenaline during bicycle exer-
cise. Clin Sci 1980;58:37-43.
113. Desai MY, Peña-Almaguer E, Mannting F. Abnormal heart rate recov-
ery after exercise as a reflection of abnormal chronotropic response.
Am J Cardiol 2001;87:1164-9.
114. Sugawara J, Murakami H, Maeda S, Kuno S, Matsuda M. Change in
post-exercise vagal reactivation with exercise training and detraining
in young men. Eur J Appl Physiol 2001;85:259-63.
115. Hao SC, Chai A, Kligfield P. Heart rate recovery response to symptom-
limited treadmill exercise after cardiac rehabilitation in patients with
coronary artery disease with and without recent events. Am J Cardiol
2002;90:763-5.
116. Ohuchi H, Suzuki, Yasuda K, Arakaki Y, Echigo S, Kamiya T. Heart
rate recovery after exercise and cardiac autonomic nervous activity in
children. Pediatr Res 2000;47:329-35.
117. Tasaki H, Serita T, Irita A, Hano O, Iliev I, Ueyama C, et al. A 15-year
longitudinal follow-up study of heart rate and heart rate variability in
healthy elderly persons. J Gerontol 2000;55A:M744-9.
118. Carter III R, Watenpaugh DE, Smith ML. Genome and hormones: gen-
der differences in physiology selected contribution: gender differences
in cardiovascular regulation during recovery from exercise. J Appl Phys-
iol 2001;91:1902-7.
