Suppression of heart rate variability after supramaximal exertion

Abstract

Wingate test is short anaerobic exercise, performed with maximal power, whereas aerobic exercise at 85% maximal heart rate (HR(max)) may be performed for long period. Sustained HR elevations and changes in autonomic activity indices have been observed after latter kind of exercise. Several studies reported reduction in mean interval between consecutive R peaks in ECG (RRI) 1 h after Wingate test; however, underlying changes in autonomic activity remain elusive. In eight young males, RRI and heart rate variability (HRV) were measured daily over two 5-day trials. Subjects exercised on third day of each trial, measurements were taken 1 h after (i) two consecutive 30-s bouts of Wingate tests or (ii) after a 30-min exercise at 85% HR(max), with subjects in supine rest and breathing either spontaneously or at controlled rates of 6 and 15 breaths / min. RRI was significantly shorter after Wingate and submaximal exercise, reduction of high- and low-frequency components of HRV attained reliability only after Wingate tests. This pattern remained preserved for three modes of breathing: spontaneous, 6 and 15 breaths /min. After 24 and 48 h, no exercise effects were traceable. We hypothesize that (i) anaerobic exertion is followed by sustained inhibition of vagal activity, (ii) parasympathetic system plays dominant role in mediating suppression of high- and low-HRV frequency components during postexercise recovery, (iii) degree of alteration of autonomic activity caused by anaerobic and strenuous aerobic exercise may be similar and (iv) normalization of vagal activity precedes normalization of sympathetic cardiac nerves activity during final stage of postexercise recovery.

Full text

Suppression of heart rate variability after supramaximal
exertion
W. Niewiadomski
1
,A.Ga˛ siorowska
1
, B. Krauss
2
, A. Mro
´z
2
and G. Cybulski
1
1
Department of Applied Physiology, Medical Research Center, Polish Academy of Sciences, Warsaw, and
2
Department of Biochemistry and Physiology, Academy
of Physical Education, Warsaw, Poland
Correspondence
Wiktor Niewiadomski, Department of Applied
Physiology, Medical Research Center, Polish
Academy of Sciences, 5 Pawinski St. 02-106
Warsaw, Poland
E-mail: wiktorn@cmdik.pan.pl
Accepted for publication
Received 20 October 2006;
accepted 14 June 2007
Key words
autonomic activity; controlled breathing; heart rate;
postexercise recovery; submaximal exercise
Summary
Wingate test is short anaerobic exercise, performed with maximal power, whereas
aerobic exercise at 85% maximal heart rate (HR
max
) may be performed for long
period. Sustained HR elevations and changes in autonomic activity indices have been
observed after latter kind of exercise. Several studies reported reduction in mean
interval between consecutive R peaks in ECG (RRI) 1 h after Wingate test; however,
underlying changes in autonomic activity remain elusive. In eight young males, RRI
and heart rate variability (HRV) were measured daily over two 5-day trials. Subjects
exercised on third day of each trial, measurements were taken 1 h after (i) two
consecutive 30-s bouts of Wingate tests or (ii) after a 30-min exercise at 85%
HR
max
, with subjects in supine rest and breathing either spontaneously or at
controlled rates of 6 and 15 breaths ⁄min. RRI was significantly shorter after Wingate
and submaximal exercise, reduction of high- and low-frequency components of
HRV attained reliability only after Wingate tests. This pattern remained preserved for
three modes of breathing: spontaneous, 6 and 15 breaths ⁄min. After 24 and 48 h,
no exercise effects were traceable. We hypothesize that (i) anaerobic exertion is
followed by sustained inhibition of vagal activity, (ii) parasympathetic system plays
dominant role in mediating suppression of high- and low-HRV frequency
components during postexercise recovery, (iii) degree of alteration of autonomic
activity caused by anaerobic and strenuous aerobic exercise may be similar and (iv)
normalization of vagal activity precedes normalization of sympathetic cardiac nerves
activity during final stage of postexercise recovery.
Introduction
The risk of cardiac events, including sudden death, increases not
only during vigorous exercise, but also during periods of
recovery (Cobb & Weaver, 1986; Mittleman et al., 1993; Willich
et al., 1993; Albert et al., 2000). Autonomic activity seems to
play an important role in determining the outcome of exercise
induced circulatory challenges. Numerous studies, mostly using
induced cardiac ischaemia in exercising dogs, have demonstra-
ted that parasympathetic activity protects against ventricular
fibrillation (VF), while sympathetic activity increases the risk of
VF (Schwartz et al., 1992; Schwartz, 1998; Adamson & Vanoli,
2001).
Sustained changes in autonomic activity, evidence in a
lasting elevation of HR at least 1-h postexercise, were
observed after intensive submaximal (Floras et al., 1989; Hara
& Floras, 1995; Forjaz et al., 1998) or maximal incremental
exercise (Coats et al., 1989; Piepoli et al., 1994). Sustained
elevation of HR was observed not only after vigorous aerobic
exertion, but also after 30- to 75-s anaerobic exercise,
performed as single or multiple Wingate tests (Hussain et al.,
1996; Hoffman et al., 1997; Falk et al., 1998; Backx et al.,
2000). Wingate test is the most widely used anaerobic
performance test, and its result is known to be a valid
predictor of the performance of an array of anaerobic
exercises, be it running, swimming or skating. During the
Wingate test, the subject maintains highest possible pedalling
velocity against resistance set individually in a manner, known
to maximize the subjects mean power attained during the
test. Typical 30-s Wingate tests duration has been chosen for
being sufficiently long to allow for developing the maximal
glycolytic power, and sufficiently short for maintaining
maximal effort until the end of test (Inbar et al., 1996;
Dotan, 2006; Micklewright et al., 2006).
Clin Physiol Funct Imaging (2007) 27, pp309–319 doi: 10.1111/j.1475-097X.2007.00753.x
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319 309

Analysis of heart rate variability (HRV) both in frequency and
time domain offers insights into autonomic activity. Total
power of HRV, equal to its variance or SD
2
, has been used as a
measure of tonic parasympathetic activity. More specific indices
of this activity are part of the total power distributed in the
range of high frequencies (typically 0Æ15–0Æ4 Hz), denoted HF
and RMSSD – time domain index – reflecting fast beat-to-beat
changes of HR. It still remains controversial whether power
distributed in the range of low frequencies (typically 0Æ04–
0Æ15 Hz), termed LF, may serve as an index of sympathetic
activity (Eckberg, 1997).
Only few studies have examined postexercise HRV during a
period extended over 1 h after exercise cessation. Oida et al.
(1997) found HRV attenuation 45 min after a 30 min-lasting
exercise at 70% of maximal oxygen uptake level. Furlan et al.
(1993) reported reduction of HRV 1-h postexercise, but the
exercise training protocol was not specified. Legramante et al.
(2002) noticed no change at that time after maximal incre-
mental exercise, whereas Mourot et al. (2004) found signifi-
cantly reduced HRV 1 h after vigorous exercise.
As long-term changes in HRV have not been evaluated after
anaerobic effort, we examined HRV after the Wingate tests.
Our primary aim was to determine the sustained modification
of HRV at 1, 24 and 48 h after exercise; 48 h was the longest
time point of recovery, for which alterations in HRV have
been noticed to date (Hautala et al., 2001; Mourot et al.,
2004).
The effects of Wingate tests were then compared with those
of vigorous aerobic exercise at 85% HR
max
, which lasted for
30 min. These two types of exercise cause sustained postexercise
HR elevation. The Wingate test is almost completely anaerobic
and performed with maximal power, which rapidly declines
towards the end of the test. In contrast, exercise at 85% HR
max
is
predominately aerobic and may be performed at this intensity
for a long period (Meyer et al., 1999). Respiratory arrhythmia is
an important component of HRV and amplitude of respiratory
arrhythmia strongly depends on breathing frequency (Brown
et al., 1993). Therefore, beside measurements during sponta-
neous breathing, we also intended to obtain standardized HRV
measurement during phases of controlled breathing rates at 6
and 15 breaths ⁄min.
We hypothesized that, despite its short duration, anaerobic
effort should be followed by marked reduction of HRV, parallel
to prolonged reduction of RRI, observed by others, analogously
to prolonged reduction of RRI and HRV seen after vigorous
aerobic exercise.
Methods
Subjects
Eight healthy, young male students of physical education
participated in this study. They gave their written consent,
and the study protocol was approved by Ethical Committee of
Medical Research Center in Warsaw.
Preliminary testing
Before commencing with the experimental protocol, anthrop-
ometric data were collected, and peak oxygen uptake and peak
heart rate for each subject were determined.
For this purpose, the subjects undertook a progressive
exercise test on a mechanically braked cycle ergometer (Monark
884 E, Monark Exercise AB, Vansbro, Sweden). They began
pedalling at 60 W for 3 min, and then the exercise load was
increased by 30 W every 3 min. The test was continued until
volitional exhaustion.
Oxygen uptake was determined for each successive 10-s
period (V
max
29, Sensormedics, VIASYS Healthcare Inc., Yorba
Linda, CA, USA). The last 3 min before test termination were
used for peak oxygen consumption. Average value from every
60 s within these 3 min was calculated and the greatest value
was taken as the peak oxygen consumption. Heart rate was
monitored using a heart rate monitor (Team Polar, Polar Electro
Oy, Kempele, Finland) and power output was calculated by
using a PC software
MCE
v. 4Æ5 (JBA Z. Staniak, Warszawa,
Poland).
Experimental protocol
The subjectsHR and HRV were examined in the late morning
each day during two 5-day trials, separated by 5-day interval
(Fig. 1a). During the first 5-day trial, a Wingate test was
performed on day 3. Similarly, during the second 5-day trial,
the subjects performed 30-min submaximal exercise at 85%
HR
max
intensity on a cycle ergometer, also on the third day.
After both types of exercise, subjects recovered for 1 h before
ECG measurements were taken. During this break, they were
allowed to walk, sit, to drink modest amount of non-caffeinated
fluid but no food intake. They were also asked to avoid intensive
physical or mental activity.
Before ECG measurements, subjects rested supine for 10 min
and then remained in the same body position during measure-
ment. The subjects performed the following sequence of
breathing modes: (i) spontaneous breathing – 10 min, (ii)
controlled breathing at 15 breathes ⁄min rate – 3 min, (iii)
spontaneous breathing – 2 min, (iv) controlled breathing at 6
breathes ⁄min rate – 3 min. The period between 4th and 9th
minute of spontaneous breathing and the 3-min interval of
controlled breathing were analysed (Fig. 1b).
Wingate tests were performed by using cycle ergometer
(Monark 884 E) with sensors affixed to the flywheel. Data were
collected and two performance indices – mean and peak power
– commonly used in Wingate test were calculated with the
software package
MCE
v. 4Æ0 (JBA, Zb. Staniak). Wingate tests
were preceded by 5-min warming-up at 50 W. Immediately
after the warming-up period, the subjects performed two 30-s
Wingate tests. The two tests were separated by 3 min of active
recovery (cycling without resistance). Standard weight resist-
ance was applied, corresponding to 7Æ5% subjects body weight
(Inbar et al., 1996). During tests, the subjects were encouraged
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
310

to pedal against resistance at the highest possible velocity and to
maintain it to the test end. Following the second Wingate test,
the subjects had 6 min of active recovery.
Instrumentation and signal analysis
During both types of exercises, HR was continuously monitored
and recorded using a Polar Vantage heart rate monitor (Polar
Electro Oy).
During measurements performed in supine rest, ECG
measurements were performed in supine rest using lead II
of a cardiotachometer (CTK-3011, Temed, Poland). Flow of
respiratory air was recorded continuously by a Flow
Transducer Interface equipped with Fleisch gauge (Medikro
Oy, Kuopio, Finland) and analogue signals were digitized at a
sampling rate of 200 Hz (WinAcq data acquisition system,
Absolute Aliens Oy, Turku, Finland), computer stored and
processed by
WINCPRS
software (Absolute Aliens Oy). R peaks
were software detected and R peak position markers were
displayed superimposed on ECG signal. Markers of errone-
ously detected or missed R peaks were properly edited, and
RR intervals, time and frequency indices of HRV were
calculated. Respiratory air flow recordings were transformed
into respiratory volume curves, parameters of breathing cycles
were software determined and mean frequency of breathing
was calculated. Spectral analyses of HRV were performed with
Fast Fourier Transformation (FFT) methods. Before FFT, the
linear trend was removed, signal linearly interpolated and
resampled with sampling rate of 5 samples ⁄s. Signal was
windowed by using Hanning window function. The spectrum
was smoothed by a triangular window over the frequency
range of 0Æ01 Hz.
Blood pressure measurements were conducted using an
automatic oscillometric sphygmomanometer, with cuff placed
upon brachial artery during spontaneous breathing.
Data analysis
The following indices were calculated:
RRI (ms) ¼mean of all normal RR intervals.
Time-domain indices of HRV calculated for all three breathing
modes:
SDNN (ms) ¼SD of normal RR intervals,
RMSSD (ms) ¼the square root of the mean of the sum of
the squares of differences between
adjacent normal RR intervals.
Frequency domain indices of HRV calculated:
(a) for spontaneous breathing
HF ðms2Þ¼power in the 0.15-0.40 Hz frequency band
LFðms2Þ¼power in the 0.04-0.15 Hz frequency band
(b) for controlled breathing at 15 breaths ⁄min
RF15ðms2Þ¼power in the 0.23-0.27 Hz frequency band,
centered at respiratory frequency (0.25 Hz),
(c) for controlled breathing at 6 breaths ⁄min
RF6ðms2Þ¼power in the 0.08-0.12 Hz frequency band,
centered at respiratory frequency (0.1 Hz).
We introduced RF15 and RF6 as frequency-domain HRV
indices tailored to measure power of respiratory peaks.
Although these frequency bands were located either in HF
range or in LF range for 15 breaths ⁄min and 6 breaths ⁄min,
respectively, respiratory peaks during controlled breathing were
much narrower than HF and LF ranges. Therefore, the values of
DAY 1 DAY 5
DAY 1 DAY 5
TRIAL
(a)
(b)
I
DAY 3
1 h
DAY 2 DAY 4
1 2 RECOVERY 3 4 5
85% HR
max
30’
TRIAL II
DAY 3
DAY 2 DAY 4
1 2 4 5
RECOVERY 3
WINGATE TESTS
1 h
SEQUENCE OF BREATHING MODES
10’ 13’ 15’ 18’
15 SP 6SP
HRV
9’4’0’
HRV HRV
Figure 1 Experimental protocol. Heart rate
variability (HRV) – period used for HRV
measurement; SP – spontaneous breathing;
15:15 breaths ⁄min; 6:6 breaths ⁄min.
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
311

RF15 and RF6 depended primarily on the amplitude of
respiratory modulation of HR, and HRV peaks of possibly
non-respiratory origin located beyond well-defined band
around respiratory frequency were filtered out.
Statistical analysis
Two-way ANOVA with repeated measurements was used to
evaluate the effect of exercise type (submaximal versus Wingate
tests) and of time (day of 5-day trial) on RRI and HRV indices.
P<0Æ05 was assumed as the threshold for statistical significance.
The Newman–Keuls post hoc analysis was performed when
significant factor effects or their interactions were detected.
Where appropriate data were transformed using logarithmic
transformation to induce normality and improvement in
normality was assessed using Normal Probability Plot.
Results
Subjects and graded exercise test performance
Anthropological data of subjects and results of graded exercise
test are shown in Table 1. It is very likely that VO
2peak
determined here attained VO
2max
because all but one subjects
fulfilled two, out of three conditions of VO
2max
attainment
criterion (Duncan et al., 1997). Peak HR was >200 minus age in
seven subjects and the peak respiratory quotient (RQ) was >1Æ1
in all subjects. Blood lactate was not measured.
Wingate tests performance
Mean and peak power were 729 ± 154 W and 901 ± 210 W in
the first test, and 608 ± 177 W and 877 ± 249 W in the second
test. HR achieved at the end of second Wingate test was 185 ± 5
bpm, which was significantly higher than the 85% HR
max
main-
tained during submaximal exercise (161 ± 9 bpm; P<0Æ0001).
Breathing frequency
During spontaneous breathing, a wide range of breathing
frequencies was observed: from 8Æ4 breaths ⁄min (0Æ14 Hz) to
22 breaths ⁄min (0Æ37 Hz), with the mean breathing frequency
close to 16 breaths ⁄min (0Æ27 Hz). Hence, spontaneous
breathing test was performed at some higher average breathing
frequency than controlled breathing test (0Æ25 Hz). During
controlled breathing tests, subjects maintained well the prede-
termined breathing frequencies (0Æ10 Hz for 6 breaths ⁄min and
0Æ25 Hz for 15 breaths ⁄min) (Table 2).
HRV suppression 1 h after anaerobic effort and aerobic
exercise
Overall suppression of HRV
The whole HRV may be measured in time domain as the variance
of RRI, in frequency domain as total power of HRV, variance and
total power being numerically equal. SDNN is directly related to
whole HRV as a square root of RRI variance. Results of ANOVA for
SDNN revealed a significant effect of trial day, and a significant
interaction between type of effort and day of trial (Table 3).
Post hoc Newman–Keuls analysis revealed that SDNN after Wingate
tests was significantly lower in comparison with pre-exercise day,
and also to the 5th day. There were no significant differences
between SDNN obtained after submaximal exercise (Fig. 1), and
the remaining day of trial. The decline of SDNN from pre-exercise
to exercise day was greater for Wingate tests than for submaximal
Table 1 Anthropological data and results of
graded exercise test.
n
Age
(years)
Height
(cm)
Weight
(kg)
VO
2max
(ml kg
)1
min
)1
)RQ
max
HR
max
[bpm]
Peak
aerobic
power (W)
121Æ0 176 72 55 1Æ09 182 312
221Æ0 186 72 50 1Æ27 194 294
320Æ9 186 80 57 1Æ16 172 330
420Æ6 183 74 58 1Æ24 207 360
521Æ8 188 80 49 1Æ14 189 306
621Æ4 177 76 45 1Æ18 185 240
724Æ1 180 67 57 1Æ23 184 330
821Æ0 183 94 49 1Æ17 197 330
Mean ± SD 21Æ5±1Æ1 182 ± 4 77 ± 8 53 ± 5 1Æ19 ± 0Æ06 189 ± 11 313 ± 35
Table 2 Breathing frequency in Hz
(mean ± SD) on pre-exercise and exercise day
measured 1 h after either two 30-s Wingate
tests or 30 min of cycling at 85% HR
max
.
Wingate tests Submaximal exercise
Pre-exercise
day
Exercise
day
Pre-exercise
day
Exercise
day
Spontaneous 0Æ265 ± 0Æ075 0Æ281 ± 0Æ080 0Æ270 ± 0Æ075 0Æ275 ± 0Æ057
15 breaths⁄min 0Æ251 ± 0Æ001 0Æ250 ± 0Æ000 0Æ250 ± 0Æ000 0Æ250 ± 0Æ000
6 breaths⁄min 0Æ110 ± 0Æ008 0Æ103 ± 0Æ003 0Æ100 ± 0Æ000 0Æ100 ± 0Æ000
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
312

exercise, and this decline was statistically different for sponta-
neous and 6 breaths ⁄min respiration (Table 4).
Suppression of the high-frequency component of HRV
In this study, high-frequency component of HRV was measured
with RMSSD – time domain index sensitive more to rapid than
to slow changes in HR; this index was applied to all three modes
of breathing. The high-frequency component was also measured
with two frequency domain indices: HF and RF15, applied to
spontaneous and controlled breathing at 15 breaths ⁄min,
respectively.
Results of ANOVA for RMSSD revealed a significant effect of
trial day (with exception of RMSSD values noted during 6
breaths ⁄min respiration, see Table 3), and a significant inter-
action between type of effort and day of trial. Post hoc Newman–
Keuls analysis revealed that RMSSD after Wingate tests were
significantly lower in comparison with pre-exercise day, and to
the 5th day. There were no significant differences between
RMSSD obtained after submaximal exercise (Fig. 2), and the
remaining day of trial. The decline of RMSSD from pre-exercise
to exercise day was greater for Wingate tests than for
submaximal exercise (Fig. 3), and these declines were statisti-
cally different for spontaneous and 6 breaths ⁄min respiration
(Table 4).
The ANOVA for HF revealed a significant effect of trial day
and its significant interaction with type of effort (Table 3). Post
hoc Newman–Keuls analysis showed that HF after Wingate tests
was significantly different in comparison with all other day
(Fig. 2). The decline of HF from pre-exercise to exercise day
was significantly greater for Wingate tests than for submaximal
exercise (Table 4).
Statistical analysis of RF15 showed significant effect of trial
day, and it also interacted with type of effort (Table 3). Post hoc
Newman–Keuls analysis confirmed that RF15 on Wingate tests
Table 3 Effects of day of trial and exercise modality on mean RR
interval (RRI) and power spectral density (HRV) indices: SDNN, RMSSD,
high frequency (HF), low frequency (LF), RF15, RF6, assessed with
two-way ANOVA for repeated measurements, I factor: (5 day), II factor
type of exercise (two 30-s Wingate tests or 30 min of cycling at 85%
HR
max
).
Breathing
mode
RRI and
HRV indices
Factors
III I·II
spontaneous SDNN P<0Æ01 NS P<0Æ05
15 breaths ⁄min SDNN P<0Æ05 NS NS (P=0Æ052)
6 breaths ⁄min SDNN P<0Æ05 NS P<0Æ05
spontaneous RMSSD P<0Æ05 NS P<0Æ01
15 breaths ⁄min RMSSD P<0Æ01 NS P<0Æ05
6 breaths ⁄min RMSSD NS NS P<0Æ05
spontaneous HF P<0Æ05 NS P<0Æ05
15 breaths ⁄min RF15 P<0Æ01 NS P<0Æ01
spontaneous LF P<0Æ05 NS P<0Æ05
6 breaths ⁄min RF6 NS NS P<0Æ05
spontaneous RRI P<0Æ01 NS NS
15 breaths ⁄min RRI P<0Æ01 NS NS
6 breaths ⁄min RRI P<0Æ001 NS NS
Table 4 Comparison of mean RR interval (RRI) and heart rate variability (HRV) indices SDNN, RMSSD, high frequency (HF), low frequency (LF),
RF15, RF6 (mean ± SD) on pre-exercise day and exercise day and comparison of differences between pre-exercise day and exercise day values.
Significance of breathing frequency was evaluated with one-way ANOVA for repeated measurements, significance of trial day for a given exercise
modality, and significance of exercise modality for difference between pre-exercise day and exercise day value were evaluated with t-test for depended
samples, significance was assumed at P<0Æ05.
Type of
breathing
RRI and
HRV indices
Type of exercise
Wingate tests Submaximal exercise
Pre-exercise day Exercise day Difference Pre-exercise day Exercise day Difference
Spontaneous RRI (ms)
15
959
P⁄E
± 128 802 ± 208 157 ± 144 941
P⁄E
± 164 837 ± 126 103 ± 117
15 breaths ⁄min RRI (ms)
6,S
893
P⁄E
± 127 727 ± 162 167 ± 94 894 ± 166 809 ± 119 85 ± 39
6 breaths ⁄min RRI (ms)
15
944
P⁄E
± 125 784 ± 163 160 ± 79 923
P⁄E
± 162 824 ± 119 99 ± 81
Spontaneous SDNN (ms)
6,15
94
P⁄E
±41
6
45 ± 39 50
W⁄S
±38
6
79 ± 34
6
69 ± 25 10 ± 28
15 breaths ⁄min SDNN (ms)
6,S
59
P⁄E
±28
6
33 ± 22 26 ± 22
6
66 ± 48
6
59±49 8±11
6 breaths ⁄min SDNN (ms)
S,15
130
P⁄E
±64
S,15
85 ± 60 45
W⁄S
±36
S,15
129 ± 63
S,15
111 ± 56 18 ± 13
Spontaneous RMSSD (ms)
15
91
P⁄E
± 54 37 ± 49 53
W⁄S
±58
6
78 ± 56
6
57 ± 33 21 ± 44
15 breaths ⁄min RMSSD (ms)
6,S
58
P⁄E
±37
6
24 ± 22 34 ± 28
6
65 ± 52
6
46 ± 49 19 ± 11
6 breaths ⁄min RMSSD (ms)
15
108
P⁄E
±67
15
60 ± 53 48
W⁄S
±38
S,15
105 ± 69
S,15
85 ± 50 20 ± 15
Spontaneous HF (ms
2
) 2658
P⁄E
± 3308 509 ± 980 2149
W⁄S
± 3479 1782 ± 1535 837 ± 653 945 ± 1576
Spontaneous LF (ms
2
) 2094
P⁄E
± 1488 542 ± 646 1552
W⁄S
± 1344 1676 ± 1612 1446 ± 1509 230 ± 788
15 breaths ⁄min RF15 (ms
2
) 1121
P⁄E
± 1472 294 ± 455 827
W⁄S
± 1129 1140 ± 1499 639 ± 937 501 ± 733
6 breaths ⁄min RF6 (ms
2
) 13634
P⁄E
± 11968 5806 ± 6846 7828 ± 7608 11542 ± 11557 7350 ± 7552 4192 ± 6721
6 – according to post hoc Newman–Keuls test significantly different from 6 breaths ⁄min respiration value.
S – according to post hoc Newman–Keuls test significantly different from spontaneous respiration value.
15 – according to post hoc Newman–Keuls test significantly different from 15 breaths ⁄min respiration value.
P⁄E – according to t-test significantly different from exercise day.
W⁄S – according to t-test, change between pre-exercise day and exercise day of Wingate test session significantly different from such difference of
submaximal exercise session.
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
313

day was significantly different in comparison with all other day.
The decline of RF15 from pre-exercise to exercise day was
significantly greater for Wingate tests than for submaximal
exercise (Fig. 4, Table 4).
Suppression of the low-frequency component of HRV
In this study, low-frequency component of HRV was measured with
two frequency domain indices: LF and RF6, applied to
spontaneous and controlled breathing at 6 breaths ⁄min rate,
respectively.
The ANOVA for LF revealed a significant effect of trial day
and its significant interaction with type of effort (Table 3).
Despite this, post hoc Newman–Keuls analysis did not show any
significant difference between values from different day of
trial. However, P-values for paired comparisons between
Wingate tests exercise day versus each other trial day were
only marginally above 0Æ05. The decline of LF from pre-
RRI (ms)
700
800
900
1000
Wingate
85% HR
max
x
SDNN (ms)
20
40
60
80
100
120
xx
RMSSD (ms)
10
50
90
130
xx
ln HF
8
10
12
14
16
xxx
Day
ln LF
10
12
14
16
1 2 3 4 5
Figure 2 Mean values (SE) of RR interval and heart rate variability
(HRV) indices: SDNN, RMSSD, high frequency, and low frequency
measured in eight subjects during two 5-day trials. The 3rd day of each
trial was an exercise day, measurements were performed after 1-h
recovery. Subjects breathed spontaneously in supine position. Two
consecutive 30-s Wingate tests were performed during first trial, 30-min
submaximal exercise at 85% HR
max
during second trial. Data were
analysed with two-way ANOVA for repeated measurements and
subsequently with post hoc Neuman–Keuls test. x – 3rd day of both trials
significantly (P<0Æ05) different from all other day of both trials; xx – 3rd
day of Wingate trial significantly (P<0Æ05) different from 2nd and 5th
day of this trial; xxx – 3rd day of Wingate trial significantly (P<0Æ05)
differed from all other day of both trials.
RRI (ms)
600
700
800
900
1000
(a)
(
b)
S156 S156 S156 S156
S156 S15 6 S156 S15
6
Preexercise day
Exercise day
**
*
*
*
x
Wingate
85% HR
max
85% HR
max
Wingate
RMSSD (ms)
0
40
80
120
*
*
*
x
x
x
Figure 3 Effects of type of breathing (S: spontaneous breathing, 15:15
breaths ⁄min, 6:6 breaths ⁄min) and exercise modality (Wingate – two
consecutive 30-s Wingate tests, 85% HR
max
– 30 min submaximal
exercise at 85% HR
max
) on mean RR interval (a) and RMSSD (b). Values
are mean (SE), n= 8. Significance of breathing frequency was evaluated
with one-way ANOVA for repeated measurements, difference between
pre-exercise day and exercise day values (the same type of breathing and
the same trial) were evaluated with t-test for dependent samples. * –
significant (P<0Æ05) difference between pre-exercise and exercise day
values; x – significant (P<0Æ05) difference between value obtained at
given type of breathing and values obtained at two others types of
breathing.
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
314

exercise to exercise day was significantly greater for Wingate
tests than for submaximal exercise (Table 4).
The pattern of RF6 changes was similar to the rest of HRV
indices; however, two-way ANOVA failed to detect the
significant effect of trial day, but there was a significant
interaction between type of effort and trial day (Table 3).
Analysis of pre-exercise and exercise day (Table 4) showed that
RF6 on Wingate tests day was significantly smaller than on pre-
exercise day. The decline of RF6 from pre-exercise to exercise
day was insignificantly greater for Wingate tests than for
submaximal exercise.
Effects of breathing mode on HRV
Effect of breathing mode on HRV was evaluated as an effect on
time domain indices – SDNN and RMSSD, because only these
indices were applied to all three breathing modes. Breathing
mode did not change the pattern of HRV responses to two kinds
of exercise (Table 4); however, it generally changed magnitude
of SDNN and RMSSD; both indices were greatest during
respiration at 6 breaths ⁄min and smallest during respiration at
15 breaths ⁄min. The significance of the effect of breathing
modes was confirmed by one-way ANOVA for repeated
measurements, with mode of breathing as a factor, performed
separately on results from pre-exercise day and exercise day
(Table 4).
Similar shortening of RRI after anaerobic effort and 1 h
after strenuous aerobic exercise
Two-way ANOVA of RRI results yielded a reliable main effect of
day, but not of type of exercise (Table 3). Post hoc analysis
revealed that RRI values measured on exercise day both after
Wingate tests and submaximal effort were significantly different
from RRI values recorded on all others day (Fig. 2). There were
no significant differences between RRI values recorded on non-
exercise day, except for RRI values measured during 15
breaths ⁄min respiration, for which first and second day values
differed significantly from each other. Analysis limited only to
pre-exercise and exercise day (Table 4) revealed that following
both types of exercise RRI was significantly shorter on exercise
day in comparison with pre-exercise day, except for 15
breaths ⁄min respiration periods before and after submaximal
exercise (Fig. 3). The shortening of RRI from pre-exercise to
exercise day was greater after Wingate tests than after
submaximal exercise, but this difference was not significant.
Frequency of breathing did not change the general pattern of
RRI response to two kinds of exercises, however, affected
generally RRI duration: RRI was longest during spontaneous
respiration, and shortest during 15 breaths ⁄min respiration
(Table 4, Fig. 3). This was different from the effect of breathing
frequency on HRV indices, which were persistently greatest at 6
breaths ⁄min. The effect of breathing modes was analysed using
Frequency (Hz)
(a) (b)
(c) (d)
0·25
Frequency (Hz)
0·25
PSD (10
5
ms
2
/Hz) PSD (10
5
ms
2
/Hz)
PSD (10
5
ms
2
/Hz) PSD (10
5
ms
2
/Hz)
Frequency (Hz)
0·25
Frequency (Hz)
0·25
Figure 4 The example of heart rate variability (HRV) spectra obtained in the same subjects (Case No 5), during respiration at controlled rate 15
breaths ⁄min in supine position. The respiratory peak is centered at 0Æ25 Hz. RF15 was calculated by integrating power spectral density in the frequency
band 0Æ23 ± 0Æ27 Hz marked by two vertical cursors. The band of 0Æ04 Hz width usually encompasses the whole respiratory peak of HRV spectrum.
Spectra (a) and (c) were calculated for pre-exercise day, spectra (b) and (d) were calculated for exercise day. The spectrum (b) shows the clear
reduction of respiratory peak observed 1 h after Wingate test as compared to pre-exercise day (a). The respiratory peak in spectrum (d) observed 1 h
after the cessation of submaximal exercise is also decreased in comparison to pre-exercise day (c); however, the attenuation is less pronounced than
that seen after Wingate test.
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
315

one-way ANOVA for repeated measurements, with mode of
breathing as a factor, performed separately on results from pre-
exercise day and exercise day. This analysis revealed that
significant effect of breathing mode on RRI appeared only on
pre-exercise day of Wingate tests trial.
Blood pressure data provide no clues to explain the differential
effects of the two types of efforts on heart rhythm. Two-way
ANOVA revealed no significant effects on SBP and DBP of trial
day, type of exercise and no interaction of these factors. Blood
pressure, both SBP and DBP, was slightly (1–5 mmHg) and non-
significantly lower on exercise day; this attenuation was
marginally stronger after submaximal exercise. It could have
resulted in greater shortening of RRI after this kind of effort, but
we observed that RRI was longer after submaximal efforts than
after Wingate tests. Blood pressure lowering of similar magni-
tude was found at the time of recovery from submaximal exercise
(Forjaz et al., 1998; Terziotti et al., 2001; Mourot et al., 2004),
and from Wingate test (Hussain et al., 1996).
Discussion
This is, to our knowledge, the first study where heart rate
variability has been examined during the late stage of recovery
after short anaerobic exercise and compared with relevant
changes after intensive aerobic exercise.
The main findings of this study were (i) anaerobic effort in
the form of two consecutive Wingate tests was followed by
sustained, significant suppression of both high- and low-
frequency components of HRV and by sustained, significant
shortening of RRI and (ii) after aerobic exercise significant
shortening of RRI was accompanied by insignificant HRV
suppression. In the following discussion, we attempt to infer
from the observations outlined above possible changes in
autonomic activity during recovery after anaerobic effort and
after strenuous aerobic exercise.
Sustained inhibition of the postexercise vagal activity
It is postulated that vagal tone recovers promptly after exercise
cessation causing rapid HR decline and further decrease of HR is
due solely to the progressive decrease of sympathetic activity
(Perini et al., 1989; Imai et al., 1994). We argue that vagal tone
may remain inhibited at least 1 h after anaerobic exercise and
over considerable period after strenuous aerobic exercise. It is
accepted that high-frequency component of HRV, i.e. RR
interval fluctuations of frequencies above 0Æ15 Hz, is mediated
almost entirely by parasympathetic system, whereas those below
by both branches of ANS. In case of spontaneous breathing,
high-frequency component is measured as HF. HF was strongly
reduced 1 h after Wingate tests suggesting sustained inhibition
of vagal activity. Results obtained from controlled breathing
agreed with those from spontaneous breathing. Maintaining
breathing frequency above 0Æ15 Hz and at fixed rate ascertains
that well-defined peak of respiratory arrhythmia is mediated by
alteration of vagal tone only; power of this peak was measured
with RF15 index. RF15 was strongly attenuated after Wingate
tests similarly to HF, thus corroborating vagal tone suppression.
In our study, reduction of the high-frequency component 1 h
after aerobic exercise did not attain significance; however,
significant reduction of this component has been noted 45 min
(Oida et al., 1997), 30 min (Javorka et al., 2002) and 1 h
(Mourot et al., 2004) after strenuous aerobic exercise. Together,
these results implicate sustained vagal inhibition after anaerobic
and strenuous aerobic exercise.
During postexercise recovery, low-frequency component
of HRV is mediated mainly by parasympathetic system
During spontaneous breathing, LF – an index of low-frequency
component of HRV – was attenuated 1 h after Wingate tests
almost as strongly as HF. In case of slow breathing, the peak of
respiratory arrhythmia was centred at 0Æ1 Hz, well below
0Æ15 Hz, thus contribution of sympathetic branch could not be
excluded. The power associated with this peak – RF6 – was
reduced after Wingate test similarly to LF, indicating dominant
role of vagal activity in mediating the respiratory arrhythmia
during slow breathing. This similarity occurred despite different
origin of LF and RF6, former being of non-respiratory origin,
latter probably arising from both respiratory and non-respirat-
ory causes and despite severalfold greater power associated with
RF6 than with LF. Also, after aerobic exercise, both low- and
high-frequency components of HRV were reduced though
insignificantly. Concomitant reduction of both components after
moderate- and high-intensity aerobic exercises was reported
(Arai et al., 1989; Furlan et al., 1993; Goldberger, 1999; Javorka
et al., 2002; Mourot et al., 2004). Our observations and those of
others are inconsistent with the notion that low-frequency
component of HRV is related to sympathetic activity. Rather,
they are consistent with the view that this component is
mediated mainly by parasympathetic system, at least during
postexercise recovery.
Rate of recovery of vagal activity after anaerobic effort
may be similar to that after heavy aerobic exercise
It is known that aerobic exercise reduces HF and LF (Arai et al.,
1989; Perini & Veicsteinas, 2003). Initial recovery of HR and
HRV is fast and independent of exercise intensity, probably
because of prompt (though incomplete as we imply) restoration
of vagal tone. After low-intensity effort recovery of HR and HRV
is complete within 5 min (Perini et al., 1990), while after
moderate- and high-intensity exercises – as already mentioned –
recovery of high- and low-HRV frequency components lasts
much longer. Our observations show that 1 h after cessation of
Wingate tests HRV was significantly reduced, thus the time
required for accomplishing recovery of vagal activity after
double Wingate test exceeds 1 h. This time is probably longer
than the time of vagal activity recovery after heavy aerobic
exercise, as 1 h after cessation of strenuous aerobic exercise
HRV was insignificantly reduced, what corresponds with data of
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
316

Oida et al. (1997), and Javorka et al. (2002), though significant
HRV reduction lasting 1 h was noted by Furlan et al. (1993) and
Mourot et al. (2004). It seems plausible that time required for
vagal activity to normalize is related to the degree of ANS
activity alteration. If so, we could assume that alteration of
autonomic activity after Wingate tests might be as strong or
even stronger than that caused the strenuous aerobic exercise.
Normalized vagal and augmented sympathetic cardiac
nerves activity during late recovery
Persistent shortening of RRI after anaerobic effort might result
from inhibited vagal and augmented sympathetic activity. The
shortening of RRI after submaximal exercise might be caused
mainly by lasting augmentation of sympathetic activity, almost
normal vagal activity contributing only slightly. We have to
admit that it is not certain whether return of HRV to baseline
precedes that of RR interval or vice versa during postexercise
recovery. Terziotti et al. (2001) reported that, 1 h after a 20-min
lasting exercise at 80% of the individuals anaerobic threshold,
HRV was close to pre-exercise level, but RR intervals were still
significantly reduced. However, Oida et al. (1997) reported
return of RR interval to baseline, yet HF remained attenuated
45 min after a 30-min exercise at ventilatory threshold
intensity. It remains to be seen whether the recovery of HRV
and RRI after Wingate tests will follow the same course, as
found after the aerobic exercise.
The interpretation of elevated HR concomitant with normal
HRV depends on the believed way two branches of autonomic
system interact. According to Pomeranz et al. (1985) who found
that in supine position vagal blockade completely abolished
HRV whereas effects of propranolol were inconsistent and
insignificant; return of HRV to normal should be interpreted as
normalization of vagal activity. Consequently, elevated HR
evidences increased the sympathetic activity of sympathetic
cardiac nerves. The more recent findings of Taylor et al. (2001),
who found that sympathetic system attenuates HRV, are difficult
to reconcile with our findings. If HR was elevated due to
sympathetic activity, HRV should be also attenuated; if on the
other hand sympathetic activity returned to normal, then HR
had to be elevated due to reduced vagal activity and HRV should
be reduced as well.
It is possible that in the situation of late recovery we should
refrain from referring to augmented sympathetic activity. This
notation implicates generalized increase of sympathetic activity.
However, such generalization might be questionable. Halliwill
et al. (1996a) found both significantly elevated HR and plasma
noradrenaline up to 75 min after moderate-intensity dynamic
exercise. On the other hand, Halliwill et al. (1996b) found that
1 h after the same kind of exercise muscle sympathetic nerve
activity was reduced. Therefore, elevated HR should be
interpreted specifically as a sign of augmented sympathetic
cardiac nerves activity.
Two rather unexpected observations deserve short comment.
Firstly, higher breathing rates coincide with smaller amplitudes
of respiratory arrhythmia (Hirsch & Bishop, 1981; Eckberg,
1983; Saul et al., 1989; Kollai & Mizsei, 1990; Grossman et al.,
1991; Brown et al., 1993; Cooke et al., 1998). Therefore, we
expected RMSSD, the time domain index of HRV which is
strongly related to the amplitude of respiratory arrhythmia, to
be slightly smaller during spontaneous breathing, than during
15 breaths ⁄min as the average spontaneous breathing rate was
slightly higher than 15 breaths ⁄min. However, the reverse was
true. This can be explained by the effect of voluntary control of
breathing, which may attenuate respiratory arrhythmia (Pat-
wardhan et al., 1995b). The significance of this effect is
disputable because its strength may depend on complexity of
respiratory task to be performed. It was found that breathing at
fixed rate, equal to the average breathing rate during sponta-
neous respiration, which was easier than the respiratory task
described in the above-mentioned study, did not reduce
respiratory arrhythmia (Patwardhan et al., 1995a).
Secondly, in contrast to HRV, which was greatest at 6
breaths ⁄min, RRI was longest during spontaneous breathing.
The effect of breathing rate on RRI is controversial, as slowing of
breathing resulted in lengthening (Eckberg, 1983), non-
uniform changes (Kollai & Mizsei, 1990), or no alteration of
RRI at all (Eckberg, 2003). Our results are best compatible with
the observation of Patwardhan et al. (1995b), who found that
voluntary control of breathing shortened RRI.
This study demonstrates that exercise at maximal power
output causes long-lasting changes in autonomic activity in
young and healthy men. They qualified as fit, according to their
maximal oxygen consumption and peak power attained during
Wingate test (Astrand & Rodhal, 1986; Inbar et al., 1996).
Sedentary individuals are at much greater risk of cardiovascular
events, especially that induced by strenuous exercise (Bartels
et al., 1997), and a role of the ANS in precipitating the outcome
of these events may be significant (Schwartz et al., 1992;
Schwartz, 1998; Adamson & Vanoli, 2001). Thus, our findings
might be of considerable significance for this population. We
hypothesize that prolonged disturbance of autonomic activity,
similar to that we observed after Wingate tests, might follow
resistance exercises. Resistance exercises are anaerobic, and they
also strongly activate SNS (Hurley et al., 1984). If this hypothesis
turns true, observations presented here might be of importance
for elderly, as resistance exercises are strongly recommended for
preventing the age-related loss of mass and strength of skeletal
muscles (Evans, 1999).
In conclusion, the main findings of this study were the
persistent suppression of high- and low-HRV frequency
components accompanied by significant shortening of RRI after
short anaerobic effort, insignificantly suppressed HRV accom-
panied by significant shortening of RRI after strenuous aerobic
exercise. This suggests that (i) sustained inhibition of the vagal
activity following anaerobic exertion, (ii) dominant role of
parasympathetic system in mediating suppression of the high-
and low-HRV frequency components during postexercise
recovery, (iii) similar degree of alteration of ANS activity
caused by anaerobic and strenuous aerobic exercise, (iv)
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
317

normalization of vagal activity preceding normalization of
sympathetic cardiac nerves activity during final stage of
postexercise recovery.
Acknowledgments
We thank Profs Krystyna Nazar and Hanna Kaciuba-Us
´ciłko
for their encouragement and help carry out this study, and for
reviewing earlier drafts of this manuscript, and Dr G. Riedel for
careful review of its present version.
References
Adamson PB, Vanoli E. Early autonomic and repolarization abnormalities
contribute to lethal arrhythmias in chronic ischemic heart failure:
characteristics of a novel heart failure model in dogs with postmyo-
cardial infarction left ventricular dysfunction. J Am Coll Cardiol (2001);
37: 1741–1748.
Albert CM, Mittleman MA, Chae CU, Lee IM, Hennekens CH, Manson JE.
Triggering of sudden death from cardiac causes by vigorous exertion.
N Engl J Med (2000); 343: 1355–1361.
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–H141.
Astrand PO, Rodhal K. Textbook of Work Physiology: Physiological Bases of Exercise,
3rd edn. (1986). McGraw Hill, New York
Backx K, McNaughton L, Crickmore L, Palmer G, Carlisle A. Effects of
differing heat and humidity on the performance and recovery from
multiple high intensity, intermittent exercise bouts. Int J Sports Med
(2000); 21: 400–405.
Bartels R, Menges M, Thimme W. Effect of physical activity on incidence
of sudden cardiac death. Study of the Berlin-Reinickendorf and Berlin-
Spandau population. Med Klin (Munich) (1997); 92: 319–325.
Brown TE, Beightol LA, Koh J, Eckberg DL. Important influence of
respiration on human R-R interval power spectra is largely ignored.
J Appl Physiol (1993); 75: 2310–2317.
Coats AJS, Conway J, Isea JE, Pannarale G, Sleight P, Somers VK. Systemic
and forearm vascular resistance changes after upright bicycle exercise
in man. J Physiol (1989); 413: 289–298.
Cobb LA, Weaver WD. Exercise: a risk for sudden death in patients with
coronary heart disease. J Am Coll Cardiol (1986); 7: 215–219.
Cooke WH, Cox JF, Diedrich AM, Taylor JA, Beightol LA, Ames JE 4th,
Hoag JB, Seidel H, Eckberg DL. Controlled breathing protocols probe
human autonomic cardiovascular rhythms. Am J Physiol (1998); 274:
H709–H718.
Dotan R. The Wingate anaerobic tests past and future and the compa-
tibility of mechanically versus electro-magnetically braked cycle-erg-
ometers. Eur J Appl Physiol (2006); 98: 113–116.
Duncan GE, Howley ET, Johnson BN. Applicability of VO
2max
criteria:
discontinuous versus continuous protocols. Med Sci Sports Exerc (1997);
29: 273–278.
Eckberg DL. Human sinus arrhythmia as an index of vagal cardiac out-
flow. J Appl Physiol (1983); 54: 961–966.
Eckberg DL. Symathovagal balance A critical appraisal. Circulation (1997);
96: 3224–3232.
Eckberg DL. The human respiratory gate. J Physiol (2003); 548: 339–352.
Evans WJ. Exercise training guidelines for the elderly. Med Sci Sports Exerc
(1999); 31: 12–17.
Falk B, Radom-Isaac S, Hoffmann JR, Wang Y, Yarom Y, Magazanik A,
Weinstein Y. The effect of heat exposure on performance of and
recovery from high-intensity, intermittent exercise. Int J Sports Med
(1998); 19: 1–6.
Floras JS, Sinkey CA, Aylward PE, Seals DR, Thoren PN, Mark AL.
Postexercise hypotension and sympathoinhibition in borderline
hypertensive men. Hypertension (1989); 14: 28–35.
Forjaz CLM, Matsudaira Y, Rodrigues FB, Nunes N, Negrao CE. Post-
exercise changes in blood pressure, heart rate and rate pressure
product at different exercise intensities in normotensive humans. Braz J
Med Biol Res (1998); 31: 1247–1255.
Furlan R, Piazza S, DellOrto S, Gentile E, Cerutti S, Pagani M, Malliani A.
Early and late effects of exercise and athletic training on neural
mechanisms controlling heart rate. Cardiovasc Res (1993); 27: 482–488.
Goldberger JJ. Sympathovagal balance: how should we measure it? Am J
Physiol (1999); 276: H1273–H1280.
Grossman P, Karemaker J, Wieling W. Prediction of tonic parasympa-
thetic cardiac control using respiratory sinus arrhythmia: the need for
respiratory control. Psychophysiology (1991); 28: 201–216.
Halliwill JR, Taylor JA, Hartwig TD, Eckberg DL. Augmented baroreflex
heart rate gain after moderate-intensity, dynamic exercise. Am J Physiol
(1996a); 270: R420–R426.
Halliwill JR, Taylor JA, Eckberg DL. Impaired sympathetic vascular
regulation in humans after acute dynamic exercise. J Physiol (1996b);
495: 279–288.
Hara K, Floras JS. Influence of naloxone on muscle sympathetic nerve
activity, systemic and calf haemodynamics and ambulatory blood
pressure after exercise in mild essential hypertension. J Hypertens
(1995); 13: 447–461.
Hautala A, Tulppo MP, Makikallio TH, Laukkanen R, Nissila S, Huikuri
HV. Changes in cardiac autonomic regulation after prolonged max-
imal exercise. Clin Physiol (2001); 21: 238–245.
Hirsch JA, Bishop B. Respiratory sinus arrhythmia in humans: how
breathing pattern modulates heart rate. Am J Physiol (1981); 241:
H620–H629.
Hoffman JR, Falk B, Radom-Isaac S, Weinstein Y, Magazanik A, Wang Y,
Yarom Y. The effect of environmental temperature on testosterone
and cortisol responses to high intensity, intermittent exercise in
humans. Eur J Appl Physiol (1997); 75: 83–87.
Hurley BF, Seals DR, Ehsani AA, Cartier LJ, Dalsky GP, Hagberg JM,
Holloszy JO. Effects of high-intensity strength training on cardiovas-
cular function. Med Sci Sports Exerc (1984); 16: 483–488.
Hussain ST, Smith RE, Medbak S, Wood RFM, Whipp BJ. Haemody-
namic and metabolic responses of the lower limb after high intensity
exercise in humans. Exp Physiol (1996); 81: 173–177.
Imai K, Sato H, Hori M, Kusuoka H, Ozaki H, Yokoyama H, Takeda H,
Inoue M, Kamada T. 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: 529–535.
Inbar O, Bar-Or O, Skinner JS. The Wingate Anaerobic Test. Human Kinetics
(1996). Champaign, IL, USA.
Javorka M, Zila I, Balharek T, Javorka K. Heart rate recovery after
exercise: relations to heart rate variability and complexity. Braz J Med
Biol Res (2002); 35: 991–1000.
Kollai M, Mizsei G. Respiratory sinus arrhythmia is a limited measure of
cardiac parasympathtic control in man. J Physiol Lond (1990); 424:
329–342.
Legramante JM, Galante A, Massaro M, Attanasio A, Raimondi G, Pigozzi
F, Iellamo F. Hemodynamic and autonomic correlates of postexercise
hypotension in patients with mild hypertension. Am J Physiol Regul Integr
Comp Physiol (2002); 282: R1037–R1043.
Meyer T, Gabriel HH, Kindermann W. Is determination of exercise
intensities as percentages of VO
2max
or HR
max
adequate? Med Sci Sports
Exerc (1999); 31: 1342–1345.
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
318

Micklewright D, Alkhatib A, Beneke R. Mechanically vs. electro-
magnetically braked cycle ergometer: performance and energy cost of
the Wingate anaerobic test. Eur J Appl Physiol (2006); 96: 748–751.
Mittleman MA, Maclure M, Tofler GH, Sherwood JB, Goldberg RJ,
Muller JE. Triggering of acute myocardial infarction by heavy physical
exertion. Protection against triggering by regular exertion. Determi-
nants of Myocardial Infarction Onset Study Investigators. N Engl J Med
(1993); 329: 1677–1683.
Mourot L, Bouhaddi M, Tordi N, Rouillon JD, Regnard J. Short- and
long-term effects of a single bout of exercise on heart rate variability:
comparison between constant and interval training exercises. Eur J Appl
Physiol (2004); 92: 508–517.
Oida E, Moritani T, Yamori Y. Tone-entropy analysis on cardiac recovery
after dynamic exercise. J Appl Physiol (1997); 82: 1794–1801.
Patwardhan AR, Evans JM, Bruce EN, Eckberg DL, Knapp CF. Voluntary
control of breathing does not alter vagal modulation of heart rate.
J Appl Physiol (1995a); 78: 87–94.
Patwardhan AR, Vallurupali S, Evans JM, Bruce EN, Knapp CF. Override
of spontaneous respiratory pattern generator reduces cardiovascular
parasympathetic influence. J Appl Physiol (1995b); 79: 1048–1054.
Perini R, Veicsteinas A. Heart rate variability and autonomic activity at
rest and during exercise in various physiological conditions. Eur J Appl
Physiol (2003); 90: 317–325.
Perini R, Orizio C, Comande A, Castellano M, Beschi M, Veicsteinas A.
Plasma norepinephrine and heart rate dynamics during recovery from
submaximal exercise in man. Eur J Appl Physiol Occup Physiol (1989); 58:
879–883.
Perini R, Orizio C, Baselli G, Cerutti S, Veicsteinas A. The influence of
exercise intensity on the power spectrum of heart rate variability. Eur J
Appl Physiol Occup Physiol (1990); 61: 143–148.
Piepoli M, Isea JE, Pannarale G, Adamopoulos S, Sleight P, Coats AJS. Load
dependence of changes in forearm and peripheral vascular resistance
after acute leg exercise in man. J Physiol (1994); 478: 357–362.
Pomeranz B, Macaulay RJ, Caudill MA, Kutz I, Adam D, Gordon D,
Kilborn KM, Barger AC, Shannon DC, Cohen RJ, Benson H.Assess-
ment of autonomic function in humans by heart rate spectral analysis.
Am J Physiol (1985); 248: H151–H153.
Saul JP, Berger RD, Chen MH, Cohen RJ. Transfer function analysis of
autonomic regulation. II. Respiratory sinus arrhythmia. Am J Physiol
(1989); 256: H153–H161.
Schwartz PJ. The autonomic nervous system and sudden death. Eur Heart J
(1998); 19 (Suppl. F): F72–F80.
Schwartz PJ, La Rovere MT, Vanoli E. Autonomic nervous system and
sudden cardiac death. Experimental basis and clinical observations for
post-myocardial infarction risk stratification. Circulation (1992);
1(Suppl.): I77–I91.
Taylor JA, Myers CW, Halliwill JR, Seidel H, Eckberg DL. Sympathetic
restraint of respiratory sinus arrhythmia: implications for vagal-car-
diac tone assessment in humans. Am J Physiol Heart Circ Physiol (2001);
280: H2804–H2814.
Terziotti P, Schena F, Gulli G, Cevese A. Post-exercise recovery of
autonomic cardiovascular control: a study by spectrum and cross-
spectrum analysis in humans. Eur J Appl Physiol (2001); 84: 187–194.
Willich SN, Lewis M, Lowel H, Arntz HR, Schubert F, Schroder R.
Physical exertion as a trigger of acute myocardial infarction. Triggers
and Mechanisms of Myocardial Infarction Study Group. N Engl J Med
(1993); 329: 1684–1690.
HRV suppression after supramaximal exertion, W. Niewiadomski et al.
2007 The Authors
Journal compilation 2007 Blackwell Publishing Ltd •Clinical Physiology and Functional Imaging 27, 5, 309–319
319