Hyperpnea training attenuates peripheral chemosensitivity and improves cycling endurance
1 Exercise Physiology, Swiss Federal Institute of Technology and University
of Zurich, Zurich, Switzerland
2 John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii,
USA
* Author for correspondence (e-mail: spengler{at}physiol.unizh.ch)
Accepted 16 September 2002
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Summary |
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Key words: respiratory muscle endurance training, carotid body, control of breathing, hyperpnea, exercise, human
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Introduction |
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Respiratory muscle training (RMT: 20x 30 min sessions of voluntary
normocapnic hyperpnea) was used to simulate the high
E achieved during heavy exercise. RMT
isolates the effect of high levels of ventilation on the pRc
sensitivity while minimizing other potentially confounding adaptations, e.g.
adaptations of the cardiovascular system, that normally accompany whole-body
exercise (Markov et al.,
2001
), although both types of training improve endurance
performance (Boutellier et al.,
1992
; Boutellier and Piwko,
1992
; Spengler et al.,
1999
).
Markov et al. (1996)
investigated the effects of RMT on the resting hypoxic ventilatory response
and found no significant change. However, it is known that the pRc
respond to stimuli other than hypoxia, e.g. CO2, [H+]
and [K+] (reviewed by Nye,
1994
). Furthermore, the hypoxic ventilatory response and thus the
pRc sensitivity may be increased during exercise
(Weil et al., 1972
). With
these factors in mind, we reasoned that any changes resulting from an exercise
or a respiratory training program would be more readily identifiable by
examining the response of the pRc to their full range of stimuli
during exercise. Therefore, to assess the complete pRc contribution
to
E during exercise, we used a
modified Dejours O2 test
(Dejours, 1963
). The modified
Dejours O2 test assumes that the pRc drive to breathe is
effectively eliminated by briefly breathing 100% O2.
We hypothesized that RMT would decrease pRc sensitivity, as whole-body endurance training has been shown to do, if the high levels of ventilation occurring during exercise were responsible for the change in pRc sensitivity after whole-body training.
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Materials and methods |
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Before obtaining written informed consent, the study requirements, the experimental protocol, and all risks associated with the study were outlined for each subject. However, the subjects were kept unaware of the purpose of the study. The study was approved by the Ethics Committee of Physiology and Pharmacology at the University of Zurich.
Protocol
On a separate day, prior to any testing, subjects underwent at least one
familiarization session, including familiarization with the respiratory
training device. This familiarization was critical to ensure normocapnic
conditions during hyperpnea, to remove any learning effect associated with the
use of the respiratory training device, and to select an appropriate
ventilatory level for the breathing endurance test (see below). After the
familiarization session(s), both groups of subjects underwent four test
sessions on four different days. The test sessions consisted of: (1)
spirometric measurements followed by a pause of at least 15 min and then an
incremental cycling test to exhaustion; (2) breathing endurance test; (3)
modified Dejours O2 test; (4) cycling endurance test to exhaustion.
All four test sessions were performed on separate days with a minimum of 2
days between test sessions. The entire test period lasted approximately 14
days. A 4-6 week RMT or control period followed.
During the RMT period, subjects completed 20 voluntary normocapnic
hyperpnea sessions of 30 min duration each, using a special device (see
below). The E of the first training
session was approximately 60% of the individual maximum voluntary ventilation
in 15 s. Afterwards, the intensity level was increased such that the subjects
could hold the training-
E constant for
at least 30 min, but no longer than 35-40 min, i.e. subjects had to feel that
they could have continued for a maximum of 5-10 min longer than the actual
training time of 30 min. Increases in training intensity were made by
increasing
E, primarily by increasing
breathing frequency. The subjects performed their training at home. Every
fifth RMT was performed in the laboratory where training logs were checked and
subjects were connected to the metabolic cart during training to observe their
training technique [constant tidal volume (VT) and respiratory
frequency (fR)] and to ensure normocapnia. Analysis of the four
observed RMT training sessions performed in the laboratory showed the subjects
maintained the end-tidal fractional concentration of carbon dioxide
FETCO2 within the range 4.6-5.8%. After the RMT or control
period, the four test sessions were repeated.
For technical reasons, the cardiorespiratory data pertaining to the cycling endurance test of two subjects, one from each group, was not available for the final analysis. Another two subjects, one from each group but different from the two above, were unable to successfully complete the modified Dejours O2 test.
Tests and equipment
Test session 1
Spirometric variables, i.e. vital capacity, forced expiratory vital
capacity, forced expiratory volume in 1 s, peak expiratory flow and maximum
voluntary ventilation, were measured according to ATS criteria (American
Thoracic Society, 1991,
1995
) with an ergospirometric
device (Oxycon Beta, Jaeger, Höchberg, Germany) using a calibrated
turbine for volume measurements.
The incremental exercise test was performed on an electromagnetically
braked cycle ergometer (Ergometrics 800S, Ergoline, Bitz, Germany) to
determine peak oxygen consumption
(O2peak) and maximal work
capacity (
max). The test
began at 100 W and the intensity was increased by 30 W every 2 min until the
subjects could no longer continue. The subjects selected their preferred
pedaling frequency and maintained this cadence ±5 revs min-1
throughout the test. Ventilatory variables and gas exchange were measured
breath by breath with the Oxycon Beta metabolic cart, using fast-responding
gas analyzers (paramagnetic for O2, infrared for CO2).
Cardiac frequency (fC) was recorded every 5 s (PE 4000, Polar
Electro, Kempele, Finland). Blood samples (20 µl), from an earlobe, were
collected at the end of each workload step and at the end of the test and the
whole blood samples were analyzed enzymatically for blood lactate
concentration with a Biosen 5040 apparatus (EKF Industrie, Barleben,
Germany).
Test session 2
The breathing endurance test was conducted at a
E corresponding to 74±10% of
the pre-RMT maximum voluntary ventilation, i.e.
E, VT and fR were
similar for breathing endurance tests before and after the RMT/control period
(
E, RMT: 142±25 versus
144±24 l min-1, control: 141±25 versus
140±24 l min-1; VT, RTM: 3.0±0.6
versus 3.1±0.61, control: 2.9±0.6 versus
2.9±0.61; fR, RMT: 47±5 versus 47±4
breaths min-1, control: 49±5 versus 49±4
breaths min-1). During the breathing endurance test, the RMT device
(see below) was connected to the metabolic cart. During familiarization
sessions (see below), a level of ventilation was chosen by the investigators
that ensured the subjects could continue for a minimum of 6 min but not longer
than 15 min. Subjects were required to maintain this pre-selected
E while holding VT and
fR, paced by a metronome (DM-20, Seiko, Tokyo, Japan), constant. If
necessary, the test administrator corrected subjects' VT or
fR (which he supervised on the metabolic cart) and he ensured
normocapnia was maintained. The test ended when the subject reached volitional
exhaustion, when the experimenter stopped the test because the subject could
not maintain the VT- or fR-target any longer (i.e. the
experimenter observed
E and if it
fell, he told the subject to increase either VT or fR; if
the subject was not able to reach the target after a 3rd `warning',
the test was stopped) or when 40 min were reached. Otherwise, subjects were
not encouraged during this test. The 40 min cut-off time was reached by five
subjects in the RMT group during the post-training breathing endurance test.
If subjects continued for more than 15 min in the pre-test or if normocapnia
was not maintained, the test was considered to be an additional `training
session', the training device was adjusted and the test was repeated on
another day (this occurred once). The end-time was used as an estimate of
respiratory muscle endurance. Ventilatory variables and gas exchange were
measured breath by breath and heart rate was sampled every 5 s.
The RMT-device allowed partial rebreathing of CO2 to maintain
normocapnia. The device consisted of a mouthpiece connected by a tube to a
rebreathing bag. The size of the bag was adjusted to be 50-60% of the
subjects' vital capacity. Subjects were instructed to fill and empty the bag
completely while additional inspiratory and expiratory flow passed through a
small hole in the tube to avoid an increase in arterial CO2 partial
pressure and a fall in O2 saturation, i.e. VT was slightly
larger than the bag itself. Breathing frequency was adjusted to reach the
target E. Correct performance, i.e.
the maintenance of normocapnia, was checked with the training device connected
to the Oxycon Beta. If normocapnia was not maintained during training
sessions, the hole was adjusted in size and/or the combination of VT
and fR was changed.
Test session 3
A modified Dejours O2 test
(Dejours, 1963) was completed
while the subjects were cycling at 40%
max. First, the subjects
rested for 10-15 min while sitting in a chair and listening to relaxing music.
Next, the subjects moved to the ergometer and cycled for 5 min breathing room
air, followed by another 5 min of breathing compressed air. The subjects'
mouthpiece was connected to a three-way valve, out of sight such that they
could not see or hear when inspired gases were changed. Then, during an
exhalation, the compressed air was surreptitiously switched to 100% oxygen for
10-14 breaths (20-30 s) while the periods of breathing compressed air lasted
for 3 min each. Every subject completed 4-6 hyperoxic trials. Dejours's
(1963
) one- or two-breath
O2 test was slightly modified as preliminary trials showed the most
consistent responses during cycling at 40%
max occurred while
breathing 100% oxygen for approximately 12 breaths, which resulted in a
decrease in ventilation to an eventual nadir within 30 s. This decrease
reflects the pRc contribution to the ventilatory drive and can be
expressed as a percentage of the pre-oxygen breathing ventilation. Blood
samples were taken prior to and at the end of the test to measure lactate
concentration.
Test session 4
The cycling endurance test at 85% of pre-RMT
max was performed to
exhaustion. This test began with 4 min of sitting quietly on the cycle
ergometer, followed by 2 min of unloaded pedaling, 2 min at 40%
max, 3 min at 60%
max and, finally, 85%
max for the remainder of
the test. Subjects chose their preferred cadence, and this was maintained
throughout all cycling endurance tests (±5 revs min-1). The
time at which the subject was unable to maintain the cadence within the proper
range or reached volitional exhaustion was used as the end-time. This time,
excluding rest and unloaded pedaling, was used as the measure of cycling
endurance. Ventilatory variables and gas exchange were recorded breath by
breath (Oxycon Beta) and fC was sampled every 5 s. Blood samples were
taken every 2 min and at the end of the test to measure lactate concentration.
The subjects never received verbal encouragement throughout any of the tests.
The last two meals before this test were supplemented by 0.51 of a 15.8%
carbohydrate drink (Wander isostar long energy; Novartis Consumer Health
Schweiz AG, Bern, Switzerland) to replenish glycogen stores.
Data analysis
The max was defined as
the highest workload sustained for a minimum of 90 s during the incremental
test.
O2peak was
obtained from the highest
O2 reached over
a 30 s period during this test.
Each modified Dejours O2 test was analyzed using
breath-by-breath measurements. The steady-state
E was obtained from the mean value
during the 30 s period preceding the switching to hyperoxia. The magnitude of
the following decrement in
E was
determined using a two-breath moving average. The lowest two-breath average
was compared to the steady-state
E
obtained prior to the switching to hyperoxia and the reduction was expressed
as percentage of the baseline ventilation. Equipment errors, sighs or swallows
(single breaths that deviated by more than ±2 S.D. from the mean
E of the prior and following breaths)
were not included in the analysis. 4-6 hyperoxic episodes were completed by
each subject. The average of these trials was taken as the subject's
pRc response.
Breath-by-breath data from the cycling endurance test was averaged into 15 s segments. For comparison of cardiorespiratory variables, these 15 s segments were organized into two categories, steady state and end-time. The 2 min samples of blood lactate concentration were grouped into similar categories. The steady-state included data from the 85% level, less the first 1 min 45 s and the last 2 min of the shorter of the pre- or post-tests. An identical time period was chosen for the longer of the two tests. Thus, the steady-state of the cycling endurance test was a comparison of identical times for the pre- and post-test of each subject. The end-time category included the last complete 60 s of each test.
Values are reported as means ± S.D. Between group comparisons of pre/post changes, i.e. changes within the subjects pre- to post-RMT or control period, were performed using unpaired t-tests with the exception of the breathing endurance test. Since this was stopped at 40 min in 5 subjects, the non-parametric MannWhitney U-test was employed. The Pearson productmoment correlation coefficients were used for calculating correlations between selected variables. Fisher's R to Z test was used for detecting statistical significance. For all tests statistical significance was defined as a value of P<0.05. Statistical analyses were completed with StatView 4.53 (Abacus Concepts, Berkeley, CA, USA).
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Results |
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Spirometry
RMT significantly improved vital capacity and maximum voluntary ventilation
compared to the control group (Table
1). Other spirometric variables, i.e. forced expiratory vital
capacity, forced expiratory volume in 1 s, and peak expiratory flow, were not
changed significantly.
|
Breathing endurance test
Following the RMT period, the time to exhaustion during the breathing
endurance test was significantly improved by more than 250% in the RMT group
compared to the control group (Table
1). After the RMT period, the breathing endurance test was stopped
at 40 min for 5 of the 10 subjects in the RMT group. None of the 10 subjects
in the control group reached the 40 min cut-off time.
Incremental test
The respiratory, cardiovascular and metabolic indicators of aerobic fitness
(i.e. O2,
fC, lactate concentration and
max), measured during the
incremental test, did not change significantly following the RMT or control
period for either group, as shown in Table
2.
|
Cycling endurance test
RMT increased cycling endurance significantly in the RMT group compared to
the control group (Fig. 2).
Ventilatory and cardiovascular parameters of the cycling endurance test in
both the steady-state and end-time categories are shown in
Table 3. The change in end-time
of the cycling endurance test did not correlate significantly with the change
in the pRc response in either group (RMT: r=0.11,
P=0.79; control: r=0.13, P=0.74) nor was the
correlation between changes in the steady-state
E of the cycling endurance test and
the change in the pRc response significant (RMT: N=8,
r=0.43, P=0.09; control: N=8, r=0.64,
P=0.31).
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Discussion |
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The effectiveness of the RMT program was demonstrated by the significant
increases in maximum voluntary ventilation and breathing endurance time. These
results are in agreement with previous studies in which subjects trained the
respiratory muscles in a similar fashion
(Boutellier et al., 1992;
Boutellier and Piwko, 1992
;
Leith and Bradley, 1976
;
Spengler et al., 1999
). The
lack of significant changes of cardiovascular and metabolic indicators of
aerobic fitness, e.g. fC, lactate concentration,
E, during the incremental test
(Table 2) and the cycling
endurance test (Table 3)
indicated that the general fitness of the subjects had not changed during the
study. This was validated by examining the subjects' training logs, which
confirmed that they kept their level of activity constant during the course of
this study. Therefore, RMT was effective and it was likely responsible for the
improved cycling endurance and the decreased pRc sensitivity.
With respect to the modified Dejours O2 test that was used to
determine pRc sensitivity during exercise, it is important to note
that a false reduction in pRc sensitivity could be detected after
RMT if pRc-stimulation per se were smaller after RMT than
before, i.e. if [H+] or any other pRc-stimulating factor
were smaller. This, however, was unlikely to be the case as ventilation, gas
exchange and blood lactate concentrations were similar during exercise before
and after RMT. Also, the strength of the pRc drive might have been
underestimated because, on the one hand, some uncertainty exists as to whether
the pRc input is completely eliminated by hyperoxia and, on the
other hand, secondary effects may stimulate ventilation after the initial
drop, masking any further hyperoxia-mediated decrease (e.g.
Ward, 1994). However, we
investigated the ventilatory decline in response to 100% oxygen under the same
conditions before and after the RMT/control period and found no difference in
the control group, so we believe that, after RMT, we observed a true reduction
in pRc sensitivity, at least with respect to the O2
drive mediated by the pRc.
This 5.8% reduction in pRc sensitivity after RMT supports the
hypothesis that RMT, which simulated the high rates of ventilation occurring
during endurance exercise, can by itself cause a reduction in
the pRc response. As the pRc are generally believed to
contribute to augment E during
exercise (reviewed by Weil and Swanson,
1991
), we expected to find a reduction in the exercise
E of the RMT group, given the
attenuated pRc sensitivity following RMT. However, exercise
E was not significantly changed
following the RMT period and there was no significant relationship between any
change in the steady-state
E of the
cycling endurance test and the change in pRc response in the RMT
group. Considering those endurance athletes that have a lower peripheral
chemosensitivity and a lower exercise ventilatory response (e.g.
Weil and Swanson, 1991
), our
findings suggest that the lower
E
during exercise is not a direct result of the lower peripheral
chemosensitivity. Results of the present study indicate that the
pRc contributed minimally to the regulation of ventilation during
aerobic exercise. This is consistent with the theory that the pRc
only serve to `fine tune' the ventilatory response to exercise
(Dempsey et al., 1995
), and
other inputs to the medullary respiratory center may play a more prominent
role in the control of breathing during exercise.
In conclusion, the high levels of ventilation achieved during exercise, as
simulated by RMT in this study, significantly reduced the pRc
sensitivity during moderate-intensity exercise and extended the time to
exhaustion during high-intensity constant-load cycling exercise. Nevertheless,
the lack of a significant correlation between the decrease in pRc
sensitivity and exercise E suggests
that the role of the pRc in the control of ventilation during
normoxic exercise is minimal.
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Acknowledgments |
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References |
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