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Vol. 83, Issue 5, 1641-1647, 1997
1 Division of Pediatric Pulmonology, Childrens Hospital Los Angeles, and Department of Pediatrics, University of Southern California School of Medicine, Los Angeles, California 90027; and 2 Constance S. Kaufman Pediatric Pulmonary Research Laboratory, Departments of Pediatrics and Physiology, Tulane University School of Medicine, New Orleans, Louisiana 70112
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Shah, Ashish R., Thomas G. Keens, and David Gozal.
Effect of supplemental oxygen on supramaximal exercise performance and recovery in cystic fibrosis. J. Appl.
Physiol. 83(5): 1641-1647, 1997.
The effects of
supplemental O2 on recovery from
supramaximal exercise and subsequent performance remain unknown. If
recovery from exercise could be enhanced in individuals with chronic
lung disease, subsequent supramaximal exercise performance could also be improved. Recovery from supramaximal exercise and subsequent supramaximal exercise performance were assessed after 10 min of breathing 100% O2 or room air
(RA) in 17 cystic fibrosis (CF) patients [25 ± 10 (SD) yr
old, 53% men, forced expired volume in 1 s = 62 ± 21%
predicted] and 17 normal subjects (25 ± 8 yr old, 59% men,
forced expired volume in 1 s = 112 ± 15% predicted). Supramaximal
performance was assessed as the work of sustained bicycling at a load
of 130% of the maximum load achieved during a graded maximal exercise.
Peak minute ventilation
(
E) and
heart rate (HR) were lower in CF patients at the end of each
supramaximal bout than in controls. In CF patients, single-exponential
time decay constants indicated faster recovery of HR
(
HR = 86 ± 8 and 73 ± 6 s in RA and O2,
respectively, P < 0.01). Similarly, fast and slow time constants of two-exponential equations providing the
best fit for ventilatory recovery were improved in CF patients during
O2 breathing
(
= 132.1 ± 10.5 vs. 82.5 ± 10.4 s;
= 880.3 ± 300.1 vs. 368.6 ± 107.1 s,
P < 0.01). However, no such improvements occurred in controls. Supramaximal performance after O2 improved in CF patients (109 ± 6% of the 1st bout after O2 vs. 94 ± 6% in RA, P < 0.01).
O2 supplementation had no effect on subsequent performance in controls (97 ± 3% in
O2 vs. 93 ± 3% in RA). We
conclude that supplemental O2
after a short bout of supramaximal exercise accelerates recovery and
preserves subsequent supramaximal performance in patients with CF.
obstructive lung disease; gas exchange
INTRODUCTION WITH ADVANCING LUNG disease, individuals with cystic
fibrosis (CF) are more likely to develop significant
O2 desaturation during aerobic
exercise (17, 19). O2
supplementation during exercise in CF patients decreases heart rate
(HR) and minute ventilation ( O2 supplementation between bouts
of exercise could provide a more practical approach. Arterial
O2 content and arterial
O2 output are decreased in
individuals with chronic lung disease (CLD) (28). As a consequence,
O2 debt may be increased during exercise in these individuals. It is therefore possible that
administration of supplemental O2
during the recovery period from a maximal or supramaximal exhaustive
exercise bout could accelerate recovery rates of muscle energy stores,
reduce the discomfort after exercise, and possibly improve subsequent
anaerobic exercise performance.
Robbins et al. (21) reported that, in normal, well-trained individuals,
supplemental O2 administered
during the recovery period after submaximal or maximal aerobic exercise
had no significant effect on recovery patterns of HR or
In the present study we hypothesized that administration of
supplemental O2 during the
recovery period after a short bout of anaerobic exercise would
accelerate HR and
MATERIALS AND METHODS
E)
requirements (15, 18). Although O2
supplementation may be beneficial during exercise, it is undoubtedly
cumbersome and impractical to use during routine daily activities or
during exercise training.
E. Peak
O2 uptake
(O2 max) also remained
unaffected during exercise after administration of
O2 (21). In well-trained healthy
individuals, however, respiratory mechanics do not limit exercise, and
one would expect a rapid return of
E and HR to
levels where little or no discomfort is present. In contrast, in
patients with obstructive lung disease such as in CF, ventilatory
function and gas exchange are impaired (11). This could lead to
prolonged recovery and respiratory discomfort, which ultimately could
lead to unwillingness to pursue regular exercise training. Therefore,
O2 supplementation could be
beneficial in accelerating the recovery period of patients with CF.
E recovery in CF patients and potentially lead to subsequent improvements in anaerobic exercise performance.
E,
O2 consumption (O2),
CO2 production
(CO2), respiratory exchange
ratio
(CO2/O2), and ventilatory equivalents for O2
(E/O2)
and CO2
(E/CO2). HR was continuously monitored by electrocardiogram and
O2 saturation (SpO2) by pulse
oximeter (Nellcor, Hayward, CA).
Graded maximal exercise testing.
This initial test was designed to establish
O2 max of each
subject and allow determination of the exercise load to be applied during supramaximal exercise. After assessment of baseline
cardiorespiratory measures at rest, the test consisted of pedaling an
electronically braked bicycle ergometer starting at zero load with
increases in load of 8 W (50 kpm/min) every 30 s until the subject was
unable to sustain a pedaling frequency of 
40 rpm for the assigned
load (8, 10, 17). Because pedal frequency may alter
O2 kinetics (3), subjects
were encouraged to maintain a pedaling frequency of 60-70
revolutions/min (rpm) throughout the test to minimize potential inter-
and intraindividual variability in performance. The load at which the
test was discontinued was recorded, and O2 max and anaerobic
threshold were determined from cardiorespiratory records (29). Subjects
were allowed to rest for 2 h before further testing.
Supramaximal exercise testing.
Subjects underwent two series of supramaximal exercise tests. Each
series consisted of two bouts of supramaximal exercise, separated by 10 min of passive recovery. The two bouts in each series were performed at
a workload ~130% of the workload recorded at
O2 max during the
graded maximal exercise test. During one of the two series, subjects
breathed room air during the 10-min rest period. During the second
series, subjects breathed 100% O2
during the rest period. The order in which the gas mixture was
delivered (room air vs. 100%
O2) was randomized, and subjects were blinded to the gas mixture given.
Initially, baseline cardiorespiratory parameters were monitored while
subjects sat immobile on the cycle ergometer and breathed room air.
When values become stable over a period of 60 s, zero-load pedaling was
allowed for 1 min at 60-70 rpm, after which subjects pedaled at
the designated load (130% of
O2 max).
E, HR, and pulse oximetry were recorded during supramaximal exercise testing and
during recovery in room air and 100%
O2. Subjects were encouraged to
maintain a pedaling frequency of ~70 rpm throughout the test. The
test was discontinued when the subject could no longer maintain a
pedaling frequency 40 rpm. After the first bout of supramaximal exercise, subjects were allowed to rest on the cycle ergometer while
breathing room air or 100% O2
through the mouthpiece from a 100-liter Douglas bag. After 9 min,
subjects began pedaling at zero load at a frequency of ~70 rpm while
still breathing the predetermined gas mixture. At 10 min the load was
increased to 130% of
O2 max, and all
subjects were switched to room air. The test was discontinued when
subjects could not maintain a pedaling frequency 40 rpm.
Within 2 wk of completion of this exercise protocol, subjects underwent
the second series of supramaximal exercise testing. The gas mixture not given for the
first series was used in the second series.
Supramaximal performance (in kpm) was assessed as the time (in minutes)
subjects could sustain bicycling at 130%
O2 max multiplied by the workload (kpm/min). The second exercise bout was
expressed as a percentage of the first supramaximal exercise bout in
each series.
Data analysis.
Unpaired t-tests were used to compare
clinical characteristics and pulmonary function values between CF
patients and control subjects. Unpaired
t-tests were used to compare
differences during supramaximal exercise between the two groups
(supramaximal performance, SpO2, peak HR,
and peak
E).
Individual HR recovery rates
(HR) during 100%
O2 or room air breathing were
assessed by computer curve-fitting procedures employing a
single-exponential equation, as previously described (23). Nonlinear
techniques were used to calculate the parameters of the equation
|
HR = 1/k) was used to quantify the
recovery time and indicates the time necessary to achieve 63.2% of the
difference between peak and baseline HR values. A two-exponential fit
was also applied to the cardiac recovery data. However, no significant
improvements in the goodness of fit were found between the
monoexponential equation and the two-exponential equation using the
F test (12).
In contrast to HR recovery, improved goodness of the fit was found for
a two-order exponential decay equation when individual E recovery
was assessed. Thus the exponential equation used was as follows
|
= 1/k1 and
= 1/k2)
were used to compare
E recovery
patterns in CF and control groups.
Two-way analysis of variance for repeated measures and the Newman-Keuls
multiple-range test for multiple comparisons were employed for
assessment of differences between CF and control groups. Two-tailed
paired t-tests were used to evaluate
potential differences within the CF group or the control group
(recovery in room air vs. 100% O2
and comparison of 2nd bout vs. 1st bout). In all tests,
P < 0.05 was considered significant.
RESULTS
Seventeen CF patients and 17 normal subjects were studied. Most CF patients showed moderate obstructive disease by pulmonary function testing, and all had some degree of hyperinflation. Control subjects had normal pulmonary function tests. CF patients had significantly decreased weight and lean body mass. Resting SpO2 was slightly lower in CF patients. Clinical characteristics, pulmonary function values, and anthropometric data are shown in Table 1.
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E, maximum HR,
and O2 max were lower
in CF patients. Anaerobic threshold occurred at a lower
O2 in CF patients than in
normal subjects. No significant O2
desaturation occurred in CF patients or control subjects (Table 2).
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E and HR were
also decreased in CF patients at the end of supramaximal exercise
compared with normal subjects (Table 3). No
O2 desaturation was observed
during supramaximal exercise in CF patients or control subjects.
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E recovery
during 100% O2 and room air
breathing in one CF patient is shown in Fig. 1. For CF
patients and control subjects, the sum of two exponentials provided a
significantly better fit of the group mean
E recovery
data than did a single exponential. For CF patients,
F = 236 and
P < 0.00001; for controls, F = 248 and
P < 0.00001. In room air the fast
() and the slow
() time decay constants for ventilation were longer in CF patients than in
control subjects (Fig. 2). However, although no changes in
or
occurred in control subjects when
O2 was administered during
recovery, significant reductions in
and
were observed in CF patients, indicating faster recovery with
O2 (Fig. 2).
E) at 15-s
intervals during recovery in room air (
) and 100%
O2 (
) in a cystic fibrosis
patient. Lines correspond to 2-exponential decay equations calculated
for each recovery. Fast time constants
() were 47.8 and 35.1 s in room air and O2,
respectively; slow time constants
() were 178.3 and 158.7 s in room air and
O2, respectively.
and
in cystic fibrosis (CF) patients and matched controls (CON) after
supramaximal exercise, as derived from individual 2-exponential
curve-fitting equations. Values are means ± SE. * Room air
vs. 100% O2 in CF for
,
P < 0.01. # Room air (RA) vs. 100%
O2 in CF for
, P < 0.03.
Similarly, time decay constants for HR (
HR) also indicated faster
recovery of HR in CF patients during
O2 breathing, whereas this effect
was absent in controls (Fig. 3).
However, no correlations were found between pulmonary
function (mean forced expiratory flow during the middle half of forced
vital capacity and forced expired volume in 1 s) and time recovery
constants
, ,
and HR in room air or
O2.
HR) in CF patients and
matched controls after supramaximal exercise, as calculated from
single-exponential equation curve fitting. Values are means ± SE.
* Room air vs. 100% O2 in
CF for HR,
P < 0.01.
No O2 desaturation was observed during recovery from supramaximal exercise in CF patients or control subjects. Subsequent supramaximal performance. In CF patients, supramaximal performance decreased from the first bout to the second bout during recovery in room air, whereas it improved albeit slightly after recovery in O2 (Fig. 4, Table 3). In normal subjects no performance differences were found in the bout after recovery in O2 or room air (Fig. 4, Table 3; CF vs. control: P < 0.001, 2-way analysis of variance).
DISCUSSION
We have demonstrated that administration of supplemental
O2 after supramaximal exercise
accelerates recovery of HR and
E in CF
patients. Also, subsequent supramaximal exercise performance improves
in CF patients compared with control subjects when 100% supplemental
O2 is administered between
anaerobic exercise bouts. In control subjects, such beneficial effects
of O2 were absent.
Aerobic and anaerobic exercise performances are decreased in CF (4, 6, 13, 15, 18). Major emphasis has been given to the improvement of aerobic exercise capacity in CF (19). Anaerobic exercise, rather than aerobic exercise, may be of more practical importance in CF, since routine daily activities often involve bouts of short anaerobic exercise. In addition, aerobic exercise training may not always improve baseline pulmonary function or increase weight gain in CF patients (27). Anaerobic exercise training such as weight lifting, however, significantly improves weight and muscle strength (24, 27). Similarly, interval training, which employs repeated bouts of anaerobic exercise, leads to improvement of aerobic exercise performance in athletes and in patients with airway obstruction (25). Therefore, optimization of anaerobic training conditions in CF patients by accelerating cardiopulmonary recovery using supplemental O2 could ultimately lead to improved performances and exercise tolerance, as well as reduced discomfort during daily tasks.
The effects of administering supplemental
O2 during aerobic exercise testing
in CF patients has been studied, although the data available are not
extensive. Previous work with CF patients from our laboratory indicated
that supplemental O2 at an
inspired O2 fraction of 0.3 during
graded exercise increased
O2 max and O2 pulse and reduced the severity
of O2 desaturation (15). In a
similar study, Nixon et al. (18) found that supplemental
O2 administered during graded
exercise minimized O2 desaturation in CF patients, who would otherwise normally desaturate during exercise. However, in contrast to the report of Marcus et al. (15),
Nixon and co-workers found no improvements in peak work capacity or
O2 in CF. Nixon and
co-workers did note that, for a given workload, CF patients given
supplemental O2 during exercise performed at lower
E and HR
during exercise than those breathing room air. Although impractical
during daily activities, it appears that supplemental
O2 during exercise in patients
with obstructive lung disease may be beneficial in reducing HR and
ventilatory outputs.
Despite widespread use of supplemental
O2 by professional athletes during
inactivity periods in a competition, data on the effects of
supplemental O2 on the recovery
from aerobic exercise and on subsequent performance are scarce. Robbins
et al. (21) administered 100% O2
after bouts of submaximal and maximal aerobic exercise in healthy male
athletes and found that breathing 100% O2 had no significant effect on
the recovery kinetics of HR or E.
Furthermore, subsequent exercise performance was unaltered by
O2 supplementation (21). The study
by Robbins et al., however, involved healthy athletes.
In well-trained individuals, supplemental O2 would not be expected to
accelerate recovery, since exercise is not primarily limited by
pulmonary mechanics.
Assessment of the kinetics of recovery from a short bout of exercise
indicates that time constants depend on the intensity of the exercise
being performed (1). Indeed, Armon et al. (1) found significant
increases of
with increasing work intensity in healthy adults and also reported that
when the workload corresponded to 125% of the anaerobic threshold, a
two-exponential rather than a single-exponential equation provided a
better fit for recovery. Our findings in this study indeed concur with
such data (1). Similar increases in
HR with workload were also
found (2). Thus precaution to match individual exercise workloads as a
constant percentage of the maximal load achieved during the graded
exercise test appears essential whenever comparisons of recovery
kinetics are contemplated across experimental
groups.
In this study we addressed the effects of supplemental
O2 on recovery from anaerobic
exercise and subsequent anaerobic performance. As in the study by
Robbins et al. (21), no significant improvements in HR or ventilatory
kinetics were found in the control group. In contrast, CF patients in
our study achieved faster recovery of HR and
E when
O2 was administered, and they were
able to enhance their subsequent performance. Although hyperoxic
inhibition of peripheral chemoreceptor tone could be advanced as one
possible explanation for accelerated decreases in cardioventilatory
outputs, this explanation appears unlikely, since it would be expected to occur in CF patients and control subjects. However, accelerated recovery rates were present in CF patients only. Another alternative explanation for the faster HR recovery could involve improvements in
cardiac output associated with O2
breathing in CF patients. This possibility is unlikely, since there was
no evidence of cardiac limitation during exercise and
HR values in room air were
similar in CF patients and controls.
O2-induced alterations in regional capillary bed resistance such that blood flow would be preferentially directed to exercised muscles could lead to faster lactate removal and
pH normalization, which in turn could reduce muscle afferent nerve
input and sympathetic recruitment.
In individuals with CLD and congestive heart failure (CHF), altered skeletal muscle metabolism has been demonstrated using 31P nuclear magnetic resonance spectroscopy (22, 28). Studies have shown reduced phosphocreatine-to-inorganic phosphate ratios in exercising muscle of individuals with CLD and CHF, which may reflect impaired oxidative metabolism (28). Arterial O2 output (cardiac output multiplied by arterial O2 content) has also been found to be reduced in CHF and CLD (28). It has been suggested that the reduced muscle metabolism in these subjects may be secondary to a number of factors, including reduced blood flow, impaired O2 delivery to muscle, and reduced mitochondrial oxidative capacity (28). In healthy individuals, energy for anaerobic exercise can come from aerobic as well as anaerobic sources (16). The energy needed for anaerobic exercise in individuals with chronic respiratory impairments may come from earlier activation of anaerobic glycolysis and increased proportion of energy from anaerobic glycolysis compared with normal individuals (11). Therefore, in individuals with CLD, a larger proportion of the overall energy produced originates from anaerobic glycolysis, such that increased O2 debt will be incurred during short, exhaustive bouts of exercise. Supplemental O2 could accelerate recovery by helping overcome some of these deficits. For example, an immediate consequence of O2 supplementation would be a significant increase in arterial O2 content if our CF patients had demonstrated significant O2 desaturations during supramaximal exercise, in contrast to control subjects, in whom the increase in arterial O2 content would have been of minor proportions. However, major decreases in O2 saturation did not occur in our CF patients, suggesting that mechanisms other than limitations in blood O2 content could be operative in this context. Higher arterial PO2 during the recovery period could accelerate the rate of muscle energy stores repletion, which might be compromised in CF because of intrinsic mechanisms inherent to CF or, more likely, as a result of severe deconditioning in these patients. Although our study design cannot provide definitive answers regarding the mechanisms underlying improved recovery from supramaximal exercise in CF, several mechanisms are postulated. Among these, improved muscle microcirculatory flows due to shifts in vascular bed resistances with preferential flow delivery to exercised muscles, improved lactate removal kinetics from exercised muscles, thereby reducing metabotropic type III/IV fiber recruitment more rapidly and thus diminishing ventilatory stimulation by such fibers, improved intracellular muscle energy recovery kinetics, and/or differences in central drive changes due to O2 breathing could be involved in O2-associated faster recovery kinetics in CF. Delineation of which of theses potential mechanisms underlies the improvement in cardiorespiratory recovery in CF patients with supplemental O2 during the recovery period awaits further study.
Several methodological issues deserve comment. Improvements in lung function in our CF patients during the period between the two supramaximal exercise series could exert profound effects on overall performance. However, our CF patients were clinically stable and were randomly assigned to receive O2 or room air during the recovery period. Indeed, 9 of the 17 CF patients received O2 in their first series. Similarly, a training effect could have induced changes in performance over time. Such an effect is unlikely, since the only improvements in performance were those associated with O2 supplementation. Finally, a placebo effect could modify the motivation during the exercise bouts. However, CF patients and control subjects were unaware of the gas mixture being administered, and there were absolutely no visual cues in the laboratory setting that may have been conducive to an assumption in either direction.
In summary, supplemental O2 does not modify the recovery from supramaximal exercise and will not modify subsequent supramaximal performance in healthy individuals. However, in CF patients, accelerated recovery and improved supramaximal performance ensue. We speculate that optimization of anaerobic exercise training by the administration of supplemental O2 during recovery may not only enhance compliance with training schedules but also lead to increased anaerobic and aerobic exercise tolerance, resulting in overall improvements in the quality of life.
ACKNOWLEDGEMENTS
The authors thank the technicians of the Pulmonary Physiology Laboratory at Childrens Hospital Los Angeles for technical support and all participants for their enthusiastic cooperation.
FOOTNOTES
Address for reprint requests: D. Gozal, Sect. of Pediatric Pulmonology, SL-37, Dept. of Pediatrics, Tulane University School of Medicine, 1430 Tulane Ave., New Orleans, LA 70112.
Received 25 June 1996; accepted in final form 27 June 1997.
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