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John Rankin Laboratory of Pulmonary Medicine, University of Wisconsin, Madison, Wisconsin 53705
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Babcock, Mark A., David F. Pegelow, Bruce D. Johnson, and
Jerome A. Dempsey. Aerobic fitness effects on exercise-induced low-frequency diaphragm fatigue. J. Appl.
Physiol. 81(5): 2156-2164, 1996.
We used
bilateral phrenic nerve stimulation (BPNS; at 1, 10, and 20 Hz at
functional residual capacity) to compare the amount of exercise-induced
diaphragm fatigue between two groups of healthy subjects, a high-fit
group [maximal O2
consumption (
O2 max) = 69.0 ± 1.8 ml · kg
1 · min1,
n = 11] and a fit group
(O2 max = 50.4 ± 1.7 ml · kg1 · min1,
n = 13). Both groups exercised at
88-92% O2 max
for about the same duration (15.2 ± 1.7 and 17.9 ± 2.6 min for
high-fit and fit subjects, respectively,
P > 0.05). The supramaximal BPNS test showed a significant reduction (P < 0.01) in the BPNS transdiaphragmatic pressure (Pdi) immediately
after exercise of 
23.1 ± 3.1% for the high-fit group and
23.1 ± 3.8% (P > 0.05)
for the fit group. Recovery of the BPNS Pdi took 60 min in both groups.
The high-fit group exercised at a higher absolute workload, which
resulted in a higher CO2
production (+26%), a greater ventilatory demand (+16%) throughout the
exercise, and an increased diaphragm force output (+28%) over the
initial 60% of the exercise period. Thereafter, diaphragm force output
declined, despite a rising minute ventilation, and it was not different
between most of the high-fit and fit subjects. In summary, the high-fit
subjects showed diaphragm fatigue as a result of heavy endurance
exercise but were also partially protected from excessive fatigue,
despite high ventilatory requirements, because their hyperventilatory
response to endurance exercise was reduced, their diaphragm was
utilized less in providing the total ventilatory response, and possibly
their diaphragm aerobic capacity was greater.
low-frequency fatigue; aerobic capacity; diaphragm force output
INTRODUCTION THIS STUDY WAS AIMED at determining the effects of
aerobic capacity or maximal O2
consumption ( We hypothesized that the subjects with greater aerobic capacity will be
protected completely or at least partially from exercise-induced diaphragm fatigue. In the present study, we have used bilateral phrenic
nerve stimulation (BPNS) (5) to provide more objective and specific
measures of diaphragm fatigue in 24 normal subjects of widely varying
levels of habitual activity and
METHODS
O2 max) on
exercise-induced diaphragm fatigue. Heavy endurance exercise to
exhaustion has been shown to cause significant reductions in the force
production of the diaphragm in response to low-frequency supramaximal
phrenic nerve stimulation (2, 3, 18). This fatigue of the diaphragm is
in part determined by the amount of force output by the diaphragm during exercise (3). Because the highly trained subject is capable of
sustaining endurance exercise at greater-than-average metabolic rates,
ventilatory outputs, and inspiratory muscle force outputs, these
increased requirements may make the athlete more susceptible to
exercise-induced diaphragm fatigue. On the other hand, the endurance of
the respiratory muscles, as judged by the maximum ventilation
sustainable to the point of volitional task failure, is generally
greater in the endurance athlete (8, 10, 13) and increases in formerly
sedentary subjects who undergo whole body physical training (27). These
adaptations of the respiratory muscles to whole body training may
protect the athlete from exercise-induced diaphragm fatigue. In fact,
Coast et al. (11) claim, on the basis of measurements of maximal
volitional inspiratory occlusion pressure before and after exercise in
the trained and untrained subject, that highly trained subjects were completely protected from exercise-induced respiratory muscle fatigue.
O2 max who were
subjected to whole body endurance exercise of comparable intensity and
duration.
O2 max by use of a
progressive short-term test to volitional exhaustion, as outlined
previously (19). Nineteen of the subjects ran on a treadmill, and five
exercised on a stationary cycle ergometer.
The endurance exercise session was conducted on a separate day. The
various BPNS measures were completed before exercise (baseline measures). Subjects warmed up briefly with light exercise and were then
quickly brought up to a workload that required 95%
O2 max, which was
maintained until volitional exhaustion. Immediately after exercise the
BPNS measures were repeated (within 6-12 min); this was also done
30 min after exercise and then every 30 min until the BPNS Pdi
measurements returned to the baseline.
During the exercise at 3-min intervals and at exercise termination, the
subjects were asked to rate whole body effort using the Borg 10-point
scale (7). Each test was terminated at the subject's volitional
fatigue. During exercise, expired gases, flow, volumes, Pes, Pga, Pdi,
and mouth pressure were monitored continuously. Blood
O2 saturation was measured
throughout exercise by ear oximetry (Hewlett-Packard). At 2- to 3-min
intervals, inspiratory capacity efforts were made in duplicate to
estimate EELV (20). For analysis, data from 20-30 consecutive
breaths were averaged at 3-min intervals during the exercise. A mean
value for the time integral of the inspiratory Pdi
(
Pdi) and the mean time integral of the
inspiratory Pes (Pes) were calculated over the
20- to 30-breath sample by the computer. Each of the time integrals was
multiplied by the breathing frequency (f) to provide results of force
output of the diaphragm
(Pdi · f) and all the
inspiratory muscles (Pes · f).
Statistical analyses were done using the statistical program Systat.
Values are means ± SE. One-way analysis of variance with repeated
measures was used to determine differences in mean values over the
duration of the exercise and recovery period. Student's unpaired
t-test was used to detect differences
between mean values of the high-fit and fit groups. The level of
significance was set at P < 0.05.
RESULTS
The subjects were divided into two groups on the basis of a
O2 max of 60 ml · kg1 · min1
(Table 1). The high-fit group
O2 max
(n = 11) ranged from 61.1 to 78.6 ml · kg1 · min1,
and the fit group
O2 max
(n = 13) ranged from 39.5 to 58.6 ml · kg1 · min1.
The results of the routine pulmonary function tests are also reported
in Table 1. There was no difference between the high-fit and fit
groups, except the high-fit group had a higher MVV than the fit group.
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23.7 ± 3.1% in the
high-fit group and 23.1 ± 3.8% in the fit group
(P > 0.05). All but 3 of 24 subjects
showed a >15% decrease in the diaphragm fatigue index after
endurance exercise at an intensity >90%
O2 max.
) and fit (
) groups to supramaximal
bilateral phrenic nerve stimulation (BPNS) with use of single-twitch (A): 10-Hz (B); and 20-Hz (C)
frequencies before exercise and during postexercise (Post-Exer)
recovery. Pdi, transdiaphragmatic pressure. Values are group means ± SE. 
Significantly
different from preexercise (pre-exerc) value,
P < 0.05.
The percent change in the BPNS Pdi at 6-12 min after exercise at each of the three stimulation frequencies is shown for all subjects in Fig. 2 as a function of their
O2 max. The magnitude of the reduction in BPNS Pdi after exercise varied between subjects and
with different stimulation frequencies. However, at any given BPNS
stimulation frequency, the exercise-induced decrease in BPNS Pdi was
not systematically different among subjects with different O2 max.
) in BPNS Pdi from before to
(immediately) after exercise in response to single-twitch (n = 24), 10-Hz
(n = 24), and 20-Hz
(n = 21) frequencies. , High fit;
, fit. O2 max,
maximal O2 uptake.
The group mean values for the supramaximal BPNS Pdi and the relative contributions of Pga and Pes to Pdi at each stimulation frequency are shown in Table 2. No changes were found after exercise in the amplitude of the left or the right M wave; nor were there changes in the lung volume at which the stimulations were done (data not shown). The fall in the BPNS Pdi after the endurance exercise was due to a greater decrease in the absolute Pes component, but the relative contribution of Pes to Pdi remained constant at all three stimulation frequencies, as did the Pga-to-Pdi ratio (Table 2). The ratios reported here were similar to reports in the literature obtained in control conditions and after inspiratory resistive loading to the point of task failure (31). Changes in the time to peak tension and RT1/2 of the "twitch" after exercise were small and not significant.
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O2 max (88.8% at start
of exercise and 97.8% at end of exercise). There was also no
difference in exercise duration between the two groups: the high-fit
group exercised for 15.2 ± 1.7 min and the fit group for 17.9 ± 2.6 min (P > 0.40). Even though the
high-fit and fit groups exercised at the same relative intensity
(percentage of
O2 max), the absolute
O2 consumption and
CO2 production
(CO2) were 25.6 and 26.7%
higher, respectively, in the high-fit group (P < 0.05). The higher metabolic
cost of the exercise for the high-fit group required a 16% higher
minute ventilation
(E; P < 0.056). Both groups showed an
increase in
E-to-CO2
ratio with time during exercise, although the mean
E-to-CO2
ratio (Fig. 3B) averaged 20% lower
in the high-fit group throughout exercise
(P < 0.05). At the end of exercise
the rating of perceived exertion, on a 10-point Borg scale, was 9.8 ± 0.1 for the high-fit group and 9.9 ± 0.1 for the fit group.
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O2 max) for
high-fit () and fit () groups.
CO2, CO2 production;
E, minute
ventilation;
VT/TI,
mean inspiratory flow rate;
Pdi · f, diaphragm force
output; Pes · f, total
inspiratory muscle force output.
Significant difference
between groups, P < 0.05.
Inspiratory muscle force output during exercise. Exercise effects on the time integrals for Pes and for Pdi are shown for the fit and high-fit groups throughout exercise in Fig. 3, and mean values for the last 3 min of exercise are summarized in Table 3. The mean
Pes · f increased in both
groups throughout exercise, but it was substantially greater in the
high-fit group throughout the exercise time.
Pdi · f was greater in the
high-fit group than in the fit group up to 60% of the total exercise
time. Thereafter Pdi · f
declined with time in the high-fit group but remained constant in the
fit group, so that mean values over the final 40% of the exercise
duration were not different between groups.
Figure 4 shows
Pdi · f during tidal breathing
vs. O2 max
for each subject at the beginning, in the middle, and at the end of
exercise. We found significant correlations of force output with
O2 max over the time
course of the exercise. These plots, across the continuum of
O2 max,
emphasize the substantial overlap in
Pdi · f among subjects
throughout the duration of exercise. Also five of the high-fit subjects
experienced exceptionally high
Pdi · f over the latter 40% of
the exercise. These same five subjects did not show any greater
diaphragm fatigue than the other high-fit or fit subjects (Fig. 2).
Pdi · f at 3 different times of exercise [20 (A), 60 (B), and
100% (C) of total exercise time]. Total exercise
time = 15.2 ± 1.7 and 17.9 ±2.6 min for high-fit and
fit groups, respectively.
Pdi · f and
O2 max are expressed
per kilogram of body weight. , High fit; , fit.
Flow- and pressure-volume relationship. Figure 5 shows the mean flow-volume and Pes-volume relationships during exercise for the high-fit and fit groups. The high-fit group was progressively more flow limited during expiration throughout the exercise [8.0% of tidal volume (VT) flow limited at 3 min vs. 50.8% at the end of exercise]. These subjects also reached or slightly exceeded their maximal effective expiratory pressure generation over 50% of their expired VT during the last 3 min of exercise. In the fit group VT was not flow limited during expiration throughout exercise.
The high-fit group reached 31% (at the beginning of exercies), 49% (in the middle of exercise), and 90% (in the last 3 min of exercise) of their dynamic PcapI during tidal inspiration at peak Pes and at high lung volumes. In the fit group, peak inspiratory Pes reached during exercise were 37% (beginning), 38% (middle), and 40% (end) of PcapI.
DISCUSSION
Our data showed that the high-fit group was not protected by an increased aerobic capacity from exhibiting exercise-induced low-frequency diaphragm fatigue after intense whole body endurance exercise. This is in contrast to other reports that showed no changes in maximal volitional tests of inspiratory muscle force output (6, 11) in highly trained athletes compared with untrained subjects after severe exercise to exhaustion. On the basis of this evidence, we had hypothesized that the high-fit group would not have exhibited a substantial amount of low-frequency diaphragm fatigue after intense whole body endurance exercise. We reject this hypothesis now, because the high-fit and fit groups experienced similar amounts of exercise-induced low-frequency diaphragm fatigue at all stimulation frequencies immediately after whole body endurance exercise.
Why were the high-fit subjects able to exercise at a higher absolute workload and a resultant greater ventilatory requirement and not incur a greater level of low-frequency diaphragm fatigue? There are at least two possibilities: 1) despite the higher ventilatory requirement, the high-fit group may have utilized their diaphragm during endurance exercise to the same extent as the fit group, and 2) the aerobic capacity of the diaphragm of the high-fit group was appropriately increased similar to that of the limb locomotor muscles. We now discuss each of these possibilities with reference to the current literature.
Diaphragm force production during whole body exercise. Did all the subjects regardless ofO2 max experience the
same amount of exercise-induced low-frequency diaphragm fatigue because
the Pdi · f was similar? We
know that the Pdi · f increased
four to five times above rest values in the first few minutes after
exercise onset (2, 3, 18); as exercise continued the
Pdi · f declined slightly,
despite further time-dependent increases in
E
and Pes · f. The group mean
data for Pdi · f during
exercise showed that the high-fit group produced more force (+28%)
during the first 60% of the exercise time, but over the last
40-50% of the exercise diaphragm force production was not
different from the fit group (Figs. 3 and 4). Thus the higher
ventilatory demand in most high-fit subjects was (with some notable
exceptions, see below) dependent on increased recruitment of accessory
inspiratory muscles as exercise time progressed. Because force
development by the diaphragm is an important determinant of
exercise-induced diaphragm fatigue (3), this apparent sparing of
Pdi · f in many highly fit
subjects would be expected to alleviate some of the fatigue, despite a
higher ventilatory requirement.
We also emphasize that the ventilatory output in the high-fit subjects
was not increased in proportion to their higher absolute work rate and
CO2. That is, the
E-to-CO2
ratio remained lower throughout exercise in the high-fit group. This
reduced ventilatory requirement means that the requirement for force
output by all the inspiratory muscles would also not be increased in proportion to their higher exercise
CO2 in the highly trained subject. Our study does not address the cause of this reduced E-to-CO2
ratio in the high-fit athletes, although a similar finding has been
reported with short-term heavy exercise and attributed to reduced
levels of metabolic acidosis (21).
What does this leveling off of the
Pdi · f mean? It may be
indicative of a changing recruitment pattern of the inspiratory muscles
during intense endurance exercise in response to the onset of diaphragm
fatigue. Sieck and Fournier (28) found that the recruitment pattern of
the diaphragm muscle fibers followed the size principle, inasmuch as
the most fatigue-resistant type I fibers were recruited at low
ventilatory loads and moderately fatigue-resistant type IIa fibers were
recruited at moderate loads. The least fatigue-resistant type IIb
fibers were only recruited for nonventilatory behaviors such as
sneezing or gagging. Thus the very high ventilatory requirements during
exercise requiring greater and greater force development from the
diaphragm might make this muscle more susceptible to fatigue and
compromise its role as the major inspiratory muscle (see below). It is
appropriate, then, that diaphragm force production is inhibited perhaps
by feedback inhibition (17) and accessory inspiratory and expiratory muscles are recruited during prolonged exercise. Similar patterns of
selective recruitment of accessory muscles and derecruitment of the
diaphragm have been observed in animals undergoing severe resistive
loading (4). Furthermore, during prolonged exercise, the diaphragm
(along with the accessory inspiratory muscles) may act as a significant
force generator to displace the lungs and chest wall, but the
diaphragm, with its longer fibers, mixed fiber types, convex shape, and
high aerobic capacity, is ideally suited to serve as a major generator
of high velocities of shortening and flow rates. Hence, during the
latter stages of the endurance exercise, the diaphragm may actually
further increase its velocity of shortening and make greater
contributions to increasing flow rate at a time when its relative
contribution to force development is decreasing.
Does the diaphragm force production level off in prolonged exercise
because the diaphragm cannot produce more force or because it will not
produce the force it is capable of producing? Theoretically, at the
higher flow rates achieved during exercise, the velocity of shortening
of the diaphragm would also be quite high and thus would compromise the
muscle's capability for force production (1). However, we think this
is unlikely, because we have shown (3) that resting subjects were able
to volitionally increase and maintain diaphragm force production 78%
above the levels needed during endurance exercise and to sustain this
force for the same time period as the exercise. Therefore, the
diaphragm was capable of producing and sustaining a force production
and velocity of shortening at rates that were well above those
experienced during exercise without experiencing task failure. Whether
the diaphragm force production could be increased and sustained this
much during whole body exercise when other fatiguing influences are
present (3) remains to be determined.
We emphasize that our supramaximal BPNS test does not evaluate all the
important characteristics of diaphragm fatigue. Fatigue has been
defined as a reduction in the force-generating capacity of the muscle
resulting from activity under load that is reversible by rest (22a). By
this definition, most high-fit and fit subjects have clearly shown
low-frequency exercise-induced diaphragm fatigue. However, the BPNS
technique does not provide information on the velocity of shortening,
inasmuch as all stimulations are done at fixed lung volumes and are
assumed to be "quasi-isometric" contractions. Therefore, any
changes in the velocity of shortening of the diaphragm resulting from
the whole body endurance exercise remains to be determined, as do any
changes in this important characteristic of "fatigue" between
subjects of different aerobic capacity.
Response of the diaphragm to whole body exercise training.
A second explanation as to why the high-fit group could exercise at a
higher absolute workload and exhibit the same level of low-frequency
diaphragm fatigue as the fit group may be an enhanced diaphragmatic
aerobic capacity in the high-fit group. This explanation might apply
especially to those five high-fit subjects who clearly generated
greater force output of the diaphragm over most of the duration of the
endurance exercise and yet experienced the same amount of diaphragm
fatigue (Fig. 2). We would predict that the high-fit subjects also had
a greater Pdi relative to their absolute available capacity to generate
Pdi throughout heavy exercise, because the capacity for force
development (at any given lung volume or velocity of shortening) was
similar in the high-fit and fit subjects, and during tidal breathing in
exercise the lung volumes were similar and the inspiratory flow rates
were higher in the high-fit group.
Evidence has accumulated in animal models that supports the idea that
the aerobic capacity of the diaphragm does increase with intense and
prolonged physical training. Three types of changes in response to
whole body physical training have been documented to occur in the
diaphragm: 1) increased oxidative
enzyme activity (14, 16, 24), 2)
decreased diffusion distance from capillaries to muscle due to
decreased cross-sectional area of type I and type IIa muscle fibers
(14, 24, 25, 30), and 3) increased capillary density (15). Whether the human diaphragm responds in the
same way to whole body physical training or to increased aerobic
capacity has not been documented. The human studies have shown
improvements in volitional ventilatory muscle endurance performance
after whole body physical training, as shown by increased maximal
sustainable ventilation (10, 27) and greater MVV in trained than in
untrained subjects (8-10, 13). On the other hand, in the present
study and in others, no changes were found between normal-fit and
high-fit subjects in maximal inspiratory pressure generation at a fixed
lung volume (10, 23) or in the pressure-generating capacity of the
inspiratory muscles at any given flow rate (19).
We are uncertain whether increased aerobic capacity of the diaphragm
alone can explain our findings of similar diaphragm fatigue, despite
elevated Pdi · f in many of the high-fit subjects, because we know that more than just
Pdi · f per se causes
exercise-induced diaphragm fatigue (3). Other factors such as blood
flow distribution to diaphragm vs. locomotor muscle during endurance
exercise and circulating metabolites produced by the locomotor muscles
also contribute, and these factors might also very well be different in
the highly fit subject.
Pulmonary system limitations in the high-fit group: demand vs.
capacity.
Key determinants of the pulmonary system's capacity for maximum gas
transport during exercise include alveolar-capillary diffusion surface,
the flow-volume maximum envelope, and aerobic capacity of the
respiratory muscles. All these functions are placed under considerable
stress during heavy exercise in the high-fit subjects but appear to
have quite different susceptibilities to reaching limitation because of
their different capacities and degree of malleability in response to
physical training. In the case of diffusion limitation, many very
highly fit humans (1.5-2 times normal
O2 max) show
significant exercise-induced hypoxemia, presumably because their
extraordinary demand for O2
transport is not matched by enhanced diffusion surface area in the lung (12). This hypoxemia presents a significant limitation to systemic O2 transport and to
O2 max (26). Similarly,
the maximum flow-volume envelope is also unaltered in most highly fit
subjects (19). Accordingly, with their high metabolic and ventilatory
requirements, the highly fit individuals experience significant
expiratory flow limitation and increased ventilatory work, even in
moderately heavy exercise (Fig. 5), and many subjects will show
complete mechanical flow limitation to ventilation at maximum exercise (19). Incurring these high mechanical loads during exercise may
contribute to exercise limitation in the high-fit subjects, perhaps via
high metabolic and blood flow requirements by the respiratory muscles
or by mechanical constraint on alveolar ventilation. However, the
actual contribution of these factors to exercise and ventilatory
limitation remains controversial and unresolved.
Exercise-induced diaphragm fatigue as a third potential pulmonary
system limitation presents quite differently in these comparisons of
demand to capacity than do the diffusion or flow-volume limitations. First, healthy young adult subjects of all fitness levels and O2 max tested
to date experienced significant exercise-induced diaphragm fatigue (as
shown by a reduced force production in response to BPNS), so long as
exercise was of sufficient intensity and duration (Fig. 2). In other
words, there was no specific threshold of
O2 max,
ventilatory requirement, or
Pdi · f during the heavy
endurance exercise below which diaphragm fatigue did not occur in
healthy subjects (Fig. 1). In a sense then, the demand for sustained
force output by the diaphragm during exercise exceeded the muscle's
aerobic capacity in all healthy subjects. However, this reduction in
force output of a single, albeit primary, inspiratory muscle clearly
did not cause global respiratory muscle task failure or inadequate
alveolar ventilation (2, 3, 18).
In a recent study in which the inspiratory muscles were partially
mechanically unloaded, no differences were found in
E or exercise
performance time between normal and unloaded endurance exercise (22).
Assuming that this partial unloading may have alleviated diaphragm
fatigue, the authors interpreted these data to show that inspiratory
muscle fatigue had no effect on the ventilatory response or breathing
pattern during heavy endurance exercise. We agree and would speculate
that the significant consequence of the exercise-induced diaphragm
fatigue might be in providing a reordering of the pattern of
respiratory muscle recruitment.
Finally, the fact that the diaphragm and inspiratory muscles do show
significant increases in aerobic capacity in response to physical
training also distinguishes the chest wall from the lung in terms of
malleability. These chronic adaptations mean that the ratio of demand
to capacity in the diaphragm (during exercise) remains about the same
in trained and untrained subjects. Training effects on the respiratory
muscles may also be important in preventing a more marked
exercise-induced respiratory muscle fatigue and perhaps even task
failure, especially given the very high ventilatory requirements faced
in the highly trained during high-intensity endurance exercise.
ACKNOWLEDGEMENTS
This study was funded by the National Heart, Lung, and Blood Institute. M. A. Babcock is a Parker B. Francis Fellow of Pulmonary Research.
FOOTNOTES
Address for reprint requests: M. A. Babcock, Dept. of Preventive Medicine, 504 N. Walnut St., Madison, WI 53705.
Received 12 May 1995; accepted in final form 31 May 1996.
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