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J Appl Physiol 100: 1554-1562, 2006. First published January 19, 2006; doi:10.1152/japplphysiol.01389.2005
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Exercise-induced abdominal muscle fatigue in healthy humans

Bryan J. Taylor, Stephen C. How, and Lee M. Romer

Centre for Sports Medicine and Human Performance, School of Sport and Education, Brunel University, Middlesex, United Kingdom

Submitted 3 November 2005 ; accepted in final form 5 January 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The abdominal muscles have been shown to fatigue in response to voluntary isocapnic hyperpnea using direct nerve stimulation techniques. We investigated whether the abdominal muscles fatigue in response to dynamic lower limb exercise using such techniques. Eleven male subjects [peak oxygen uptake (VO2 peak) = 50.0 ± 1.9 (SE) ml·kg–1·min–1] cycled at >90% VO2 peak to exhaustion (14.2 ± 4.2 min). Abdominal muscle function was assessed before and up to 30 min after exercise by measuring the changes in gastric pressure (Pga) after the nerve roots supplying the abdominal muscles were magnetically stimulated at 1–25 Hz. Immediately after exercise there was a decrease in Pga at all stimulation frequencies (mean –25 ± 4%; P < 0.001) that persisted up to 30 min postexercise (–12 ± 4%; P = 0.001). These reductions were unlikely due to changes in membrane excitability because amplitude, duration, and area of the rectus abdominis M wave were unaffected. Declines in the Pga response to maximal voluntary expiratory efforts occurred after exercise (158 ± 13 before vs. 145 ± 10 cmH2O after exercise; P = 0.005). Voluntary activation, assessed using twitch interpolation, did not change (67 ± 6 before vs. 64 ± 2% after exercise; P = 0.20), and electromyographic activity of the rectus abdominis and external oblique increased during these volitional maneuvers. These data provide new evidence that the abdominal muscles fatigue after sustained, high-intensity exercise and that the fatigue is primarily due to peripheral mechanisms.

expiratory muscle fatigue; magnetic stimulation; gastric pressure

THE EXPIRATORY MUSCLES OF the rib cage and the abdominal wall are usually silent during eupnea in humans (16) but become active in response to the hyperpnea of exercise (2, 18, 24). Increased expiratory muscle activity during exercise augments expiratory airflow and facilitates an increase in tidal volume via a decrease in end-expiratory lung volume (EELV) (17). In addition to their role during expiration, the expiratory muscles assist the inspiratory muscles. By reducing abdominal wall compliance via an increase in tonic expiratory muscle activity, the "abdominal fulcrum" against which diaphragmatic contraction occurs is improved (17). Furthermore, a decrease in EELV assists the diaphragm and other inspiratory muscles to produce force by improving their length-tension relationships and mechanical geometry (37). The decrease in EELV also assists with lung volume expansion at the initiation of inspiration via passive recoil of the chest wall (3).

Despite the important contribution of the expiratory muscles to ventilation during exercise, it is unclear whether these muscles fatigue in response to whole body endurance exercise, as appears to occur in the case of the diaphragm (26). The proportion of fast-twitch fibers is typically higher in the expiratory muscles compared with the diaphragm (30), and the oxidative capacity is substantially less (54). In addition, there is evidence that muscle endurance is lower in the expiratory muscles compared with in the inspiratory muscles (22). These findings, in combination with the fact that the expiratory muscles are engaged to a similar extent as the inspiratory muscles during dynamic exercise (27), suggest that the expiratory muscles may be particularly prone to fatigue.

Although several studies have assessed the fatigability of the expiratory muscles in response to resistive breathing (22, 43, 52, 53) and maximal voluntary hyperpnea (32), only a few studies have investigated the effect of dynamic exercise (13, 21, 36). All of these studies, however, used indirect measures of fatigue that were either effort dependent, or relied on spectral shifts in the electromyographic (EMG) signal (43, 52, 53), the validity of which has been questioned (42). Magnetic stimulation of the spinal nerve roots provides an objective, nonvolitional measure of abdominal muscle function (31). Using this technique, Kyroussis et al. (31) showed that the abdominal muscles fatigue in response to maximal voluntary isocapnic hyperpnea. To our knowledge, no study has used the technique to investigate whether the abdominal muscles fatigue in response to dynamic exercise. Thus the primary aim of the present study was to determine, using magnetic stimulation, whether the abdominal muscles fatigue in response to sustained high-intensity lower limb exercise.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects

Eleven male subjects with resting pulmonary function within normal limits volunteered to participate in the study [age 28 ± 2 yr; stature 179 ± 2 cm; body mass 77.9 ± 1.4 kg; peak O2 uptake (VO2 peak) 50.0 ± 1.9 (SE) ml·kg–1·min–1]. All subjects were physically active, including two competitive cyclists. The local Research Ethics Committee approved all experimental procedures and each subject provided written informed consent.

Experimental Procedures

The experimental procedures were conducted during two visits to the laboratory. At the first visit, subjects were familiarized with the magnetic stimulation protocol and the volitional breathing maneuvers, and they performed a maximal incremental exercise test (35 W every 3 min starting from 95 W) on an electromagnetically braked cycle ergometer (Excalibur, Lode, Groningen, The Netherlands). At the second visit, stimulations were delivered to the nerves supplying the abdominal muscles at incremental power outputs to determine whether supramaximal stimulation could be achieved. Abdominal muscle function was assessed before and up to 30 min after lower limb cycle exercise to volitional exhaustion. Subjects abstained from caffeine for 12 h and stressful exercise for 48 h before each visit. Each visit was separated by at least 48 h.

Pressure Measurements

Gastric (Pga) and esophageal (Pes) pressures were measured using two conventional balloon-tipped catheters 86 cm in length (Ackrad Labs, Cooper Surgical, Berlin, Germany), which were passed per nasally into the stomach and the lower one-third of the esophagus, respectively, after the application of 2% lidocaine anesthetic gel to the naris. Each catheter was connected to a differential pressure transducer (model DP45, Validyne, Northridge, CA; range ± 229 cmH2O). The pressure-volume characteristics of the balloons were evaluated using standard procedures (38) and the balloons were filled with 2 ml of air to ensure that they did not collapse under the high expiratory pressures. The gastric balloon was positioned so that end-expiratory Pga was positive in the cycling position during eupneic breathing. The esophageal balloon was positioned using the "occlusion" technique (7). Mouth pressure (Pm) was measured at the inlet to the mouth using a third differential pressure transducer. Each transducer was calibrated across the physiological range with an electromanometer (model M14, Mercury, Glasgow, Scotland).

Magnetic Stimulation

Magnetic stimulation was delivered via a double 70-mm coil powered by a repetitive magnetic stimulator augmented by four booster modules (Magstim Super Rapid, Magstim, Whitland, Wales). For all stimulations, the coil was placed over the vertebral column between the 8th (T8) and the 11th (T11) thoracic vertebrae, with the handle at a right angle to the spine (31). The optimal coil position was defined as the vertebral level (between T8 and T11) that when stimulated evoked the highest Pga (31). The coil position was marked with indelible ink to ensure the coil was in an identical position for subsequent stimulations. All stimulations were performed against a semioccluded airway at a relaxed end-expiratory Pes that was maintained for ~1 s.

EMG

The EMG activity of the rectus abdominis (RA) and external oblique (EO) muscles was recorded using 28-mm-diameter skin-surface electrodes (Arbo Infant Electrodes, Tyco Healthcare, Neustadt Donau, Germany). Two electrodes were placed 1 cm apart over the belly of each muscle on the right-hand side of the abdomen and were secured with tape (3M, Tegaderm, Neuss, Germany). The pairs of electrodes were positioned within 2 cm superior to the umbilicus and 2–4 cm lateral to the umbilicus for RA, and 4–6 cm medial to the iliac crest for EO (21). The electrodes were placed in the same orientation as the muscle fibers (41), and a ground electrode was placed on the bony process of the anterior superior iliac spine.

Data Capture

The pressure and EMG signals were passed through an amplifier (model 1902, Cambridge Electronic Design, Cambridge, UK), digitized at sampling rates of 150 Hz and 3 kHz, respectively, using an analog-to-digital converter (micro 1401 mkII, Cambridge Electronic Design), and acquired on a personal computer running commercially available software (Spike 2 version 5.12, Cambridge Electronic Design).

Supramaximal Stimulation

To assess whether the abdominal muscles were activated maximally when stimulated, the stimulator was charged to predetermined percentages of its maximal power output (50, 60, 70, 80, 85, 90, 95, and 100%). Three single-twitch stimulations were performed at each power setting, with the subject seated on the ergometer in the riding position (i.e., relaxed, feet strapped into pedals, upper body supported by aerobars, and leg ipsilateral to EMG electrodes extended). Each of the stimulations was separated by 30 s to avoid twitch potentiation. Mean peak twitch Pga (Pga,tw) and mean M-wave amplitudes were determined for each percentage of the stimulator's power output. We were unable to secure reliable M waves for the EO in the majority of subjects; therefore, M-wave data in response to nerve stimulation are reported for the RA only. A leveling off of Pga,tw and RA M-wave amplitude was considered to represent supramaximal stimulation of the abdominal muscles and the RA, respectively. At 100% of maximal power output, Pga,tw measured at the beginning of the progressive increase in power output was not different from that obtained at the end, indicating that the incremental protocol did not elicit twitch potentiation.

Abdominal Muscle Function

After 20 min of quiet rest, the subjects adopted the riding position. Two 1-Hz stimulations were delivered, followed by two stimulations at frequencies of 25, 20, 15, 10, 5 (train length 1 s), and 1 Hz. Stimulations were administered at 100% of the stimulator's power output and were separated by 30 s. Potentiated twitch pressure is a more sensitive measure of fatigue than unpotentiated twitch pressure (34). Accordingly, we measured peak Pga elicited by a 1-Hz stimulation ~5 s after a maximal expulsive maneuver maintained for ~5 s against a semioccluded airway from total lung capacity, and we repeated this procedure four times such that four potentiated twitches were obtained. During these maneuvers, the subjects placed their elbows on the aerobars and supported their cheeks with their hands to minimize the use of the buccal muscles. Voluntary activation of the expiratory muscles during the maximal expulsive maneuvers was assessed using the interpolated twitch technique (8). Briefly, the Pga produced during a superimposed single twitch on the maximal expulsive maneuver was compared with the Pga produced by the potentiated single twitch delivered ~5 s afterward. A decline in voluntary activation after exercise is indicative of a reduction in central drive to the muscle (i.e., central fatigue). The entire assessment procedure was performed before exercise (~30 min), immediately after exercise (first stimulation <1 min), and at 30 min after exercise. The order of stimulation was identical pre- vs. postexercise.

The amplitude of the pressure response (baseline to peak), the maximal rate of pressure development (MRPD), and the maximal relaxation rate (MRR) were assessed for each of the stimulation frequencies. The 1-Hz stimulations were also assessed for contraction time (CT) and one-half relaxation time (RT0.5). Membrane excitability was determined by measuring the peak-to-peak amplitude (mV), duration (ms), and area (mV/ms) of the RA M-wave in response to 1-Hz stimulations (20). In addition, raw EMG signals from the RA and EO were obtained during the maximal expulsive maneuvers. The EMG signals were band-pass filtered (bandwidth 10–500 Hz) and full-wave rectified, and the peak root mean square was calculated using a time constant of 0.1 s (EMGRMS).

Lower Limb Cycle Exercise

After a 3-min rest in the riding position, the subjects performed a 5-min warm-up at 40% of the peak power output achieved during maximal incremental exercise. Exercise intensity was increased to 90% of the peak power output, and each subject was verbally encouraged to maintain pedal cadence above 60 rpm for as long as possible. Ventilatory and pulmonary gas-exchange indexes were measured breath by breath throughout the exercise using an online system (Oxycon Pro, Jaeger, Germany). Heart rate was measured beat by beat via telemetry (Polar Vantage, Polar Electro Oy, Kempele, Finland), and ratings of perceived exertion (dyspnea and limb discomfort) were obtained every 2 min during exercise using Borg's modified CR10 scale (10). Capillary blood was sampled from an earlobe every 2 min during exercise for the subsequent determination of hemolyzed lactate concentration by an enzymatic method (Biosen C_line Sport, EKF Diagnostic, Barleben, Germany). Inspiratory and expiratory airflow were also measured throughout the test using an ultrasonic phase-shift flowmeter (Birmingham Flowmetrics, Birmingham, UK), which was calibrated before testing with a flow-volume simulator (series 11320, Hans Rudolph, Kansas City, MO). Pga and Pes were measured throughout exercise and were aligned to the airflow signal via predetermined delays. Abdominal muscle force output ({int}Pga x fR) was calculated as the integral of Pga over the period of expiratory flow multiplied by the respiratory frequency (fR) (31).

Reproducibility

To determine the within-day, between-occasion reproducibility of neuromuscular function measurements, abdominal muscle function was assessed before and after 30 min of quiet rest in the riding position. These measures of reproducibility were collected before the constant-load exercise trials.

Statistical Analyses

Repeated-measures ANOVA was used to compare abdominal muscle function across time (before, immediately after, and 30 min after exercise) and, for measurements obtained via magnetic stimulation, also across stimulation frequencies (1, 5, 10, 15, 20, and 25 Hz). Following significant main effects, planned pairwise comparisons were made using the Bonferroni method. Within-day, between-occasion reproducibility of abdominal muscle function measurements was assessed using the coefficient of variation (CV) and the intraclass correlation coefficient (ICC). Pearson product-moment correlation coefficients (r) were used to examine relationships between the magnitude of abdominal muscle fatigue and both the subjects' aerobic fitness (VO2 peak) and the abdominal muscle force output (expressed as the percent increase from rest to the final minute of exercise, as the maximum value, and as the cumulative force output). The acceptable type I error was set at P < 0.05. Results are expressed as means ± SE. Statistical analyses were performed using SPSS version 11.5 for Windows (SPSS, Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Supramaximal Stimulation

As the power output of the stimulator increased, proportional increases in Pga,tw occurred (Fig. 1A). By contrast, M-wave amplitude for the RA muscle leveled off at the higher power outputs (Fig. 1B).


Figure 1
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  		Fig. 1. Gastric twitch pressure (Pga,tw; A) and M-wave amplitude for the rectus abdominis (B) during magnetic stimulation of the thoracic nerves (1 Hz) at different power outputs of the stimulator [expressed as a percentage of the values generated at 100% power output (%max)]. Data were collected after at least 10 min of rest but before the pre- and postexercise assessments of neuromuscular function. Values are means ± SE for 11 subjects. *P < 0.05; **P < 0.01, values significantly different from at 100% power output.

 
Reproducibility

There were no systematic differences in evoked pressures before vs. after 30 min of quiet rest (Table 1). Within-day, between-occasion reproducibility coefficients were all <9% for CV and >0.70 for ICC (Table 1).


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  		Table 1. Within-day, between-occasion reproducibility of neuromuscular function measurements

 
Potentiation

The baseline stimulation protocol potentiated Pga,tw in all 11 subjects (21.7 ± 3.8 cmH2O at start of protocol vs. 29.4 ± 3.0 cmH2O at end of protocol; P = 0.014). Maximal expulsive maneuvers did not further potentiate Pga,tw (29.4 ± 3.0 cmH2O pre- vs. 28.0 ± 2.8 cmH2O postexpulsion; P = 0.43), presumably because the preceding stimulation protocol had already fully potentiated the single twitches.

Lower Limb Cycle Exercise

Subjects exercised at 215 ± 12 W for 14.2 ± 4.2 min (range 7.2–16.3 min). After the first few minutes of exercise, oxygen uptake and minute ventilation (VE) increased gradually with time to reach final minute values of 48.5 ± 1.5 ml·kg–1·min–1 (97 ± 2% of VO2 peak) and 153 ± 9 l/min (97 ± 4% of peak VE; 71 ± 4% of maximal voluntary ventilation), respectively. The rise in VE was mediated primarily by increases in fR and corresponding reductions in the time available for expiration. Heart rate (HR), blood lactate concentration, and ratings of dyspnea and leg discomfort increased throughout exercise to reach final minute values of 184 ± 3 beats/min (98 ± 1% of peak HR), 13.4 ± 0.9 mM, 10 ± 1, and 11 ± 1, respectively. The force output of the abdominal muscles ({int}Pga x fR) increased progressively throughout exercise to reach a final minute value that was ~200% above baseline (Fig. 2).


Figure 2
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  		Fig. 2. Force output of the abdominal muscles [{int}Pga x respiratory frequency (fR)] at rest (Pre), during the warm-up (WU), and during lower limb cycling exercise to exhaustion. Absolute exercise time averaged 14.2 ± 4.2 min (range 7.2–16.3 min). Values are means ± SE for 11 subjects.

 
Exercise-Induced Abdominal Muscle Fatigue

There were no changes in the single-twitch RA M-wave amplitude, duration, or area pre- vs. postexercise (Table 2, Fig. 3). At all frequencies of stimulation, Pga immediately postexercise was reduced below baseline values (–25 ± 4% mean for all frequencies; P < 0.001) (Fig. 4A). At 30 min postexercise, Pga recovered slightly but remained below baseline values (–12 ± 4% mean for all frequencies; P = 0.001) (Fig. 4A). Figure 4B shows an identity plot for Pga pre- vs. postexercise for all subjects. Most of the points fell below the line of identity indicating that reductions in Pga occurred across all stimulation frequencies in most of the subjects. The reductions in Pga were not accompanied by changes in Pes (Fig. 5). Mean end-expiratory pressures across all stimulation frequencies were not different before vs. immediately after exercise (–0.5 ± 0.1 vs. –0.6 ± 0.1 cmH2O for end-expiratory Pes and 6.8 ± 0.1 vs. 6.9 ± 0.1 cmH2O for end-expiratory Pga, respectively; P > 0.05), indicating that all stimulations were delivered at the same lung volume and at the same abdominal muscle length before vs. after exercise.


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  		Table 2. Rectus abdominis M-wave data

 

Figure 3
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  		Fig. 3. Representative M waves obtained from the rectus abdominis in 1 subject at baseline and immediately after whole body exercise.

 

Figure 4
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  		Fig. 4. A: group mean (± SE) gastric pressure (Pga) in response to magnetic stimulation at 1 Hz (single twitch) through 25 Hz (tetanic stimulation) before, and up to 30 min after whole body exercise. B: identity plot for thoracic nerve stimulation at 1–25 Hz. Values are means ± SE for 11 subjects. *P < 0.05; **P < 0.01, values <1 min postexercise significantly different from preexercise values at the same stimulation frequency. {dagger}P < 0.05; {dagger}{dagger}P < 0.01, values 30 min postexercise significantly different from preexercise values at the same stimulation frequency.

 

Figure 5
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  		Fig. 5. Group mean (± SE) esophageal pressure (Pes) in response to magnetic stimulation at 1 Hz (single twitch) through 25 Hz (tetanic stimulation) before and up to 30 min after exercise. Values are for 11 subjects.

 
In addition to Pga at the different frequencies of stimulation, we also measured the contraction and relaxation responses (Table 3). Exercise resulted in reductions in MRPD and MRR at most frequencies of stimulation immediately postexercise. When the decreases in peak pressure were taken into account, however, neither MRPD nor MRR was altered after exercise. In addition, there were no pre- vs. postexercise differences in the single-twitch CT (176 ± 11 vs. 169 ± 14 ms, respectively) or RT0.5 (134 ± 8 vs. 139 ± 6 ms, respectively).


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  		Table 3. Group mean changes from baseline in within-twitch measurements obtained immediately after exercise

 
During the maximal expulsive maneuvers, Pga decreased from 158 ± 13 cmH2O at baseline to 145 ± 10 cmH2O immediately after exercise (P = 0.005) and recovered back toward baseline 30 min after exercise (153 ± 11 cmH2O; P = 0.58). Voluntary activation of the abdominal muscles during the maximal expulsive maneuvers was submaximal but not different pre- vs. postexercise (67 ± 6 vs. 64 ± 2%; P = 0.20). By contrast to the postexercise reduction in maximal volitional Pga, RA EMGRMS during the immediate postexercise maneuvers increased above baseline values (0.43 ± 0.08 vs. 0.38 ± 0.08 mV; P = 0.005), although EO EMGRMS was not different (0.51 ± 0.08 vs. 0.51 ± 0.08 mV; P > 0.05).

Correlations With Changes in Evoked Pga

The correlation between the subjects' aerobic fitness (VO2 peak) and the magnitude of abdominal muscle fatigue (%{Delta}Pga averaged over all frequencies of stimulation pre- vs. postexercise) was nonsignificant (r = –0.544, P = 0.084). Furthermore, there were nonsignificant correlations between the magnitude of abdominal muscle fatigue and the force output of the abdominal muscles ({int}Pga x fR), expressed either as the percent increase from rest to the final minute of exercise (r = –0.19, P = 0.59) or as the maximal {int}Pga x fR (r = –0.47, P = 0.17). However, there was a significant negative correlation between the magnitude of fatigue and the cumulative force output during exercise (r = –0.73, P = 0.017).


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGMENTS
 REFERENCES
 
Main Findings

We investigated, using objective measures of muscle function, whether the abdominal muscles fatigue in response to dynamic exercise. Using magnetic stimulation of the spinal nerve roots supplying the abdominal muscles, we found a significant decrease in Pga over a range of stimulation frequencies (1–25 Hz) after sustained, high-intensity exercise (>90% VO2 peak) in normal male subjects with a broad range of fitness (VO2 peak 45–63 ml·kg–1·min–1). In addition, concurrent decreases in maximal expiratory pressure occurred after the exercise, indicating a global loss of expiratory muscle function. The reductions in stimulated Pga were unlikely due to changes in membrane excitability because amplitude, duration, and area of the RA M wave were unaffected. The reductions in voluntary Pga were not mediated centrally because voluntary activation, assessed using twitch interpolation, did not change and EMG activity of the RA increased during the volitional maneuvers. Although the findings of the present study apply specifically to healthy male subjects, it is necessary to assert that they cannot be extrapolated necessarily to female subjects, who may have a greater resistance to muscle fatigue (25).

Technical Considerations

Abdominal muscle function was assessed using the magnetic stimulation technique, as described previously (31, 44). We opted for magnetic stimulation over electrical stimulation for several reasons. Compared with transcutaneous electrical stimulation, magnetic stimulation provides a more diffuse spread of current that stimulates a number of nerve roots. Transcutaneous electrical stimulation has been used to activate the superficial muscles of the abdominal wall (39, 50), but this technique cannot be used to stimulate the deeper abdominal muscles that are recruited preferentially as ventilation increases (1, 15). Another reason for using magnetic over electrical stimulation is that magnetic stimulation does not activate cutaneous pain receptors and, as a consequence, is less painful for subjects. In agreement with previous studies in normal subjects (44), we found that magnetic stimulation of the lower thoracic nerve roots across a range of frequencies was well tolerated by subjects.

A further consideration is whether the motor nerve input to the muscle is supramaximal. In the present study, magnetic stimulation of the thoracic nerve roots was submaximal. Although M-wave amplitude recorded from the RA leveled off above 90% of maximum stimulator power output, Pga continued to increase in response to further increases in power. These data suggest that although our stimulation technique evoked supramaximal stimulation of the RA, it failed to achieve supramaximal stimulation of the additional muscles that contribute to Pga. Our findings are in agreement with some (31, 35) but not all previous studies (11). For example, Lin et al. (35) reported that M-wave amplitudes recorded from the RA and the EO leveled off at 80% of maximum stimulator power output. By contrast, Chokroverty et al. (11) found that, on increasing the intensity of stimulation from 30 to 100%, the M-wave amplitudes for RA, EO, and intercostal muscles continued to increase.

Although stimulation was not supramaximal, we believe that stimulation was kept constant throughout the study. No changes were observed in amplitude, area, or duration of evoked M waves after exercise, suggesting that the decreases in Pga were not due to derecruitment of muscle fibers or to transmission failure. Therefore, the decreases in Pga were most likely the result of contractile fatigue (see also Causes of abdominal muscle fatigue). Previous work has shown that the reliability of Pga,tw is similar before exercise compared with after, indicating that the same proportion of the muscle is activated at each stimulation (31). In the present study, the stimulator was set to 100% of its maximum power output for all stimulations. Furthermore, the coil position was marked before exercise to ensure that it was repositioned in exactly the same location for each stimulation, even though small changes in coil position over the lower thoracic intervertebral spaces do not significantly affect Pga,tw (31, 35). To ensure that the abdominal muscles were relaxed before each set of stimulations, subjects supported their upper body on aerobars. When the subjects were tested before and after 30 min of quiet breathing there were hardly any systematic differences in the measures of neuromuscular function and reproducibility was excellent. All stimulations were initiated at the same lung volume and at the same abdominal muscle length, as judged by nonsignificant changes in end-expiratory Pes and Pga, respectively. Therefore, although stimulation was not supramaximal, we are confident that it remained constant throughout the study. Because stimulation was submaximal, the increase in muscle temperature that would be expected to occur with dynamic exercise may have increased conductance and, consequently, increased both the magnetic current and the force response (14). Thus, if anything, we may have actually underestimated the magnitude of fatigue (14).

The interpretation of our finding that lower limb cycle exercise elicits abdominal muscle fatigue is critically dependent on being able to detect relatively small systematic within-day, between-occasion changes in our measures of neuromuscular function. In the present study, CV and ICC were <9% and >0.70, respectively (see Table 1). The reproducibility of Pga,tw (CV = 3.8%) was comparable with previous studies (31, 33). For measurements obtained in the prone position, Kyroussis et al. reported a CV of 3.5% for single Pga,tw (31) and 7.2% for paired Pga,tw (33). The reproducibility of Pga for stimulation frequencies above 1 Hz has not been reported previously, but we found that the reproducibility of tetanic measures of Pga (mean CV = 3.1%) was similar to that of Pga,tw (CV = 3.8%).

A potential problem with nerve stimulation is that there is likely some recovery during the time between end-exercise and the postexercise neuromuscular measurements (40). To minimize the influence of recovery on our measures of abdominal muscle fatigue, subjects remained in the riding position, which enabled us to deliver the initial stimulations within 1 min of completing the exercise trial. Additionally, we applied the higher frequency stimulations first because force output at high frequencies recovers quicker than at lower frequencies (28). As some recovery was likely, however, we probably underestimated the level of abdominal muscle fatigue.

Exercise-Induced Abdominal Muscle Fatigue

Comparison with previous studies.   Skeletal muscle fatigue was defined as a reduction in force- and/or velocity-generating capacity of a muscle that has been under load and is relieved with rest (42). Using this definition, it is clear that the abdominal muscles fatigue in response to sustained, high-intensity exercise (>90% VO2 peak). We found a 33% reduction in Pga,tw (1 Hz) and a mean 25% reduction in the Pga response to stimulations at 1–25 Hz. We are unaware of any other study that has used nerve stimulation to determine whether the abdominal muscles fatigue in response to dynamic exercise. The percent declines in the present study, however, are remarkably similar to those reported previously for the diaphragm after exercise performed at intensities similar to those in the present study. For example, Johnson et al. (26) reported a 32% decrease in peak twitch transdiaphragmatic pressure and a 20% decrease in transdiaphragmatic pressure averaged over 1, 10, and 20 Hz in healthy subjects exercising at 90–95% of VO2 peak. Similarly, Babcock et al. (6) reported a mean 23% reduction in the transdiaphragmatic pressure response to stimulations at 1 and 10 Hz and a 28% reduction in the second twitch response to paired stimuli at frequencies of 10–100 Hz in healthy subjects exercising at ~93% VO2 peak. These results suggest that the degree of abdominal muscle fatigue induced by high-intensity, lower limb cycle exercise is similar to that of the diaphragm.

In addition to the reductions in stimulated pressures, lower limb cycle exercise elicited reductions in contraction and relaxation rates at all of the stimulation frequencies. However, when the decreases in peak pressure were taken into account, no differences were observed. This finding differs from that reported by Kyroussis et al. (32), who found that when peak pressures were equalized there was a 25% reduction in MRR of Pga in response to sharp volitional expiratory efforts at 1 min after maximal voluntary hyperpnea. Kyroussis et al. also reported that MRR of the single twitch in response to magnetic stimulation slowed after voluntary hyperpnea in two of the subjects studied using this technique.

Lower limb cycle exercise also elicited a global loss of expiratory muscle function, as reflected by a significant decrease in Pga during maximal volitional expulsive maneuvers. This finding is in agreement with previous studies. For example, Cordain et al. (13) reported reductions in maximal expiratory Pm in response to maximal incremental and constant-load (20 min at 85% maximal HR) treadmill exercise. Similarly, Loke et al. (36) found a reduction in maximal expiratory Pm in response to marathon running. A limitation of volitional measures of expiratory muscle fatigue, however, is that it is difficult to differentiate between peripheral and central processes.

Causes of abdominal muscle fatigue.   The decrease in Pga at frequencies of stimulation ranging from 1 to 25 Hz is consistent with low-frequency fatigue (28). Low-frequency fatigue is caused by a reduction in Ca2+ release from the sarcoplasmic reticulum and/or damage to the structure of the muscle fiber and the excitation-contraction coupling mechanism (28). Of these two possibilities, the low-frequency fatigue we found in the abdominal muscles was probably due to a reduced Ca2+ release from the sarcoplasmic reticulum because, by 30-min postexercise, the Pga values were returning back toward baseline. In a situation where long-lasting fatigue occurs, then muscle damage would be the most likely explanation for the long recovery (28).

Reductions in action potential transmission did not appear to account for the pre- vs. postexercise reductions in contractile function because the RA M-wave amplitude, duration, and area did not differ across time. That is not to say that changes in the characteristics of the M wave did not occur immediately after exercise (<1 min), during the period when the subjects were being instrumented for stimulation. It is also possible that changes occurred in the M wave of abdominal muscles other than the RA. We measured M waves from this superficial muscle because it was easy to locate and gave reliable recordings. Deeper abdominal muscles, however, contribute more to the hyperpnea of exercise (1).

During a maximal expulsive maneuver, subjects were able to activate only 67% of their expiratory muscles. That voluntary activation of the expiratory muscles was submaximal during voluntary efforts is in agreement with previous studies (23, 50). After exercise, Pga during the expulsive maneuver was significantly reduced below baseline. Using the interpolated twitch technique, we found that the pressure loss was primarily due to peripheral processes because voluntary activation did not decline significantly after exercise. The reduction in Pga was accompanied by an increase in EMGRMS, which could reflect an increase in neural drive, neural transmission, or membrane excitability (9). We have found no evidence for changes in neural drive or membrane excitability; therefore, more peripheral sites in the muscle remain as the most likely sources for the reduction in Pga.

Factors contributing to abdominal muscle fatigue.   Aerobic fitness does not appear to influence the magnitude of exercise-induced abdominal muscle fatigue, as suggested by the nonsignificant correlation between the subjects' VO2 peak and the percent decline in evoked Pga. This finding is similar to that reported for the diaphragm (5). Babcock et al. (5) reported that highly fit subjects did not incur a greater level of diaphragm fatigue than subjects with average fitness, despite exercising at a higher absolute workload with a greater ventilatory requirement. By contrast, the cumulative work history of the abdominal muscles does appear to have a significant influence on the magnitude of abdominal muscle fatigue, as evidenced by the significant correlation between the amount of abdominal muscle fatigue and the cumulative force output of the Pga waveform over the entire exercise period.

It is likely that abdominal muscle force output becomes even more important when the demands placed on the abdominal muscles are out of proportion to their capacity. For example, patients with chronic obstructive pulmonary disease have increased recruitment of abdominal muscles due to increased levels of expiratory flow limitation (45). The consequent increase in abdominal muscle pressure may have a mechanical effect on reducing left ventricular stroke volume and cardiac output (4, 48) and systemic O2 delivery (4), which may be expected to exacerbate limb muscle fatigue and hence exercise performance. It is unknown whether a similar scenario exists for the athlete at high exercise intensities where there is substantial expiratory flow limitation and expiratory pressures reach maximal effective pressures (27).

In addition to the effect of abdominal muscle force output, the role of the abdominals in supporting postural adjustments may also have contributed to the abdominal fatigue observed in the present study (2). However, this postural effect was likely minimal because we used cycling as the exercise modality with the assumption that cycling would cause less expiratory muscle activation compared with other modalities (24).

Functional Consequences of Abdominal Muscle Fatigue

In theory, abdominal muscle fatigue could limit endurance exercise performance via an impairment of the ventilatory response to exercise. This seems unlikely, however, because expiratory flow becomes maximal and independent of effort at levels of expiratory Pga that are well below the maximum attainable values, such that any extra effort would be wasted (27). Thus it would require significant fatigue, and subsequent loss in force-generating capacity, of the abdominal muscles to impact on expiratory flow.

Abdominal muscle fatigue may impact on exercise performance via an increased sensation of dyspnea. Certainly, abdominal muscles play an important role in overall respiratory effort sensation. For example, there are comparable increases in dyspnea in response to breathing against expiratory and inspiratory resistive loads (12). Furthermore, increases in respiratory effort during expiratory threshold loading have been related to postloading decreases in maximal expiratory mouth pressure (52). In the context of whole body exercise, respiratory effort sensation appears to be determined equally by inspiratory and expiratory pressure changes (29). As the abdominal muscles fatigue, there would likely be an increased central drive to maintain force production of these muscles, as is thought to occur with inspiratory muscle fatigue (49). An increased central respiratory drive may be perceived via central corollary discharge as an increased sense of effort, which may provide a critical signal to the central nervous system to curtail exercise performance. Training aimed specifically at the abdominal muscles has been shown to reduce the perception of exertional dyspnea via a concomitant reduction in minute ventilation, and hence central respiratory drive (51). An increase in abdominal muscle recruitment in response to fatigue may impact on exercise performance via an action of these muscles on rib cage distortion (39). Rib cage distortion may result in mechanical inefficiency and, therefore, a greater work of breathing and an increased metabolic and blood flow demand by the respiratory muscles. This fatigue-induced increase in respiratory muscle work would also be expected to increase the perception of respiratory muscle effort.

A further aspect of abdominal muscle fatigue that may limit exercise performance is sympathetically mediated vasoconstriction in limb locomotor muscles. Fatiguing abdominal muscle work causes a reflex increase in muscle sympathetic nerve activity in the resting limb of healthy humans that is likely triggered by an accumulation of metabolites in the fatiguing abdominal muscles (19). The vascular consequences of an increase in muscle sympathetic nerve activity were shown by the reduced hindlimb blood flow induced by lactic acid infusions into the deep circumflex iliac artery in the resting and exercising canine, an effect that was prevented via pharmacological sympathetic blockade (46). A reduction in blood flow to working limb muscles would be expected to increase their fatigability, as has been shown to occur when the force output of the inspiratory muscles is increased during exercise (47).

In conclusion, we tested the hypothesis that dynamic lower limb exercise elicits abdominal muscle fatigue in normal subjects with a broad range of fitness. Our results show that exercise elicits a decrease in expiratory muscle contractility across a range of stimulation frequencies (1–25 Hz).


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Dr. Alex Nowicky and Magstim Company for loaning us the repetitive stimulator and the extra booster modules, respectively. We are also grateful to Drs. Robert Shave and Thomas Korff for their helpful critique.


   FOOTNOTES
 

Address for reprint requests and other correspondence: L. M. Romer, Centre for Sports Medicine and Human Performance, School of Sport and Education, Brunel Univ., Middlesex, UB8 3PH UK (e-mail: lee.romer{at}brunel.ac.uk)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Abe T, Kusuhara N, Yoshimura N, Tomita T, and Easton PA. Differential respiratory activity of four abdominal muscles in humans. J Appl Physiol 80: 1379–1389, 1996.[Abstract/Free Full Text]
  2. Abraham KA, Feingold H, Fuller DD, Jenkins M, Mateika JH, and Fregosi RF. Respiratory-related activation of human abdominal muscles during exercise. J Physiol 541: 653–663, 2002.[Abstract/Free Full Text]
  3. Ainsworth DM, Smith CA, Eicker SW, Henderson KS, and Dempsey JA. The effects of locomotion on respiratory muscle activity in the awake dog. Respir Physiol 78: 145–162, 1989.[CrossRef][ISI][Medline]
  4. Aliverti A, Dellaca RL, Lotti P, Bertini S, Duranti R, Scano G, Heyman J, Lo Mauro A, Pedotti A, and Macklem PT. Influence of expiratory flow-limitation during exercise on systemic oxygen delivery in humans. Eur J Appl Physiol 95: 229–242, 2005.[CrossRef][ISI][Medline]
  5. Babcock MA, Pegelow DF, Johnson BD, and Dempsey JA. Aerobic fitness effects on exercise-induced low-frequency diaphragm fatigue. J Appl Physiol 81: 2156–2164, 1996.[Abstract/Free Full Text]
  6. Babcock MA, Pegelow DF, Taha BH, and Dempsey JA. High frequency diaphragmatic fatigue detected with paired stimuli in humans. Med Sci Sports Exerc 30: 506–511, 1998.[ISI][Medline]
  7. Baydur A, Behrakis PK, Zin WA, Jaeger M, and Milic-Emili J. A simple method for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis 126: 788–791, 1982.[ISI][Medline]
  8. Behm DG, St-Pierre DM, and Perez D. Muscle inactivation: assessment of interpolated twitch technique. J Appl Physiol 81: 2267–2273, 1996.[Abstract/Free Full Text]
  9. Bigland-Ritchie B. Muscle fatigue and the influence of changing neural drive. Clin Chest Med 5: 21–34, 1984.[ISI][Medline]
  10. Borg G. Borg's Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics, 1998.
  11. Chokroverty S, Deutsch A, Guha C, Gonzalez A, Kwan P, Burger R, and Goldberg J. Thoracic spinal nerve and root conduction: a magnetic stimulation study. Muscle Nerve 18: 987–991, 1995.[CrossRef][ISI][Medline]
  12. Chonan T, Altose MD, and Cherniack NS. Effects of expiratory resistive loading on the sensation of dyspnea. J Appl Physiol 69: 91–95, 1990.[Abstract/Free Full Text]
  13. Cordain L, Rode EJ, Gotshall RW, and Tucker A. Residual lung volume and ventilatory muscle strength changes following maximal and submaximal exercise. Int J Sports Med 15: 158–161, 1994.[ISI][Medline]
  14. Davies CT, Mecrow IK, and White MJ. Contractile properties of the human triceps surae with some observations on the effects of temperature and exercise. Eur J Appl Physiol 49: 255–269, 1982.
  15. De Troyer A, Estenne M, Ninane V, Van Gansbeke D, and Gorini M. Transversus abdominis muscle function in humans. J Appl Physiol 68: 1010–1016, 1990.[Abstract/Free Full Text]
  16. De Troyer A, Ninane V, Gilmartin JJ, Lemerre C, and Estenne M. Triangularis sterni muscle use in supine humans. J Appl Physiol 62: 919–925, 1987.[Abstract/Free Full Text]
  17. Dempsey JA, Adams L, Ainsworth DM, Fregosi RF, Gallagher CG, Guz A, Johnson BD, and Powers SK. Airway, lung, and respiratory muscle function during exercise. In: Handbook of Physiology. Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 11, p. 448–514.
  18. Dempsey JA, Johnson BD, and Saupe KW. Adaptations and limitations in the pulmonary system during exercise. Chest 97: 81S–87S, 1990.[Free Full Text]
  19. Derchak PA, Sheel AW, Morgan BJ, and Dempsey JA. Effects of expiratory muscle work on muscle sympathetic nerve activity. J Appl Physiol 92: 1539–1552, 2002.[Abstract/Free Full Text]
  20. Fowles JR, Green HJ, Tupling R, O'Brien S, and Roy BD. Human neuromuscular fatigue is associated with altered Na+-K+-ATPase activity following isometric exercise. J Appl Physiol 92: 1585–1593, 2002.[Abstract/Free Full Text]
  21. Fuller D, Sullivan J, and Fregosi RF. Expiratory muscle endurance performance after exhaustive submaximal exercise. J Appl Physiol 80: 1495–1502, 1996.[Abstract/Free Full Text]
  22. Gandevia SC, McKenzie DK, and Neering IR. Endurance properties of respiratory and limb muscles. Respir Physiol 53: 47–61, 1983.[CrossRef][ISI][Medline]
  23. Gandevia SC, McKenzie DK, and Plassman BL. Activation of human respiratory muscles during different voluntary manoeuvres. J Physiol 428: 387–403, 1990.[Abstract/Free Full Text]
  24. Henke KG, Sharratt M, Pegelow D, and Dempsey JA. Regulation of end-expiratory lung volume during exercise. J Appl Physiol 64: 135–146, 1988.[Abstract/Free Full Text]
  25. Hicks AL, Kent-Braun J, and Ditor DS. Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev 29: 109–112, 2001.[CrossRef][Medline]
  26. Johnson BD, Babcock MA, Suman OE, and Dempsey JA. Exercise-induced diaphragmatic fatigue in healthy humans. J Physiol 460: 385–405, 1993.[Abstract/Free Full Text]
  27. Johnson BD, Saupe KW, and Dempsey JA. Mechanical constraints on exercise hyperpnea in endurance athletes. J Appl Physiol 73: 874–886, 1992.[Abstract/Free Full Text]
  28. Jones DA. High- and low-frequency fatigue revisited. Acta Physiol Scand 156: 265–270, 1996.[CrossRef][ISI][Medline]
  29. Kayser B, Sliwinski P, Yan S, Tobiasz M, and Macklem PT. Respiratory effort sensation during exercise with induced expiratory-flow limitation in healthy humans. J Appl Physiol 83: 936–947, 1997.[Abstract/Free Full Text]
  30. Keens TG, Bryan AC, Levison H, and Ianuzzo CD. Developmental pattern of muscle fiber types in human ventilatory muscles. J Appl Physiol 44: 909–913, 1978.[Abstract/Free Full Text]
  31. Kyroussis D, Mills GH, Polkey MI, Hamnegard CH, Koulouris N, Green M, and Moxham J. Abdominal muscle fatigue after maximal ventilation in humans. J Appl Physiol 81: 1477–1483, 1996.[Abstract/Free Full Text]
  32. Kyroussis D, Mills GH, Polkey MI, Hamnegard CH, Wragg S, Road J, Green M, and Moxham J. Effect of maximum ventilation on abdominal muscle relaxation rate. Thorax 51: 510–515, 1996.[Abstract]
  33. Kyroussis D, Polkey MI, Mills GH, Hughes PD, Moxham J, and Green M. Simulation of cough in man by magnetic stimulation of the thoracic nerve roots. Am J Respir Crit Care Med 156: 1696–1699, 1997.[Abstract/Free Full Text]
  34. Laghi F, D'Alfonso N, and Tobin MJ. Pattern of recovery from diaphragmatic fatigue over 24 hours. J Appl Physiol 79: 539–546, 1995.[Abstract/Free Full Text]
  35. Lin VW, Hsieh C, Hsiao IN, and Canfield J. Functional magnetic stimulation of expiratory muscles: a noninvasive and new method for restoring cough. J Appl Physiol 84: 1144–1150, 1998.[Abstract/Free Full Text]
  36. Loke J, Mahler DA, and Virgulto JA. Respiratory muscle fatigue after marathon running. J Appl Physiol 52: 821–824, 1982.[Abstract/Free Full Text]
  37. Martin JG and De Troyer A. The behaviour of the abdominal muscles during inspiratory mechanical loading. Respir Physiol 50: 63–73, 1982.[CrossRef][ISI][Medline]
  38. Mead J, McIlroy MB, Selverstone NJ, and Kriete BC. Measurement of intraesophageal pressure. J Appl Physiol 7: 491–495, 1955.[Free Full Text]
  39. Mier A, Brophy C, Estenne M, Moxham J, Green M, and De Troyer A. Action of abdominal muscles on rib cage in humans. J Appl Physiol 58: 1438–1443, 1985.[Abstract/Free Full Text]
  40. Miller RG, Giannini D, Milner-Brown HS, Layzer RB, Koretsky AP, Hooper D, and Weiner MW. Effects of fatiguing exercise on high-energy phosphates, force, and EMG: evidence for three phases of recovery. Muscle Nerve 10: 810–821, 1987.[CrossRef][ISI][Medline]
  41. Ng JK, Kippers V, and Richardson CA. Muscle fibre orientation of abdominal muscles and suggested surface EMG electrode positions. Electromyogr Clin Neurophysiol 38: 51–58, 1998.[Medline]
  42. NHLBI Workshop. Respiratory muscle fatigue: report of the respiratory muscle fatigue workshop group. Am Rev Respir Dis 142: 474–486, 1990.[ISI][Medline]
  43. Orozco-Levi M, Gea J, Ferrer A, Mendez R, Ramirez-Sarmiento A, Maldonado D, and Broquetas J. Expiratory muscle endurance in middle-aged healthy subjects. Lung 179: 93–103, 2001.[CrossRef][ISI][Medline]
  44. Polkey MI, Luo Y, Guleria R, Hamnegard CH, Green M, and Moxham J. Functional magnetic stimulation of the abdominal muscles in humans. Am J Respir Crit Care Med 160: 513–522, 1999.[Abstract/Free Full Text]
  45. Potter WA, Olafsson S, and Hyatt RE. Ventilatory mechanics and expiratory flow limitation during exercise in patients with obstructive lung disease. J Clin Invest 50: 910–919, 1971.[ISI][Medline]
  46. Rodman JR, Henderson KS, Smith CA, and Dempsey JA. Cardiovascular effects of the respiratory muscle metaboreflexes in dogs: rest and exercise. J Appl Physiol 95: 1159–1169, 2003.[Abstract/Free Full Text]
  47. Romer LM, Lovering AT, Haverkamp HC, Pegelow DF, and Dempsey JA. Effect of inspiratory muscle work on peripheral fatigue of locomotor muscles in healthy humans. J Physiol In press.
  48. Stark-Leyva KN, Beck KC, and Johnson BD. Influence of expiratory loading and hyperinflation on cardiac output during exercise. J Appl Physiol 96: 1920–1927, 2004.[Abstract/Free Full Text]
  49. Supinski GS, Clary SJ, Bark H, and Kelsen SG. Effect of inspiratory muscle fatigue on perception of effort during loaded breathing. J Appl Physiol 62: 300–307, 1987.[Abstract/Free Full Text]
  50. Suzuki J, Tanaka R, Yan S, Chen R, Macklem PT, and Kayser B. Assessment of abdominal muscle contractility, strength, and fatigue. Am J Respir Crit Care Med 159: 1052–1060, 1999.[Abstract/Free Full Text]
  51. Suzuki S, Sato M, and Okubo T. Expiratory muscle training and sensation of respiratory effort during exercise in normal subjects. Thorax 50: 366–370, 1995.[Abstract]
  52. Suzuki S, Suzuki J, Ishii T, Akahori T, and Okubo T. Relationship of respiratory effort sensation to expiratory muscle fatigue during expiratory threshold loading. Am Rev Respir Dis 145: 461–466, 1992.[ISI][Medline]
  53. Suzuki S, Suzuki J, and Okubo T. Expiratory muscle fatigue in normal subjects. J Appl Physiol 70: 2632–2639, 1991.[Abstract/Free Full Text]
  54. Uribe JM, Stump CS, Tipton CM, and Fregosi RF. Influence of exercise training on the oxidative capacity of rat abdominal muscles. Respir Physiol 88: 171–180, 1992.[CrossRef][ISI][Medline]



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