Comparisons between gender and the fatigability of human skeletal muscle has been investigated in small and large muscle groups of both the upper and lower extremities (for review see (12). The results of several studies have reported that females in general demonstrate a longer time to task failure and less fatigue (i.e., a smaller decrement in force-generating capacity) at task failure suggesting that women have a greater resistance to fatigue compared to males (29). A difference that may persist even when males and females are matched for absolute strength (9,14). It has been speculated that gender differences in skeletal muscle fatigue may result from impaired muscle blood flow and/or oxygen delivery to the working muscles. It has been argued that males generate considerably higher absolute contractile forces than females, which in turn leads to greater intramuscular pressures and impaired blood flow to the contracting muscles when exercising at the same relative intensity as females (12). In agreement with this hypothesis, Russ and Kent-Braun (25) were able to eliminate gender differences in muscle fatigue using cuff occlusion to reduce muscle perfusion during repeated maximal isometric contractions of the dorsiflexor muscles. Compared with normal flow conditions where the males exhibited a greater decrease in force production than females, both groups exhibited a greater deficit in force production when the muscles were made ischemic but there was no difference between genders, which is consistent with the view that alterations in muscle metabolism may explain differences in fatigability between genders. In addition, a recent study has demonstrated that males experience a greater rate of decline in descending central drive than strength-matched females when performing submaximal intermittent contractions of the elbow flexor muscles (14). Nonetheless, females exhibited a longer time to task failure than males, adding further support to the view that a mechanism related to muscle perfusion (i.e., O2 delivery) and/or substrate utilization may explain the difference observed between genders and their relative fatigability.
There has been a growing interest in respiratory muscle fatigue and the effect it may have on exercise tolerance. Respiratory muscle fatigue has been reported to occur during voluntary hyperpnea (19), high-intensity cycling (16), treadmill exercise (1), inspiratory resistive breathing (8,23), and repeated generation of transdiaphragmatic pressures (2). Resistive breathing has been used extensively as a noninvasive tool for assessment of respiratory muscle performance (8,23), and is generally held as an effective method to elicit inspiratory muscle fatigue. The task requires breathing against an inspiratory load until task failure, which is often defined as the inability to generate sufficient inspiratory pressure to open the inlet-breathing valve. Inspiratory muscle strength has also been assessed noninvasively by measuring the maximal inspiratory pressure (PImax) at the mouth (4,30).
There does not appear to be a gender difference in the elastic properties of the lungs (10) and chest wall or pulmonary compliance (7); however, females typically have smaller lung volumes, lower maximal expiratory flow rates, and diffusion surface compared with males, even when corrected for height and body mass (20,22). Although it has been suggested that females may have a higher work of breathing than males (20,27) and that females may be more susceptible to exercise-induced arterial hypoxemia (11), it remains unclear whether females exhibit differences in respiratory muscle fatigue compared with males. For example, the results of earlier studies indicate that time to task failure during resistive inspiratory breathing is similar between females and males (8). However, previous research has yet to investigate the change in inspiratory muscle force (as PImax) during the submaximal fatigue task, at task failure, or during recovery. Therefore, the aim of the present study is to determine whether a gender difference can be observed in the fatigability of the inspiratory muscles by measuring PImax before, during, and after constant-load resistive breathing to task failure. Consistent with the view that females may experience inadequate alveolar-to-arterial O2 exchange (11) and/or greater O2 cost for ventilation (27), we hypothesize that females will demonstrate a greater magnitude and/or faster rate of inspiratory muscle fatigue compared with males during target resistive breathing.
MATERIALS AND METHODS
Twenty-two healthy female (N = 11) and male (N = 11) subjects provided written informed consent after being informed of all experimental procedures, the exercise protocol, and possible risks associated with participation in the study. All subjects demonstrated normal pulmonary function as demonstrated by a forced vital capacity (FVC) of >80% predicted and a forced expired volume in one second to forced vital capacity ratio (FEV1.0/FVC) of ≥78% (17). Female subjects were interviewed by the investigator and menstrual cycle history was determined. All testing occurred during the early follicular phase (between days 1 and 5) of their menstrual cycle, when both estradiol and progesterone levels are believed to be lowest. The experimental protocol was approved by the human subjects research and review committee at the University of Toledo and is in accordance with guidelines set forth by the Declaration of Helsinki.
Separate analyses were performed in a subgroup of females (N = 5) and males (N = 5) that were matched for resting PImax (i.e., absolute strength). Previous studies have found absolute strength to be an independent factor contributing to skeletal muscle fatigue during isometric muscle contractions (15). Therefore, a strength-matched gender comparison will determine whether any gender difference found in the fatigability of the inspiratory muscles was due to differences in absolute strength.
Subjects reported to the cardiopulmonary and metabolism research laboratory at the University of Toledo on two separate occasions with no less than 48 h between testing sessions. Each subject was instructed to consume only a light meal, and to abstain from vigorous exercise and caffeinated beverages for ≥12 h prior to arriving for testing. Exercise testing was performed at approximately the same time of the day for each subject.
Preliminary exercise testing was performed to both familiarize the subject with testing procedures and for the determination of their achieved maximal aerobic capacity (V̇O2peak). The highest mean oxygen uptake averaged over a 30-s interval was defined as V̇O2peak. Cardiopulmonary testing was performed on an electrically braked cycle ergometer (Excalibur Sport, Lode, The Netherlands). The maximal exercise test involved 5 min of low-intensity (20 W) cycling followed by a progressive increase in exercise intensity to the limit of tolerance. The work rate was increased as a ramp function at a rate of 20 and 25 W·min−1 for females and males, respectively. Subjects were instructed to maintain a constant pedal cadence selected by the subject and were aided by both visual feedback and verbal encouragement. Following a cool-down period, subjects were instructed on the testing protocols to be conducted during the second study session, and were allowed sufficient time to practice each of the tests.
Pulmonary gas exchange and vital capacity testing.
Pulmonary gas exchange, expired ventilation, FVC, and FEV1.0 were measured using an automated open-circuit metabolic measurement system (Jaeger, Oxycon Alpha, Germany). Expired gas flows were measured using a turbine. The flow signal was integrated to yield a volume signal that was calibrated with a syringe of known volume (3.0 L). Prior to each exercise session, the O2 and CO2 analyzers were calibrated using gases of known concentrations. Corrections for ambient temperature and water vapor were made for conditions measured near the mouth.
FVC was measured at baseline, at task failure, and after 45 min of recovery to evaluate possible changes in functional vital capacity that may have occurred during resistive breathing.
Inspiratory muscle strength and fatigue.
Maximal inspiratory pressure in centimeters of water (cm H2O) was measured with a differential pressure transducer (Validyne, Model No. DP-45/CD15 Carrier Demodulator, Northridge, CA) connected to an analog-to-digital converter (AD Instruments, PowerLab 16SP, Grand Junction, CO). The pressure signal was amplified and stored for later analysis. The data acquisition system was connected by tubing to a sampling port (2.5 cm long) on the proximal end of a cylinder (20 cm long with an internal diameter of 2 cm). The distal end of the cylinder was closed except for a small opening (2-mm internal diameter) that provided a leak to prevent exerting pressure with a closed glottis (4,6,30). The analog pressure signal was calibrated with an aneroid pressure gauge (WIKA Instruments, Germany) over a range of pressures (0 to −250 cm H2O).
As an index of the maximum amount of force-generating capacity of the inspiratory muscles, PImax was measured at the mouth near residual volume (6) according to the procedures of Black and Hyatt (4). Studies have shown this test to be a good measure of inspiratory muscle strength (30). During the PImax trials, subjects wore a nose clip, exhaled fully to near residual volume, and then inspired maximally once a tight seal was created around the mouth of the cylinder. To ensure that the highest PImax was obtained, several trials (≤15 trials) were performed at baseline (i.e., prefatigue) with at least 30 s of rest between each trial to prevent testing-induced respiratory muscle fatigue (6). For the intraindividual measurement of resting PImax, a coefficient of variation of 5.79% was obtained. Peak pressures reached during the PImax maneuver were recorded, and all PImax values are reported as the average of the two highest efforts within 5% of each other (28). Inspiratory muscle fatigue was induced by a single trial of constant-load resistive breathing using an inspiratory threshold device (Power Breathe, United Kingdom) until task failure. Resistive breathing was performed at 18 breaths per minute (−1/450% duty cycle) at a target pressure of 70% PImax, a resistance previously reported to induce respiratory muscle fatigue (24). Pilot work in our laboratory has shown this combination to elicit inspiratory muscle fatigue within 15 min of resistive breathing, and was associated with a low level of breathing discomfort experienced by the subjects while maintaining a high level of subject motivation throughout the task. The time to task failure was defined as the point at which the subject was unable to open the breathing valve for three consecutive efforts. Subjects were allowed to visually monitor pressure waveforms during resistive breathing, and were aided by verbal encouragement. To calculate the rate of inspiratory muscle fatigue, a single PImax value was obtained every 2 min during the resistive breathing test. Upon task failure subjects performed five consecutive PImax maneuvers to determine inspiratory muscle strength at fatigue. Recovery of inspiratory muscle strength was assessed by measuring PImax at 5-min increments to 30 min post-task failure with the last measurement at 45 min post-task failure.
Comparison between genders in demographic information, time to task failure, inspiratory muscle strength, along with pre- to post-task failure comparisons for PImax and FVC within each gender were performed by t-test analysis. Bivariate correlations were performed to evaluate relationships between variables. Differences between gender for PImax was analyzed using a repeated-measures ANOVA design with gender and time as the main effects. A one-way ANOVA was performed to test for differences in time within each gender. The rate of muscle fatigue (i.e., slope) was determined for each subject by linear regression using the maximal strength measurements that were obtained every 2 min during the fatiguing task. The individual slopes were averaged to provide group mean values for each gender. All values are reported as mean ± SE, and significance was set at a P ≤ 0.05.
The physical characteristics of the subjects are reported in Table 1. The mean age of female and male subjects was similar, but on average, females were shorter, had a lower body mass, and lower FVC compared to males. Subjects reported to be sedentary or involved in regular recreational activity but none were considered to be highly trained (<45 mL·kg−1·min−1).
Inspiratory muscle fatigue.
Prior to performing the inspiratory resistive breathing protocol, PImax was less in females compared with males (F: −137.0 ± 7.6 cm H2O; M: −172.5 ± 9.8 cm H2O; P ≤ 0.05) indicating that males exhibit considerably greater absolute inspiratory muscle strength than females. This difference between genders in absolute PImax persisted throughout the resistive breathing protocol and recovery (Fig. 1). Inspiratory muscle strength was significantly correlated with body surface area (pooled data, r = 0.41, P ≤ 0.05) and FVC (pooled data, r = 0.52, P ≤ 0.01). Early changes in inspiratory muscle strength were assessed after 2 min of resistive breathing. PImax was lower (P ≤ 0.05) in females, but had not yet decreased significantly in males (F: 10.2 ± 3.8% drop from resting PImax; M: 5.1 ± 4.5% drop from resting PImax) (Fig. 2a). The rate of inspiratory muscle fatigue, determined by the slope of the change in maximal inspiratory efforts during the resistive breathing protocol, was attenuated in the females compared with males (F: −1.5 ± 0.4 cm H2O·min−1; M: −2.9 ± 0.3 cm H2O·min−1; P ≤ 0.05). This finding was also found when expressed relative to resting PImax (F:−1.0 ± 0.3% drop from resting PImax; M: −1.7 ± 0.2% drop from resting PImax; P ≤ 0.05) (Fig. 3). The absolute rate of inspiratory muscle fatigue was not correlated with body surface area (pooled data, r = −0.26; females, r = 0.01; males, r = −0.03; P > 0.05), suggesting that this finding reflects a difference between genders and not simply a difference in body size between the groups. At task failure, the decrease in PImax, expressed relative to resting PImax, was similar between females (85.2 ± 2.5%) and males (83.1 ± 2.2%) (Fig. 2a). Time to task failure was not significantly different between genders (F: 843.1 ± 123.6 s; M: 735.8 ± 99.6 s). During recovery, the analysis of variance for absolute PImax values revealed significant main effects for both gender and time (no interaction effect). Females and males were found to return to resting PImax within 15 and 20 min following task failure, respectively (Fig. 1a). When recovery PImax values were expressed relative to the prefatigue PImax values (i.e., normalized to differences in absolute strength between genders) no difference between genders was observed in the recovery from fatiguing inspiratory muscle exercise (Fig. 1b).
FVC was not significantly changed from resting values at task failure or after 45 min of recovery in either gender (F: −0.1 L·min−1; M, −0.2 L·min−1) (Table 1). This finding suggests that changes in PImax following resistive breathing is not likely attributed to alterations in lung volume.
Gender comparisons when matched for strength.
Females and males matched for resting PImax were found to have similar physical characteristics (see Table 2). Resting PImax was −160.0 ± 2.0 cm H2O and −159.6 ± 2.8 cm H2O for females and males, respectively. After 2 min of resistive breathing, females resulted in a significant drop in PImax (F: 11.9 ± 5.3% drop from resting PImax; P ≤ 0.05) that was not found to be statistically significant for the males (M: 7.1 ± 6.2% drop from resting PImax;; P = 0.15) (Fig. 2b). The rate of inspiratory muscle fatigue during resistive breathing was found to be slower for females than males when analyzed for both absolute (F:−1.5 ± 0.3 cm H2O·min−1; M: −2.9 ± 0.5 cm H2O·min−1; P ≤ 0.05) and relative (F: −0.9 ± 0.2% drop from resting PImax; M: −1.8 ± 0.4% drop from resting PImax; P ≤ 0.05) changes (Fig. 3), consistent with the findings found in the original gender comparison. This finding confirms that a gender difference exists in the rate of inspiratory muscle fatigue and is not a consequence of differing initial absolute values used in the slope analysis. At task failure, both females and males demonstrated inspiratory muscle fatigue (F: −139.8 ± 4.7 cm H2O; M: −126.2 ± 4.7 cm H2O), but the magnitude of fatigue was greater for males as compared with females (F: 87.4 ± 2.6% resting PImax; M: 79.2 ± 3.4% resting PImax; P ≤ 0.05) (see Fig. 2b). This finding is in contrast to the original gender comparison and indicates that males may be more fatigable than females during target resistive breathing. Time to task failure was found to be similar between the genders (F:749.6 ± 174.6 s; M: 782.8 ± 201.6 s), and no gender difference was found during the recovery of inspiratory muscle strength following task failure, in agreement with the original gender comparison.
The primary purpose of the present study was to compare the fatigability of inspiratory muscles of females and males while performing constant-load resistive breathing to task failure. We hypothesized that females would result in a greater magnitude and/or faster rate of inspiratory muscle fatigue than males due to findings that indicate that females may experience inadequate alveolar-to-arterial O2 exchange (11) and/or greater O2 cost for ventilation (27). The primary findings of this study are that i) females demonstrate inspiratory muscle fatigue early (2 min) during resistive breathing that is not seen in males, ii) the time to task failure is similar between females and males during resistive breathing and is independent of maximal strength (resting PImax), iii) females demonstrate a slower absolute and relative (i.e., percent of resting PImax) rate of inspiratory muscle fatigue compared with males, and iv) males result in a greater magnitude of inspiratory muscle fatigue at task failure compared with strength-matched females. These findings are in contrast to our hypotheses and suggest that during resistive breathing females do not undergo fatigue processes that are in excess to that experienced by males. Instead, the slower rate of inspiratory muscle fatigue and attenuated muscle fatigue at task failure in the strength-matched comparison indicates that females may exhibit a resistance to inspiratory muscle fatigue, consistent with what has been found in other skeletal muscles (9,12,14,15,29). The additional comparison between females and males matched for resting maximal strength (PImax) also suggests that the results of the present study are due to a true gender difference and not simply a difference in absolute strength.
Rate of muscle fatigue was slower for females than males.
The rate of muscle fatigue development was determined using an approach previously described by Fulco and colleagues (9). That is, the slope of the decline in maximal force development assessed at regular intervals during the submaximal fatigue test defines the rate of muscle fatigue. As such, the rate of fatigue development is determined independent of the actual time to task failure. Using this approach, we found that females developed inspiratory muscle fatigue at a significantly slower rate than the males in response to performing a constant-load breathing test, even when matched for absolute strength. This demonstrates that the difference in rate of muscle fatigue between females and males was not dependent on absolute strength or the higher initial PImax value for males. It is presently unclear why the slower rate of inspiratory muscle fatigue in the females did not translate into an appreciably longer time to task failure. Although the time to task failure was not statistically different between genders, females performed resistive breathing on average 13% longer than the males. It is evident from the standard error values that considerable intersubject variability may have precluded finding a statistically significant difference. Other factors may influence task failure during resistive breathing such as hypercapnia and hypoventilation (21); however, we don't believe these variables played a significant role in the present study due to a moderate contraction frequency and comfortable duty cycle that allowed for a tolerable breathing pattern.
During normal breathing at rest, Toplin et al. (27) provides evidence to suggest that the respiratory muscles of females consume more O2 than those of males for the same relative task. If a gender difference does exist in respiratory muscle O2 consumption, the difference is not associated with gender differences in the elasticity of the lungs (10), chest wall compliance (7), or tracheal area (13), because these variables are similar between females and males. One possibility may be that females have a greater work of breathing than males for a given ventilation because of a smaller lung volume and increased breathing frequency. McClaran et al. (20) has demonstrated maximal expiratory flow limitation and lung hyperinflation in females as a result of a smaller lung volume during maximal flow rates during heavy exercise. However, in contrast to heavy exercise, the present study required subjects to reach a submaximal target pressure that was only maintained intermittently (18 breaths per minute, approximately 50% duty cycle). Based on tidal volume and breathing frequency alone, it is likely that the males in the present study had a greater ventilatory work of breathing than females due to a larger functional tidal volume to achieve a larger absolute inspiratory pressure. Although lung volumes were not measured in the present study during resistive breathing, we speculate that this would translate to higher respiratory muscle O2 demand during resistive breathing for males compared with females, which would have contributed to the faster rate of muscle fatigue found for males in the present study.
Early changes in inspiratory muscle fatigability.
Interestingly, in spite of the overall slower rate of muscle fatigue, females were found to have a significantly greater decline in inspiratory muscle force-generating capacity than males during the first 2 min of resistive breathing. This finding suggests that females may be less able to meet the metabolic demands of resistive breathing than males during the initial stages of exercise, but undergo a transition to a more efficient metabolic regenerative process to result in a slower rate of inspiratory muscle fatigue than males. Although we are unaware of gender differences in diaphragm muscle fiber-type composition, we acknowledge that the human diaphragm is composed of approximately 76% highly oxidative muscle fibers, 21% of which is thought to be comprised of low-oxidative fast-twitch muscle fibers (18). Interestingly, Lieberman et al. (18) has shown in the guinea pig diaphragm that the initial decline in maximal tension during repeated diaphragmatic stimulations occurs in the area of the diaphragm composed primarily of low-oxidative fast-twitch fibers. If this is the case for humans during resistive breathing, it can be postulated that females in the present study experienced more muscle fatigue in the first 2 min of intermittent inspiratory muscle contractions because of a lower potential for glycolysis relative to oxidative phosphorylation in inspiratory muscle oxidative fast-twitch fibers (26). Furthermore, adaptation to this type of exercise would likely be more difficult for females than males because females have a reduced capacity of the diaphragm to produce volume displacements and high inspiratory flow rates because of a shorter diaphragm and smaller rib cage cross-sectional area (3). Therefore, a combination of a lower potential for glycolysis in inspiratory muscle oxidative fast-twitch fibers and thoracic limitations may have led to the females exhibiting a greater degree of inspiratory muscle fatigue early on during the fatigue protocol compared with the males.
Magnitude of inspiratory muscle fatigue.
Inspiratory muscle fatigue at task failure was observed in all subjects in the present study. The level of inspiratory muscle fatigue induced in the present study (15-20%) is close to that reported by other studies utilizing a target resistive breathing task (23). However, the present study provides new information in that gender differences in inspiratory muscle fatigue were found following resistive breathing. Females and males resulted in a similar magnitude of fatigue (∼1/415%) at task failure when unmatched for strength; however, males exhibited a greater magnitude of inspiratory muscle fatigue when compared with strength-matched females (−21 vs −13%, respectively). We acknowledge that the sample size in the strength-matched comparison is relatively small, but we are confident that the gender difference found at task failure is real (effect size = 1.1). The mechanism behind males resulting in a greater inspiratory muscle fatigue at task failure than females is beyond the scope of this study, but based on studies in other skeletal muscles, the mechanism may be related to gender differences in central drive (14) or muscle metabolism (25).
At present, it is unknown whether inspiratory muscle recruitment pattern during resistive breathing is different for females and males, but a recent report by Bellemare et al. (3) indicates that this may be a likely possibility. It was determined by the ratio of gastric to transdiaphragmatic pressure that during breathing at rest, females exhibited a greater inspiratory intercostal muscle contribution than males, which was postulated to be a consequence of females having a greater inclination of the ribs than males as measured by chest radiographs. A similar tendency was found during inspiratory capacity maneuvers, but the gender difference did not reach statistical significance. Nonetheless, these findings indicate that differences in thoracic configuration causes variability in inspiratory muscle recruitment between females and males, which may result in different levels of inspiratory muscle fatigue between the inspiratory muscles.
We are unable to discern from the present study whether inspiratory muscle fatigue was localized to the diaphragm or whether accessory respiratory muscles were also affected. However, the results of a recent study by Rohrbach et al. (23) indicated that both diaphragmatic and intercostal muscle fatigue occurred during constant-load resistive breathing to task failure. It is generally thought that the inspiratory muscles do not generate the same tension with each breath during loaded breathing, and that the recruitment of inspiratory muscles may be coordinated in such a way that they protect the diaphragm against fatigue. If inspiratory muscle recruitment patterns differ between females and males during resistive breathing, the results of the present study suggest that it does not result in an appreciable improvement in exercise tolerance because the time to task failure was similar for females and males, but may explain the gender differences found in the rates of muscle fatigue.
Time to task failure for females and males.
In agreement with previous studies (8), the time to task failure for inspiratory resistive breathing was similar between females and males. The inspiratory muscle endurance times measured in this study are similar to the age-matched durations reported by others for a similar inspiratory task (8), suggesting that the subjects were highly motivated. The finding that the time to task failure was similar between females and males indicates that absolute inspiratory muscle strength does not determine inspiratory muscle endurance during resistive breathing. If a strong relationship exists between inspiratory muscle strength and time to task failure (8), a gender difference should have been found in the present study for time to task failure because PImax was found to be greater for males compared with females. However, the time to task failure during resistive breathing was similar for females and males, indicating that factors other than absolute force production contributed to task failure. The low correlation between PImax and time to task failure for the overall group in the present study (r = −0.20) is consistent with this view.
Previous studies have shown that residual volume increases following exercise (5), and that an increase in residual volume of approximately 0.5 L significantly reduces PImax (6). It is thought that the change in residual volume places the diaphragm at a less optimal position on its length-tension relationship, thereby developing less pressure. Although we did not directly assess changes in residual volume, FVC was measured in the present study before and after resistive breathing to evaluate possible changes in functional vital capacity that may have occurred during resistive breathing. We recognize that FVC is not the optimal test for evaluating changes in lung volume, but a significant increase in residual volume would theoretically decrease FVC. The results of the present study found no difference in FVC for either gender from pre- to postfatigue, suggesting that the attenuated PImax values observed at task failure in the present study were due to inspiratory muscle fatigue and not changes in lung volume.
In conclusion, gender differences are present in the fatigability of the inspiratory muscles of humans. In contrast to our hypotheses, females were found to have a slower rate of inspiratory muscle fatigue than males during resistive breathing, which resulted in less inspiratory muscle fatigue at task failure compared with strength-matched males. Our finding that females demonstrate a greater inspiratory muscle fatigue than males during the first 2 min of resistive breathing indicates a gender difference in inspiratory muscle recruitment and/or metabolic pathways utilized at the onset of resistive breathing. However, a similar fatigue function may occur during resistive breathing to limit females and males to a similar time to task failure despite different absolute strength. The overall results of the present study suggest that the inspiratory muscles of females may fatigue at a slower rate than males. Although it is not possible to discern the mechanism(s) responsible for the gender differences found in the present study, future studies comparing females and males with similar pulmonary function (e.g., lung volumes, thoracic dimensions) are warranted.
1. Babcock, M. A., D. F. Pegelow, S. R. McClaran, O. E. Suman, and J. A. Dempsey. Contribution of diaphragmatic power output to exercise-induced diaphragm fatigue. J. Appl. Physiol
. 78:1710-1719, 1995.
2. Bellemare, F., and B. Bigland-Ritchie. Assessment of human diaphragm strength and activation using phrenic nerve stimulation. Respir. Physiol
. 58:263-277, 1984.
3. Bellemare, F., A. Jeanneret, and J. Couture. Sex differences in thoracic dimensions and configuration. Am. J. Respir. Crit. Care Med
. 168:305-312, 2003.
4. Black, L. F., and R. E. Hyatt. Maximal inspiratory pressures: normal values and relationship to age and sex. Am. Rev. Respir. Dis
. 99:696-702, 1969.
5. Buono, M. J., S. H. Constable, A. R. Morton, T. C. Rotkis, P. R. Stanforth, and J. H. Wilmore. The effect of an acute bout of exercise on selected pulmonary function measurements. Med. Sci. Sports Exerc
. 13:290-293, 1981.
6. Coast, J. R., and S. D. Weise. Lung volume changes and maximal inspiratory pressure
. J. Cardiopulmonary Rehabil
. 10:461-464, 1990.
7. Estenne, M., J. C. Yernault, and A. De Troyer. Rib cage and diaphragm-abdomen compliance in humans: effects of age and posture. J. Appl. Physiol
. 59:1842-1848, 1985.
8. Fiz, J. A., P. Romero, R. Gomez, et al. Indices of respiratory muscle endurance in healthy subjects. Respir
. 65:21-27, 1998.
9. Fulco, C. S., P. B. Rock, S. R. Muza, et al. Slower fatigue and faster recovery of the adductor pollicis muscle in women matched for strength with men. Acta Physiol. Scand
. 167:233-239, 1999.
10. Gibson, G. J., N. B. Pride, C. O'Cain, and R. Quagliato. Sex and age differences in pulmonary mechanics in normal nonsmoking subjects. J. Appl. Physiol
. 41:20-25, 1976.
11. Harms, C. A., S. R. McClaran, G. A. Nickele, D. F. Pegelow, W. B. Nelson, and J. A. Dempsey. Exercise-induced arterial hypoxemia in healthy young women. J. Physiol
. 507:619-628, 1998.
12. Hicks, A. L., J. Kent-Braun, and D. S. Ditor. Sex differences in human skeletal muscle fatigue
. Exercise Sport Sci. Rev
. 29:109-112, 2001.
13. Hoffstein, V. Relationship between lung volume, maximal expiratory flow, forced expiratory volume in one second, and tracheal area in normal men and women. Am. Rev. Respir. Dis
. 134:956-961, 1986.
14. Hunter, S. K., A. Critchlow, I.-S. Shin, and R. M. Enoka. Men are more fatigable than strength-matched women when performing intermittent submaximal contractions. J. Appl. Physiol
. 96:2125-2132, 2004.
15. Hunter, S. K., and R. M. Enoka. Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J. Appl. Physiol
. 91:2686-2694, 2001.
16. Johnson, B. D., M. A. Babcock, O. E. Suman, and J. A. Dempsey. Exercise-induced diaphragmatic fatigue in healthy humans. J. Physiol
. 460:385-405, 1993.
17. Knudson, R. J., M. D. Lebowitz, C. J. Holberg, and B. Burrows. Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am. Rev. Respir. Dis
. 127:725-734, 1983.
18. Lieberman, D. A., J. A. Faulkner, A. B. Craig Jr., and L. C. Maxwell. Performance and histochemical composition of guinea pig and human diaphragm. J. Appl. Physiol
. 34:233-237, 1973.
19. Martin, B., M. Heintzelman, and H. I. Chen. Exercise performance after ventilatory work. J. Appl. Physiol
. 52:1581-1585, 1982.
20. McClaran, S. R., C. A. Harms, D. F. Pegelow, and J. A. Dempsey. Smaller lungs in women affect exercise hyperpnea. J. Appl. Physiol
. 84:1872-1881, 1998.
21. McKenzie, D. K., G. M. Allen, J. E. Butler, and S. C. Gandevia. Task failure with lack of diagragm fatigue during inspiratory resistive loading in human subjects. J. Appl. Physiol
. 82:2011-2019, 1997.
22. Mead, J. Dysanapsis in normal lungs assessed by the relationship between maximal flow, static recoil, and vital capacity. Am. Rev. Respir. Dis
. 121:339-342, 1980.
23. Rohrbach, M., C. Perret, B. Kayser, U. Boutellier, and C. M. Spengler. Task failure from inspiratory resistive loaded breathing: a role for inspiratory muscle fatigue
? Europ. J. Appl. Physiol
. 90:405-410, 2003.
24. Roussos, C. S., and P. T. Macklem. Diaphragmatic fatigue in man. J. Appl. Physiol
. 43:189-197, 1977.
25. Russ, D. W., and J. A. Kent-Braun. Sex differences in human skeletal muscle fatigue
are eliminated under ischemic conditions. J. Appl. Physiol
. 94:2414-2422, 2003.
26. Simoneau, J.-A., G. Lortie, M. R. Boulay, M. C. Thibault, G. Theriault, and C. Bouchard. Skeletal muscle histochemical and biochemical characteristics in sedentary male and female subjects. Can. J. Appl. Physiol
. 63:30-35, 1985.
27. Topin, N., P. Mucci, M. Hayot, C. Prefaut, and M. Ramonatxo. Gender influence on the oxygen consumption of the respiratory muscles in young and older healthy individuals. Int. J. Sports Med
. 24:559-564, 2003.
28. Wen, A. S., M. S. Woo, and T. G. Keens. How many maneuvers are required to measure maximal inspiratory pressure
29. West, W., A. Hicks, L. Clements, and J. Dowling. The relationship between voluntary electromyogram, endurance time and intensity of effort in isometric handgrip exercise. Europ. J. Appl. Physiol
. 71:301-305, 1995.
30. Wijkstra, P. J., T. W. van der Mark, M. Boezen, R. van Altena, D. S. Postma, and G. H. Koeter. Peak inspiratory mouth pressure in healthy subjects and in patients with COPD. Chest