Men exhibited greater peak torque (P < 0.0001) than women (Fig. 1B) at both the ankle (45.0 ± 1.7 vs 30.1 ± 1.0 N·m, respectively) and the elbow (75.7 ± 3.1 vs 34.4 ± 2.2 N·m, respectively). Similar differences were observed for normalized peak torque (Fig. 1C) for men and women, respectively, at the ankle (0.58 ± 0.02 vs 0.51 ± 0.01 N·m·kg−1) and at the elbow (0.97 ± 0.03 vs 0.58 ± 0.03 N·m·kg−1). The corresponding effect sizes for peak torque sex differences were large for both muscle groups (Table 2). Peak torque and normalized peak torque were significantly related to endurance time at the elbow (Figs. 2A and C) but not at the ankle (Figs. 2B and D).
Peak torque and normalized peak torque were significantly greater for the elbow flexors than the ankle dorsiflexors for men (P < 0.0001) but did not reach significance (P > 0.06) in women. Accordingly, the effect sizes for the between-joint peak torque differences were large for men (3.16) but only moderate for women (0.65).
EMG data were incomplete because of data collection complications during the ankle (n = 4) and the elbow (n = 6) fatigue tasks; thus, sample sizes were reduced for the muscle activity analyses. Using the ANOVA, mean EMG increased significantly over time during the 50% fatigue tasks for both muscle groups and sexes (P < 0.0001; Fig. 3). Muscle activity did not vary between men and women (P = 0.13). However, EMG was significantly higher at the elbow than at the ankle overall (P = 0.001) and increased at a greater rate than the ankle (P = 0.04). Follow-up paired t-tests at 25%, 50%, and 75% of total endurance time were further analyzed to determine if one muscle group was consistently greater. These tests revealed that elbow muscle activity was significantly greater than ankle muscle activity at each relative time point assessed: 25% (P = 0.012), 50% (P = 0.003), and 75% (P = 0.001) of endurance time.
Perceived pain and exertion.
Both men and women reported similar peak pain and exertion ratings across both muscle groups (Figs. 4A and C, P > 0.15). The absolute time of each fatigue task did not appear to influence peak perceptual ratings because women were able to sustain the elbow task longer than men, with no significant difference in peak ratings. The ankle fatigue task was reported to be significantly more painful than the elbow task across all subjects (Fig. 4A, P = 0.016) but did not achieve significance when considering only male (P = 0.08) or female (P = 0.09) subjects separately. Peak exertion did not vary between muscle groups (Fig. 4B, P = 0.24). The mean pain increase per minute did not vary between sexes or muscle groups (Figs. 4B and D, P > 0.65). However, men reported significantly faster increases in perceived exertion at the elbow (P = 0.002) than women, resulting in a significant overall difference between muscle groups (P = 0.003). The most frequently identified qualitative pain descriptors on the SF MPQ immediately after fatigue for both tasks were "cramping," "aching," and "tiring/exhausting."
No pain measures (peak or rate of change) resulted in significant correlations with endurance time. In men, both ankle and elbow endurance times were related to exertion rate of change (r = −0.81 and −0.82, respectively), whereas in women, only ankle endurance time was correlated to exertion rate of change (r = −0.67). Peak exertion did not significantly correlate with any endurance time variables.
Predicting endurance time.
For the elbow, only sex was a significant predictor in the model to predict endurance time (considering peak torque, sex, and self-reported activity) using stepwise linear regression techniques (R2 = 0.30). Once sex was accounted for, peak torque did not add any additional predictive information, but these two variables were collinear (r = 0.89). Thus, either variable provided essentially equivalent information (i.e., Fig. 2A). For the ankle, no linear regression model achieved significance, using peak torque, sex, and self-reported activity levels as possible predictors.
The most notable findings of this study are as follows: 1) the large sex differences in fatigue associated with sustained isometric contractions at the elbow were not observed at the ankle, 2) peak torque was a good predictor of fatigue resistance only at the elbow, 3) muscle activation strategies differed between muscle groups but not between sexes, 4) no sex differences were exhibited for peak pain or exertion ratings across both muscle groups, and 5) the ankle fatigue task was reported to be significantly more painful than the elbow task across all subjects.
The observed endurance times for both ankle dorsiflexion and elbow flexion are consistent with other published values (10,29,34), suggesting that our study population was not substantially different from other populations investigated. The observed sex differences for the elbow flexors (effect size, d = 1.4) are largely in accordance with previous findings at the elbow, with a median effect size of 0.8 from previous studies (range = −0.7 to 3.9) (2,4,9,18,19,21,22,44). At the ankle, the median effect size was 0.1 (range = −1.1 to 3.1) (14,15,24,31,33,39), similar to that observed here (d = 0.3). Thus, women consistently are significantly more resistant to fatigue than men for elbow flexors but not for ankle dorsiflexors. Few other muscle groups have been systematically studied for sex differences, but the limited evidence available suggests that sex differences may not be readily predictable, as shoulder abduction was not different between men and women, whereas trunk flexion was more fatigue resistant in women (43).
Historically, assessment of isometric endurance between men and women has been performed at single, not multiple, muscle groups. Underlying differences in protocols and/or laboratory settings confound the ability to conclusively evaluate regional versus systemic sex differences in fatigue resistance. A limited number of studies include two muscle group protocols but typically had very small sample sizes and/or no representation of women. The current study demonstrates that sex differences in fatigue development during a sustained isometric force task are regional and muscle group dependent. Thus, the regional differences suggested in a recent review (16) are further substantiated by our findings.
In studies that have observed fatigue sex differences, the most commonly postulated explanatory mechanisms can be parceled into muscle mass/perfusion, neuromuscular activation, and substrate utilization. Hicks et al. (12) suggest that larger massed muscles may result in greater intramuscular pressure and blood flow occlusion at a given contraction intensity, resulting in more rapid fatigue when compared with smaller muscles. Because peak torque is roughly proportional to muscle mass (via cross-sectional area), endurance time has been noted to decrease linearly (23) or exponentially (40) with increasing peak torque. However, in the current study, women were weaker than men for both muscle groups, yet only the elbow yielded a significant sex difference in endurance time. In addition, peak torque explained 30% of the variance in endurance time at the elbow but only 3% at the ankle. These findings suggest that muscle mass may be one contribution to fatigue differences but cannot fully account for variations in endurance time between men and women, particularly across bodily regions.
Additional vascular mechanisms, such as vascular reactivity and vasoconstriction, are not uniform throughout the body (36) and thus could influence muscle perfusion during a sustained fatiguing contraction. Clearly, the lower extremities are chronically exposed to elevated hydrostatic pressures in upright postures, suggesting that upper and lower limbs may differentially respond to changes in intramuscular pressure. Sex differences have been documented in vasodilatation (35), capillary fluid filtration (28), and blood flow during sustained (40) and brief maximal (20) contractions. However, blood flow and vascular conductance were not able to explain sex differences in fatigue using an intermittent contraction endurance task (20). Thus, it is not yet clear whether differential limb vascular response can potentially explain a portion of the regional fatigue sex differences observed between the elbow and the ankle.
Neuromuscular activation strategies, assessed via comparison of EMG amplitudes, were similar to previous studies with a gradual increase in activation over time during a submaximal isometric task (8,24). Unfortunately few, if any, studies have compared EMG activation between men and women at more than one muscle group. Consistent with previous sustained isometric tasks that did not strength match women, no sex differences in activation strategy were evident at the elbow (19,23). However, when matched for strength, conflicting results have been observed. For example, at the elbow, women display a reduced rate of activation despite similar endurance times as men (18), whereas at the ankle, no sex differences in activation strategy or endurance time were observed (11). Although not strength matched, we also observed no difference in ankle activation strategy between men and women. However, both men and women consistently displayed greater EMG activity at the elbow compared with the ankle, suggesting that activation strategies may vary more between muscle groups than between sexes. Thus, muscle activation does not appear to play a key mechanistic role in explaining the fatigue sex differences observed only at the elbow.
Another possible neuromuscular activation component that could result in apparent sex differences in fatigue is central activation. If women do not maximally activate during the MVIC testing, that is, interpolated twitch techniques, then their relative-intensity target workload will be less than expected. A recent meta-analysis modeled endurance times as a function of task intensity for sustained isometric contractions at several joints (7). Using these models, the current 30-s difference in endurance time observed between men and women at the elbow would require a difference in central activation of 14%-16% between the sexes (e.g., 100% vs 84%-86%). It has been suggested that women are less able to achieve full central activation, similar to that seen in children (5), although the available data are inconsistent. Central activation ratios did not significantly differ between men and women for the elbow flexors (≤4%) (17) or the ankle dorsiflexors (≤1%) (26) before or after a fatiguing task. Thus, it is unlikely that voluntary activation sufficiently explains the difference in endurance time observed for the elbow flexors.
Substrate utilization has been suggested as another mechanism that may contribute to differences in fatigue between men and women (12). Men may preferentially rely on glycolytic pathways (38), whereas women may preferentially use oxidative processes for energy metabolism (42). Although this may contribute to sex differences in fatigue, particularly when evaluating fatigue resistance across a range of relative intensities, it is not clear how differences in substrate utilization may help explain the sex differences observed at a single intensity at the elbow but not the ankle. It may reflect differential motor-unit activation between men and women or possibly differences in daily functional use of these two muscle groups (e.g., training) between the sexes (e.g., walking vs lifting and carrying). Future studies are warranted to specifically assess the effect of daily use patterns on fatigue sex differences.
Variations in endurance time across bodily regions may be readily explained by differences in muscle composition. Elbow flexors (biceps brachii) are predominantly composed of type II fibers (∼61% ± 5% type II) (30), whereas the ankle dorsiflexors (tibialis anterior) are composed of primarily type I fibers (∼77% ± 7% type I) (25). These reported compositions mirror our observed endurance times, with the ankle dorsiflexors being more fatigue resistant than the elbow flexors overall. However, muscle composition has not been shown to significantly differ between men and women (32). Thus, although muscle fiber composition may be the leading explanation for the fatigue differences between muscle groups, it is less clear how muscle composition contributes to the sex differences observed predominantly for one muscle group. As previously mentioned, it may be that in muscle groups with greater type II fibers, women are better able to sustain contractions because of their preferential use of oxidative metabolism and activation of type I fibers. However, the relationship between muscle composition and fatigue resistance is complex and may vary by task intensity. Endurance times of the elbow flexor and extensor groups did not differ at 40% MVIC but differed by more than 600% at 10% MVIC despite similar compositions (6).
Differential excitation between men and women of group III and group IV afferents during fatigue may lead to differences in muscle activation and/or endurance time (16). However, in this study, neither rate of pain increase or peak pain varied between sexes. This differs somewhat from studies demonstrating sex differences in elicited pain response after isometric exercise (13,27). Only the rate of exertion was significantly related to endurance time, suggesting that nociceptive input was not a primary mechanism explaining the observed localized sex differences. Group III and group IV afferents include a wide variety of afferent input, including nociceptive signals in response to changes in metabolite concentration. Thus, afferent signals uniquely contributing to perceived exertion may be important.
Several study limitations warrant discussion as they may impact further interpretation. The lack of significant sex difference in endurance time at the ankle may be a result that our study was underpowered to detect that level of effect size (0.3). Power analysis estimates indicate that 178 subjects per group would be needed to detect this small effect size as significant (P ≤ 0.05, β = 0.2). A small effect size would put into question the clinical relevance even if statistical significance was present with a sufficient sample size. A second potential limitation is that no methods such as interpolated twitch were used to measure the degree of muscle activation during the MVIC; therefore, we could not quantify if men and women were able to similarly fully activate their elbow flexor or ankle dorsiflexor muscle groups. Third, we caution against the extension of these results to additional muscle groups or tasks. Future studies are needed to better define whether sex differences in fatigue can be generalized across neighboring joints and/or extremities and to examine whether these muscle-dependent sex differences also occur with position-matching tasks in addition to force-matching tasks.
These results may have implications in rehabilitation and sport as well as ergonomics. Regardless of whether the goal is to restore function or to improve performance, exercise prescription may be erroneously based on inappropriate dose-response relationship assumptions that the body fatigues uniformly between sexes and muscle groups. This information may be most directly applicable to the postsurgical patient where isometric contractions are a frequent intervention. In addition, it may be valuable for the advancement of mathematical fatigue models used increasingly in ergonomic applications. To this end, accurate models will require more information highlighting the multifaceted influences on fatigue.
In summary, this study demonstrated that sex differences in fatigue resistance are not necessarily uniform and systemic but can vary by region, suggesting strong localized influences. Women were significantly more fatigue resistant for the elbow flexors but not the ankle dorsiflexors during sustained isometric contractions. Further, peak torque was associated with endurance time at the elbow but not the ankle. Thus, factors that may contribute to fatigue resistance for one muscle group (e.g., sex, peak torque) may not be critical for another. Future studies are needed to better delineate additional underlying mechanisms that may contribute to this phenomenon.
Author justification: This project was performed by all eight of the authors. Each author contributed to the development of the concept, design, and/or protocol. The first seven authors performed all data collection and initial processing. The first and the last authors performed all statistical analysis. The article was written largely by the first and the last authors, with input from the remaining six authors.
This study was sponsored in part by funding from the NIH grant nos. K12 HD055931 (LFL), 1K01AR056134 (LFL), and NRSA F31 AR056175 (KGA) and the Foundation for Physical Therapy (KGA).
The authors have no conflicts of interest to report.
We would like to acknowledge Carol Leigh for her assistance with manuscript preparation and Grant Norland with his assistance with data collection.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
1. Borg G. Borg's Perceived Exertion and Pain Scales
. Champaign (IL): Human Kinetics; 1998. p. 63-7.
2. Calder KM, Stashuk DW, McLean L. Physiological characteristics of motor units in the brachioradialis muscle across fatiguing low-level isometric contractions. J Electromyogr Kinesiol
3. Craig CL, Marshall AL, Sjostrom M, et al. International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc
4. Dimitrova NA, Arabadzhiev TI, Hogrel JY, Dimitrov GV. Fatigue analysis of interference EMG signals obtained from biceps brachii during isometric voluntary contraction at various force levels. J Electromyogr Kinesiol
5. Dotan R, Falk B. Task-specific sex differences in muscle fatigue: is there a common underlying cause? Exerc Sport Sci Rev
6. Fallentin N, Jorgensen K. Blood pressure response to low level static contractions. Eur J Appl Physiol Occup Physiol
7. Frey Law LA, Avin KG. Endurance time is joint-specific: a modeling and meta-analysis investigation. Ergonomics
8. Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM. Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol
9. Gamet D, Maton B. The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study. I. Assessment of muscular fatigue by means of surface EMG. Eur J Appl Physiol Occup Physiol
10. Hansen JW. Effect of dynamic training on the isometric endurance of the elbow flexors. Int Z Angew Physiol
11. Hatzikotoulas K, Siatras T, Spyropoulou E, Paraschos I, Patikas D. Muscle fatigue and electromyographic changes are not different in women and men matched for strength. Eur J Appl Physiol
12. Hicks AL, Kent-Braun J, Ditor DS. Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev
13. Hoeger Bement MK, Dicapo J, Rasiarmos R, Hunter SK. Dose response of isometric contractions on pain perception in healthy adults. Med Sci Sports Exerc
14. Houtman CJ, Heerschap A, Zwarts MJ, Stegeman DF. pH heterogeneity in tibial anterior muscle during isometric activity studied by (31)P-NMR spectroscopy. J Appl Physiol
15. Houtman CJ, Stegeman DF, Van Dijk JP, Zwarts MJ. Changes in muscle fiber conduction velocity indicate recruitment of distinct motor unit populations. J Appl Physiol
16. Hunter SK. Sex differences and mechanisms of task-specific muscle fatigue. Exerc Sport Sci Rev
17. Hunter SK, Butler JE, Todd G, Gandevia SC, Taylor JL. Supraspinal fatigue does not explain the sex difference in muscle fatigue of maximal contractions. J Appl Physiol
18. Hunter SK, Critchlow A, Shin IS, Enoka RM. Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. J Appl Physiol
19. Hunter SK, Enoka RM. Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J Appl Physiol
20. Hunter SK, Griffith EE, Schlachter KM, Kufahl TD. Sex differences in time to task failure and blood flow for an intermittent isometric fatiguing contraction. Muscle Nerve
21. Hunter SK, Lepers R, MacGillis CJ, Enoka RM. Activation among the elbow flexor muscles differs when maintaining arm position during a fatiguing contraction. J Appl Physiol
22. Hunter SK, Ryan DL, Ortega JD, Enoka RM. Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans. J Neurophysiol
23. Hunter SK, Schletty JM, Schlachter KM, Griffith EE, Polichnowski AJ, Ng AV. Active hyperemia and vascular conductance differ between men and women for an isometric fatiguing contraction. J Appl Physiol
24. Hunter SK, Yoon T, Farinella J, Griffith EE, Ng AV. Time to task failure and muscle activation vary with load type for a submaximal fatiguing contraction with the lower leg. J Appl Physiol
25. Jaworowski A, Porter MM, Holmback AM, Downham D, Lexell J. Enzyme activities in the tibialis anterior muscle of young moderately active men and women: relationship with body composition, muscle cross-sectional area and fibre type composition. Acta Physiol Scand
26. Kent-Braun JA, Ng AV, Doyle JW, Towse TF. Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol
27. Koltyn KF, Trine MR, Stegner AJ, Tobar DA. Effect of isometric exercise on pain perception and blood pressure in men and women. Med Sci Sports Exerc
28. Lindenberger M, Lanne T. Decreased capillary filtration but maintained venous compliance in the lower limb of aging women. Am J Physiol Heart Circ Physiol
29. Lowery M, Nolan P, O'Malley M. Electromyogram median frequency, spectral compression and muscle fibre conduction velocity during sustained sub-maximal contraction of the brachioradialis muscle. J Electromyogr Kinesiol
30. MacDougall JD, Sale DG, Alway SE, Sutton JR. Muscle fiber number in biceps brachii in bodybuilders and control subjects. J Appl Physiol
31. Melbech S, Johansen SH. Endurance time in slow and fast contracting muscle groups. Work Environ Health
32. Miller AE, MacDougall JD, Tarnopolsky MA, Sale DG. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol
33. Ng AV, Dao HT, Miller RG, Gelinas DF, Kent-Braun JA. Blunted pressor and intramuscular metabolic responses to voluntary isometric exercise in multiple sclerosis. J Appl Physiol
34. Ohashi J. Effects of contraction level on the changes of surface electromyogram during fatiguing static contractions. Ann Physiol Anthropol
35. Parker BA, Smithmyer SL, Pelberg JA, Mishkin AD, Proctor DN. Sex-specific influence of aging on exercising leg blood flow. J Appl Physiol
36. Proctor DN, Newcomer SC. Is there a difference in vascular reactivity of the arms and legs? Med Sci Sports Exerc
37. Russ DW, Elliott MA, Vandenborne K, Walter GA, Binder-Macleod SA. Metabolic costs of isometric force generation and maintenance of human skeletal muscle. Am J Physiol Endocrinol Metab
38. Russ DW, Lanza IR, Rothman D, Kent-Braun JA. Sex differences in glycolysis during brief, intense isometric contractions. Muscle Nerve
39. Shahidi AV, Mathieu PA. Endurance time characteristics of human ankle dorsiflexors and plantarflexors. Eur J Appl Physiol Occup Physiol
40. Thompson BC, Fadia T, Pincivero DM, Scheuermann BW. Forearm blood flow responses to fatiguing isometric contractions in women and men. Am J Physiol Heart Circ Physiol
41. Ulmer HV, Knieriemen W, Warlo T, Zech B. Interindividual variability of isometric endurance with regard to the endurance performance limit for static work. Biomed Biochim Acta
42. Venables MC, Achten J, Jeukendrup AE. Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study. J Appl Physiol
43. Yassierli, Nussbaum MA, Iridiastadi H, Wojcik LA. The influence of age on isometric endurance and fatigue is muscle dependent: a study of shoulder abduction and torso extension. Ergonomics
44. Yoon T, Schlinder Delap B, Griffith EE, Hunter SK. Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle Nerve
Keywords:©2010The American College of Sports Medicine
ISOMETRIC CONTRACTION; ELBOW; ANKLE; MAXIMUM ENDURANCE TIME