AVIN, KEITH G.; NAUGHTON, MAUREEN R.; FORD, BRETT W.; MOORE, HALEY E.; MONITTO-WEBBER, MAYA N.; STARK, AMY M.; GENTILE, A. JOHN; FREY LAW, LAURA A.
Women have demonstrated greater fatigue resistance for a variety of tasks, including isometric force matching (19,22), isometric position matching (22), and isometric contractions with intermittent rests (37). Several factors have been considered to explain observed differences in fatigue resistance, ranging from muscle mass differences to hormonal influences (12). However, others have reported no sex differences in fatigue resistance with isometric force-matching tasks (9,41). In a recent review, Hunter (16) suggests that sex differences in muscle fatigue can be influenced by task specificity: encompassing contraction mode, contraction intensity, position- versus load-matching tasks, cognitive load, age, and muscle group. Thus, the statement that women are more fatigue resistant than men for relative-intensity tasks is clearly an oversimplification.
In particular, a review of several fatigue studies suggests that there are differences in the sex effect between elbow flexor and ankle dorsiflexor muscles (16). However, this comparison has never been directly assessed in the same cohort of individuals. Thus, these apparent sex differences between muscle groups could simply be due to cohort or methodological variance. Other potential mediating factors may include peak torque (18,19), muscle activation strategies (18,34), and/or noxious afferent feedback (16). Whether these factors contribute to sex differences or vary between muscle groups is not clear.
Thus, the primary purpose of this study was to examine sex differences in fatigue resistance at two distinct muscle groups, the elbow flexors and the ankle dorsiflexors, considering several potential contributors to fatigue. These factors included peak torque, self-reported activity level, muscle activation strategy, perceived pain, perceived exertion, and rate of increase for pain and exertion. This finding may help to better elucidate the underlying mechanisms contributing to sex differences in fatigue resistance. For example, if fatigue differences are indeed muscle group specific, local (e.g., muscle mass) rather than systemic (e.g., hormonal milieu) mechanisms are likely to be responsible for this phenomenon. This information may be used to better discern whether sex differences are widespread or localized phenomena. An improved understanding of factors influencing fatigue may be useful for mathematical fatigue modeling applications as well as impact optimal training and performance in sport, exercise, and rehabilitation applications.
Thirty-two recreationally active young adults (16 men and 16 women) participated in this study (for subject demographics, see Table 1). All subjects were classified as healthy with no major medical history, including cardiovascular disease, asthma, diabetes, elbow or ankle major joint trauma, neuromuscular disease, or chronic pain conditions. Subjects who were college- or professional-level athletes were excluded because of their unique level of training. Before participation, all subjects provided written, informed consent. The study procedures were approved by the University of Iowa institutional review board. All participants were reimbursed for their time.
Subjects performed isometric force-matching fatigue tasks at 50% maximal voluntary isometric contraction (MVIC) for both elbow flexion and ankle dorsiflexion during one visit. The order of testing was block randomized by sex to minimize any fatigue effects. A 20-min rest was provided between the two fatigue tasks, during which time participants completed the activity questionnaire.
The fatigue task for each muscle group started with a 5-min warm-up on a stationary bike, followed by assessing maximum torque generating capability using a Biodex Isokinetic Dynamometer System 3 (Biodex Medical Systems, Shirley, New York). Maximum torque was operationally defined as the maximum of three MVIC trials separated by 1-min rests. The fatigue task was then performed using the isokinetic dynamometer at 50% MVIC until volitional failure with visual and verbal feedback. Failure was operationally defined as the inability to maintain torque within 10% of the target level for 5 s or falling below the target level three times within a 30-s window. For the elbow flexion fatigue task, subjects were seated, with the forearm positioned at 60° of elbow flexion and the shoulder flexed approximately 30°. For the ankle dorsiflexion fatigue task, subjects were tested in a seated position, with the knee flexed approximately 90° and the ankle positioned at 20°of plantarflexion.
Participants were asked to verbally rate their pain and exertion throughout and immediately after the fatigue tasks using the Borg category ratio 0-10 numeric rating scale (1). A written script, modified from Borg (1), was read to each participant to ensure consistent instructions for scale use. The peak values were extracted for further analysis. The mean rate of change for pain and exertion was calculated using linear regression techniques for each individual subject (i.e., slope of each rating vs time relationship). Immediately after the fatigue protocol for both the ankle and the elbow, participants completed the McGill Pain Questionnaire-Short Form (SF MPQ). The SF MPQ is comprised of three subscales, providing both qualitative and quantitative pain assessments. Participants rated their pain using 15-adjective verbal descriptors, a 10-cm horizontal visual analog scale, and a 6-point evaluative scale.
Height (cm) and weight (kg) were measured using calibrated scales to document subject demographics. Activity levels were assessed using the International Physical Activity Questionnaire (IPAQ), a self-report measure of activities performed in the past 7 d (3). Assessments include estimates of leisure, domestic and gardening, work, and transportation-related physical activities. Calculated algorithms on the basis of activity levels classify the participant as low, moderate, or high physical activity (3).
Muscle activity was measured using four channels of surface muscle EMG (Delsys Bagnoli, Boston, MA), band-pass filtered from 20 to 450 Hz. For the elbow, EMG electrodes were attached to the skin over the biceps brachii, brachioradialis, triceps brachii, and upper trapezius muscles. For the ankle, EMG electrodes were attached to the skin over the tibialis anterior, medial and lateral gastrocnemius, and soleus muscles. The skin was prepared with 70% alcohol wipes, and electrodes were adhered using medical-grade adhesive tapes. The EMG signals are preamplified peripherally at the electrode (10 times) and again before analog-to-digital conversion (1000 times) to maximize signal quality.
All torque and EMG signals were collected using custom Labview (National Instruments, Austin TX) software at 1000 Hz. Torque signals were low-pass filtered at 10 Hz. Absolute and normalized (by body mass) peak torque values were used in the analyses. Times to fatigue were determined from the torque tracings offline and corroborated with stop watch results collected during each fatigue trial. The EMG data were rectified, filtered using a moving average with a 200-ms window, and standardized by their respective maximum EMG values. EMG data were averaged across each successive 5% time interval from 0% to 100% endurance time for each muscle.
Summary statistics were calculated for endurance time, peak torque, peak torque normalized by body mass, peak pain and exertion, mean rate of change for pain and exertion, surface EMG, and demographic data. Data are reported as mean ± SEM within the text and figures. Independent and paired t-tests were used to compare endurance time and peak torque between sexes for each muscle group and secondarily between the two muscle groups. Repeated-measures ANOVA was used to compare EMG amplitude between sexes and between muscle groups at 25%, 50%, and 75% of task duration, with follow-up paired t-tests as appropriate. Effect sizes (Cohen's d) were calculated for between-joint and between-sex differences. Large effect sizes were operationally defined as d values of 1.0 or greater. Correlation analyses assessed the relationships between endurance time and the following variables: peak torque, normalized peak torque (peak torque/body mass), peak pain, peak exertion, rate of pain increase, and rate of exertion increase for each muscle group separated by sex. Stepwise, linear regression techniques were used to model endurance time for each muscle group as a function of sex, peak torque, rate of pain or exertion, and activity level. All statistical analyses were performed using the Statistical Package for the Social Sciences for Windows (Version 16.0, SPSS Inc., Chicago, IL), with alpha set at 0.05.
Subject demographics are provided in Table 1. Men were heavier and taller than women, but age and activity levels were not significantly different. Self-reported activity levels were predominant in the moderate (n = 15) and high activity (n = 15) levels, with only one in the low range on the basis of normative data for the IPAQ (3). One subject's IPAQ data were excluded as the survey was not completed correctly.
Women (112.3 ± 6.2 s) were significantly more resistant to fatigue than men (80.3 ± 5.8 s) for elbow flexion (P = 0.001; see Fig. 1). Conversely, no significant difference (P = 0.45) in endurance time occurred between women (140.6 ± 10.7 s) and men (129.2 ± 10.5 s) for the ankle dorsiflexion task. The corresponding effect sizes (Cohen's d) for the observed sex difference were large for the elbow flexors but small for the ankle dorsiflexors (Table 2). Comparing endurance times between muscle groups revealed that ankle dorsiflexion was more resistant to fatigue than elbow flexion for both women (Δ 28.3 s, P = 0.021) and men (Δ 48.9 s, P < 0.001). The corresponding effect sizes for the ankle to elbow muscle group differences were 0.85 and 1.49 for women and men, respectively.
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).
FIGURE 2-Linear regr...Image Tools
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.
FIGURE 3-Mean EMG fo...Image Tools
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.
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