Introduction
Muscle fatigue, defined as the inability to maintain a given force or power output (8 10,15,32
Several studies have demonstrated that sex differences exist in muscle fatigue during exercise. Specifically, women typically display greater relative muscular endurance, defined as time to failure for a task at a given percentage of maximal strength, than men. This has been most often demonstrated following intermittent or sustained isometric contraction protocols of a low to intermediate intensity in a variety of muscle groups (2,9,16,18,20,24,31 3,18
Dynamic contractions are typically comprised of both concentric (i.e., muscle shortening) and eccentric (i.e., muscle lengthening) contractions. Eccentric contractions are 1 of the most important components of a training program designed to produce gains in muscle strength and size. Due to the force-velocity relationship of skeletal muscle function (13 11,30,33 6,7,12
While eccentric exercise is known to promote strength and size gains, the high forces involved also increase the risk of injury via muscle strain (1,4 19 17,22
While the ability of muscle to produce peak force is the most widely investigated index of muscle fatigue, additional information concerning the function of the muscle can also be gleaned from the torque-time profile generated during exercise. In addition to impairing the ability of the muscle to produce peak forces (i.e., muscle fatigue), sufficiently intense exercise protocols also cause changes in other contractile properties, such as an inability to produce muscular work and maximal rates of force development. These properties can affect performance variables, such as maximal power, and can also influence injury rates. For instance, if maximal force development rates drop, the muscle is less resistant to strain injuries as fatigue develops.
Even if men and women had similar deficits in force production, there may be underlying differences in contractile properties that could affect injury rates and performance. Therefore, sex differences were also tested for in contraction time, work , half relaxation time, and maximal rate of force development. As with maximal force, it was hypothesized that relative changes in the selected contractile properties would be similar between men and women.
Methods
Experimental Approach to the Problem
Muscle fatigue of the elbow flexors was tested by measuring maximal isometric strength prior to, during, and immediately postexercise. Eccentric strength was collected throughout exercise. Contractile properties of each eccentric contraction were then derived from the time-torque series produced by the subject. Testing in both contraction modes afforded an opportunity to describe changes in both static and dynamic muscle capabilities as exercise progressed.
Baseline (i.e., pre-exercise) isometric maximal voluntary contraction (MVC) strength was collected on 3 occasions 48 hours apart. Following baseline MVC testing on visit 3, subjects performed 50 maximal eccentric contractions of the elbow flexors in 5 sets of 10 repetitions, with 12 seconds between repetitions and 2 minutes of rest between sets. Torque was collected continuously during exercise and later used to calculate muscle function parameters, such as maximal eccentric torque (MET), contraction time, work , peak rate of force development, and half relaxation time. Maximal voluntary contraction was also collected immediately following the last eccentric contraction of each set of contractions, with the post-fifth set MVC representing the immediately postexercise MVC.
Subjects
Forty-six young (age, 18-29 years) men and women (22 men and 24 women) completed the study. Subject characteristics are included in Table 1 . On average, the men were slightly older (21.5 years versus 19.7 years, respectively; p < 0.05) and significantly taller and heavier than the women (p < 0.05). However, body mass index was not significantly different between the men and women (24.1 versus 23.3, respectively; p = 0.6).
Table 1: Subject characteristics.
On their first visit to the laboratory, the subjects signed an informed consent document approved by the University of Massachusetts Institutional Review Board. Exclusion criteria were resistance training with the upper extremities in the past 6 months; history of a musculoskeletal injury to the nondominant shoulder, elbow, or wrist; a job requiring upper-body lifting or recreational pursuits involving repetitive arm motions, such as volleyball or ultimate Frisbee; and caloric restriction or current use of muscle-building dietary supplements. All subjects were right hand-dominant, and all testing was done with the nondominant (i.e., left) arm.
This cohort was also used to test a separate research question regarding the contributions of peripheral and central activation on prolonged muscle dysfunction following eccentric exercise (14
Procedures
Eccentric Exercise
Measures during exercise were collected on an isokinetic dynamometer (Biodex System 3; Biodex Medical Systems, Inc., Shirley, NY). The lower body was seated in an upright position and secured with shoulder and waist straps. The elbow was secured to the dynamometer with a wide Velcro strap, and the wrist was strapped into a modified lever arm support so that the wrist flexors were not recruited to produce force during testing. During exercise, the lever arm was customized to travel through each subject's designated elbow range of motion. Subjects were verbally encouraged throughout testing and were also given continuous visual feedback of torque on the Biodex monitor.
This exercise protocol was adapted from the authors' previous work (21,22,25-29 work done) was the maximal effort of each subject to resist the forced lengthening of the dynamometer arm. The contraction speed was 60°·s−1 over the subject's range of motion. A single 3-second MVC contraction at a 90° elbow angle was done immediately after the last eccentric contraction in each set. During exercise, torque values were continuously collected at 100 Hz and downloaded for further analysis.
Isometric Strength Testing
Maximal voluntary contraction was assessed at 90° of elbow flexion and 80° of shoulder flexion on an isokinetic dynamometer (Biodex System 3). Subject positioning was described in the previous section.
Three days of baseline elbow flexion MVC strength were collected and averaged, with 48 hours between tests (visits 1-3). During baseline testing, each subject performed 5 3-second contractions, with 1 minute of rest between contractions. During exercise, a single 3-second MVC contraction was collected immediately following the final eccentric contraction of each set and was used to track isometric fatigue during exercise.
Data were sampled at 100 Hz, and a 60-point moving average was used to smooth the data for analyses. Maximal voluntary contraction was defined as the postsmoothing maximal value for each single trial (i.e., during exercise) and the average of the maximal values across the highest 3 of the 5 trials for the baseline assessment.
Assessment of Eccentric Strength and Contractile Properties
Eccentric strength capacity and other parameters of muscle function were calculated from the isokinetic dynamometer torque output of the dynamometer. Raw data containing the torque-time series were exported from the Biodex to a text file. All subsequent calculations were done by using MATLAB software, version 6.0 (The Mathworks, Inc., Natick, MA).
The outcome measures calculated from MATLAB were MET, contraction time, work , peak rate of force development, and half relaxation time. All data were first smoothed with a 60-point (i.e., 60 ms) moving average to minimize signal noise. Maximal eccentric torque was calculated as the peak eccentric torque for each contraction. Contraction time was calculated as the length of time from the onset of the contraction (i.e., elevation of torque above the stable baseline) to the completion of the contraction (i.e., when the torque returned to baseline). Work was calculated as the total area under the torque-time curve between the onset and completion of each contraction. Peak rate of force development was the maximal slope during torque generation calculated from the first derivative of the torque-time curve. Half relaxation time was the length of the time series between the peak torque and the time at which the torque equaled 50% of the MET. One experienced investigator performed all of the calculations on 2 independent occasions. If the second measure was not within 5% of the first measure, a third measure was completed. The average values from the 2 analysis trials, or the closest 2 of 3 trials, for each parameter were used in the final data analyses.
Statistical Analyses
During the study design, sample size was computed by assuming a power (1 - β) of 0.80 and α of 0.05. A sample size of 20 subjects per group was calculated based on effect size and variance estimates available from relevant literature concerning sex and muscle fatigue (23,28
Reliability of baseline MVC was assessed by using an intraclass correlation coefficient for baseline measures and a single factor analysis of variance (ANOVA) (time) to ensure that there were no significant differences between days.
Absolute changes in MVC, MET, and contractile properties during exercise were assessed by using a 2-way analysis of covariance (ANCOVA) (sex Ă— time) with repeated factors over time and initial values as the covariate to account for baseline differences between men and women. Relative changes in MVC, MET, and contractile properties during exercise were assessed by using a 2-way ANOVA (sex Ă— time) with repeated factors over time. Examination of the main effects over time allowed for the identification of variable changes due to eccentric exercise alone. The interaction term between sex and time allowed for the determination of whether variables changed differently in men and women.
For all within-exercise analyses, the information from all 50 contractions was distilled to 6 time points, or sets. The 0 set was calculated as the average of the first 3 contractions in the first set. Each successive set measure was calculated as the average of the last 2 contractions within each set. Doing so eliminated the between-set recovery of muscle function parameters from the interaction term in these analyses.
Results
Baseline Measures
Maximal voluntary contraction was collected over 3 baseline days. The intraclass correlation between baseline days was R = 0.98. There were no significant differences over baseline days for MVC (p > 0.05). Thus, the reliability of the measure was judged to be very good.
Maximal Eccentric Torque
Absolute MET and relative torque loss over all 50 contractions are depicted in Figure 1A, B , respectively. An ANCOVA of absolute MET detected a significant main effect for sex and time (p < 0.001) and a significant interaction effect (p < 0.001). An ANOVA of relative MET detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.59) or interaction effect (p = 0.55) (Figure 1C ). Men lost 34% of MET during exercise, while women lost 39%. For MET, the equation y−1 = a + b/x2 (y = MET and x = time) best described the relative fatigue curves for both sexes.
Figure 1: (A) Absolute maximal eccentric torque during exercise. (B) Eccentric torque relative to maximal eccentric torque during exercise. (C) Average eccentric torque over the last 2 contractions of each set relative to baseline. Values are mean ± SEM . Eccentric strength values in the entire cohort decreased over time, but there were no significant differences between groups (p = 0.55).
Maximal Isometric Force
An ANCOVA of absolute maximal isometric force detected a significant main effect for sex and time (p < 0.001) but no significant interaction effect (p = 0.12). An ANOVA of relative maximal isometric force detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.60) or interaction effect (p = 0.10) (Figure 2 ). Men lost 32% of MVC during exercise, while women lost 39%. For MVC, the equation y = a + bx0.5 (y = MVC and x = time) best described the relative fatigue curves for both sexes.
Figure 2: Average isometric torque over the last 2 contractions of each set relative to baseline. Values are mean ± SEM . Isometric strength values in the entire cohort decreased over time, but there were no significant differences between groups (p = 0.10).
Contraction Time
An ANCOVA of absolute contraction time detected a significant main effect for sex (p < 0.05) and time (p < 0.001) but no significant interaction effect (p = 0.08). An ANOVA of relative contraction time detected a significant main effect for time (p < 0.005) but no significant main effect for sex (p = 0.24) or interaction effect (p = 0.06) (data not shown). Men lost 10% of contraction time during exercise, while women lost 4%.
Work An ANCOVA of absolute work detected significant main effects for sex and time (p < 0.001) and a significant interaction effect (p < 0.001). An ANOVA of relative work detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.39) or interaction effect (p = 0.07) (Figure 3 ). Men lost 41% of work during exercise, while women lost 43%. For work , the equation y = a + bx0.5 (y = work and x = time) best described the change curves for work in both sexes.
Figure 3: Average work done over the last 2 contractions of each set relative to baseline. Values are mean ± SEM . Work values in the entire cohort decreased over time, but there were no significant differences between groups (p = 0.07).
Maximal Rate of Torque Development
An ANCOVA of absolute maximal rate of torque development detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.07) or interaction effect (p = 0.65). An ANOVA of relative maximal rate of torque development detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.96) or interaction effect (p = 0.85) (Figure 4 ). Men lost 13% of relative maximal rate of torque development during exercise, while women lost 11%.
Figure 4: Average maximal rate of torque development over the last 2 contractions of each set relative to baseline. Values are mean ± SEM . Rate of torque development values in the entire cohort decreased over time, but there were no significant differences between groups (p = 0.85).
Half Relaxation Time
An ANCOVA of absolute half relaxation time detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.37) or interaction effect (p = 0.88). An ANOVA of relative half relaxation time detected a significant main effect for time (p < 0.001) but no significant main effect for sex (p = 0.94) or interaction effect (p = 0.91) (data not shown). Men lost 22% of half relaxation time during exercise, while women lost 21%.
Discussion
Several studies have shown less fatigability in women than in men in response to isometric exercise (2,9,16,18,20,24,32 2,18
With resistance training, concentric and eccentric muscle actions are typically balanced during controlled isotonic dynamic exercise. However, resistance training techniques, such as negatives, can also be used to accentuate the eccentric phase. Hill (13 5,6,12
The average untrained man demonstrates higher absolute eccentric torques than the average untrained woman at baseline (24 p < 0.001). However, the patterns of relative torque losses were remarkably similar between men and women (Figure 1B, C ) (p = 0.55) and demonstrated that women are not less fatigable than men over the course of intense eccentric exercise. Therefore, size and strength gains should not be compromised and risk of injury should not be greater in 1 sex versus the other.
The few studies that have reported strength losses immediately following maximal eccentric exercise had measured maximal isometric force capacity of the muscle. Both Rinard et al. (22 28
Muscle function during a task can be described by several variables, with the ability to generate peak force or torque being the most commonly used in research. Another useful variable is the quantification of the ability to produce force over time, also known as muscular work . The current study demonstrated that men and women experience similar losses in the ability to produce work over the course of the exercise bout. At the conclusion of the exercise, men and women were remarkably similar in work generation capacity, with only a 2% difference between groups (i.e., 41% loss in men versus 43% loss in women).
Similar changes were detected in other muscle contractile properties, such as total contraction time, maximal rate of torque development, and half relaxation time. That contraction time decreased similarly for both groups indicated an inability to voluntarily maintain torque generation over the entire range of motion for the exercise. Rates of torque development and relaxation also changed over time similarly in men and women. These rates, as measured in voluntary contractions, give gross indications of the ability of the muscle to achieve muscular power (i.e., work per angular distance) and to relax after contraction. The largest change in torque development rate occurred during the first set of exercise (i.e., an approximate 20% drop) and then maintained its level throughout the rest of the exercise bout. Half relaxation time slowly declined progressively during each set of the exercise bout. Patterns for each variable were similar between men and women over the 50 contractions of the exercise.
In summary, data from the current study indicate that men and women have similar relative capacities for muscle function over the course of a single bout of novel eccentric exercise. Men demonstrated higher strength levels at baseline. However, when variables were analyzed with regard to relative changes over time, no differences between men and women were found. The results of this study clearly demonstrated that there are no sex differences in muscle fatigue or changes in other muscle function parameters during eccentric exercise in untrained men and women. Further study will be needed to determine if prolonged exercise training provokes any sex differences in eccentric fatigability.
Practical Applications
Increasing numbers of women are participating in resistance training activities with the desire to increase muscle performance for competitive events that set the bar higher each year for performance requirements for women. To meet these demands, women are incorporating a greater volume of eccentric (i.e., muscle lengthening) actions into their strength training programs due to the greater strength and size gains associated with eccentric versus concentric training. Excessive muscle fatigue during eccentric contractions would limit the ability to train optimally and can increase the risk of injury. While other studies have indicated that men and women develop fatigue at different rates during isometric exercise, little is known about the baseline abilities of men and women to perform intense eccentric exercise, which is both a potent stimulator for size and strength gains and known to produce exercise-induced muscle damage. The current study tested for basic muscle functional differences between untrained men and women during eccentric exercise and found that women can perform similarly to men relative to baseline measures, while men always demonstrate higher absolute strength. Thus, there is no reason to suspect that women may be more vulnerable to fatigue-related injury during intense eccentric exercise.
Acknowledgments
This study was partially funded by a National Strength and Conditioning Association Student Research Grant (M.J. Hubal). The authors would also like to acknowledge the help of Stephanie Dallaire, Katherine Eck, and Ian Lanza in data collection and MATLAB programming.
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