The Relevance of Sex Differences in Performance Fatigability

Abstract

Performance fatigability differs between men and women for a range of fatiguing tasks. Women are usually less fatigable than men, and this is most widely described for isometric fatiguing contractions and some dynamic tasks. The sex difference in fatigability is specific to the task demands so that one mechanism is not universal, including any sex differences in skeletal muscle physiology, muscle perfusion, and voluntary activation. However, there are substantial knowledge gaps about the task dependency of the sex differences in fatigability, the involved mechanisms, and the relevance to clinical populations and with advanced age. The knowledge gaps are in part due to the significant deficits in the number of women included in performance fatigability studies despite a gradual increase in the inclusion of women for the last 20 yr. Therefore, this review 1) provides a rationale for the limited knowledge about sex differences in performance fatigability, 2) summarizes the current knowledge on sex differences in fatigability and the potential mechanisms across a range of tasks, 3) highlights emerging areas of opportunity in clinical populations, and 4) suggests strategies to close the knowledge gap and understanding the relevance of sex differences in performance fatigability. The limited understanding about sex differences in fatigability in healthy and clinical populations presents as a field ripe with opportunity for high-impact studies. Such studies will inform on the limitations of men and women during athletic endeavors, ergonomic tasks, and daily activities. Because fatigability is required for effective neuromuscular adaptation, sex differences in fatigability studies will also inform on optimal strategies for training and rehabilitation in both men and women.

Figure 1. Numbers and ratio of men and women in 200 fatigability studies (1972-2015)

A. Shown are the numbers of men and women reported in a sample of 200 studies (n = 4113 subjects total) published between 1972 and 2015 that assessed fatigability in humans. These human studies were sampled from several muscle fatigue reviews (2, 19, 53) and a literature search using an online data base (pubmed.org) to include data from more recent years. The vertical bar for each sex shows the number of men and women that were in a single sex study (black) or if both sexes were included in the study (hashed). B. Shown are the ratios of the numbers of women-to-men in the studies for those studies published in ≤2000, 2001-2009 and 2010-2015. A ratio of 1 is indicated by the dashed line and represents equal numbers of men and women. There is an increase in the number of women included in the studies relative to men, but there are still large deficits across all the years. Each vertical bar shows the proportion of the subjects represented in the vertical bar included in a study with women only (black), men only (white) or both sexes included (gray). Thus, the low ratio of women-to-men across the different years in the sample of 200 studies is largely attributed to a greater number of studies that include men only.

Figure 2. Sex differences in fatigability for voluntary isometric contractions

Represented are mean data from 46 isometric contraction studies (intermittent and sustained) published between 1975 to 2015 that assessed fatigability of men and women. Plotted is the percentage sex difference in fatigability in each study, calculated as the mean difference in fatigability between the men and the women as a percent of the women's value. The fatigability values used for the calculation was either the fatigue index or time to task failure for the sustained or intermittent isometric fatiguing contractions. The x-axis represents the contraction intensity (percentage of maximal voluntary contraction, MVC) at which the fatiguing contractions were performed. Upper limb muscles are represented in closed symbols and lower limb muscles in open symbols. Back and neck muscles are represented as grey symbols. Most data points are above the line indicating women were less fatigable than men for many of the muscle groups. There was a significant negative relation between the relative contraction intensity and the magnitude of the sex difference for the isometric contractions when all muscle groups were included (r² = 0.19). Updated and adapted (40).

Figure 3. Mechanisms for sex differences in fatigability

Shown are potential mechanisms that can contribute to women less fatigable than men during fatiguing contractions. The contribution of a potential mechanism will vary with the task conditions and demands so that one dominant mechanism is not universal to the sex difference in performance fatigability. A negative sign indicates that the physiological variable or process is less in women than men and, conversely, a positive sign indicates it is greater in women than men. Adapted from (40).

Figure 4. Type I fiber area (%, proportional area of the sample) of skeletal muscle in men and women

The cross-sections of muscle were histochemically analyzed for myosin ATPase activity from muscle biopsy samples of vastus lateralis (VL), tibialis anterior (TA), lateral gastrocnemius (LG) and biceps brachii (BB) of young men and young women who were sampled in the same study. All studies included biopsies of young adults with a mean age between 21 and 26 years for 12 of the 13 studies and 49 years (<57 years) for one study (91). The proportional area (% area of sample) shown for the men and women in each study, was calculated from the percentage number of fibers within a sample and the mean cross-sectional area of each fiber type within the sample. Thirteen studies are identified on the x axis. These studies are coded below by the muscle that was biopsied (VL, TA, LG or BB) and a number that corresponds to the citation. The numbers of men and women biopsied in each study are also included below and this varied between 8 and 215 men or women. The mean (± SEM) proportional area of type I fibers of all the muscles from the 13 studies is plotted on the right side of the figure. Women had greater type I fiber area (%) than men for the 13 studies when pooled (P<0.05). This graph was adapted and updated from data previously published (40). VL-1 (86): 37 men, 38 women (26, 25 years, respectively) VL-2 (85): 215 men, 203 women (24, 23 years) VL-3 and BB-3 (64): 8 men, 8 women (23, 25 years) VL-4 (25): 20 men, 19 women (25, 23 years) VL-5 (88): 95 men, 55 women (22, 21 years) VL-6 (12): 8 men, 8 women (22, 22 years) VL-7 (24): 7 men, 8 women (25, 23 years) VL-8 (91): 22 men, 18 women (49 years, 26-57 years) VL-9 (78): 8 men, 9 women (25, 24 years) VL-10 (60): 12 men, 12 women (21, 22 years) VL-11 (22): 9 men, 8 women (26, 25 years) TA-12 (71): 15 men, 15 women (26, 23 years) LG-13 (57): 9 men, 43 women (27, 23 years)