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. 2014 Apr;210(4):768-89.
doi: 10.1111/apha.12234. Epub 2014 Feb 25.

Sex Differences in Human Fatigability: Mechanisms and Insight to Physiological Responses

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Free PMC article

Sex Differences in Human Fatigability: Mechanisms and Insight to Physiological Responses

S K Hunter. Acta Physiol (Oxf). .
Free PMC article

Abstract

Sex-related differences in physiology and anatomy are responsible for profound differences in neuromuscular performance and fatigability between men and women. Women are usually less fatigable than men for similar intensity isometric fatiguing contractions. This sex difference in fatigability, however, is task specific because different neuromuscular sites will be stressed when the requirements of the task are altered, and the stress on these sites can differ for men and women. Task variables that can alter the sex difference in fatigability include the type, intensity and speed of contraction, the muscle group assessed and the environmental conditions. Physiological mechanisms that are responsible for sex-based differences in fatigability may include activation of the motor neurone pool from cortical and subcortical regions, synaptic inputs to the motor neurone pool via activation of metabolically sensitive small afferent fibres in the muscle, muscle perfusion and skeletal muscle metabolism and fibre type properties. Non-physiological factors such as the sex bias of studying more males than females in human and animal experiments can also mask a true understanding of the magnitude and mechanisms of sex-based differences in physiology and fatigability. Despite recent developments, there is a tremendous lack of understanding of sex differences in neuromuscular function and fatigability, the prevailing mechanisms and the functional consequences. This review emphasizes the need to understand sex-based differences in fatigability to shed light on the benefits and limitations that fatigability can exert for men and women during daily tasks, exercise performance, training and rehabilitation in both health and disease.

Keywords: central fatigue; fibre types; gender; metabolism; peripheral fatigue; women.

Conflict of interest statement

Conflict of Interest

I have no conflict of interest.

Figures

Figure 1
Figure 1. Sex differences in muscle fatigue for voluntary isometric contractions (A) and dynamic contractions (B)
Represented are mean data from 59 studies: 43 isometric contraction studies (A) and 16 dynamic contraction studies (B) that assessed muscle fatigue in men and women for various muscle groups. Plotted in both panels is the difference between the mean fatigue index or time to task failure of the men and women (as a percent of the women’s value) within a study as a function of the contraction intensity of the fatigue task. In both panels, upper limb muscles are in closed symbols and lower limb muscles represented in open symbols. Back and neck muscles are represented as grey symbols. A. Sex differences in muscle fatigue for sustained and intermittent isometric fatiguing contractions are plotted. Most data points are above the line indicating women are more fatigue resistant than men for most 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 are included (r2 = 0.20). B. Sex differences in muscle fatigue for shortening (S) and lengthening (L, triangle-up symbols) fatiguing contractions are plotted. There was no relation between contraction intensity and the sex difference for dynamic contractions, although data from two studies for the elbow flexor muscles (between 50–90% max), however, showed a significant negative relation (r2 = 0.97) for shortening contractions. There are more data points than number of stated studies because some studies involved multiple contraction types or intensities.
Figure 2
Figure 2
Summary of findings from 4 studies showing the influence of increased arousal on time to task failure of a fatiguing isometric contraction (20% MVC until failure) with the elbow flexor muscles in young men and women. In each study, two sessions were performed. A fatiguing contraction with no imposed stressor (control) and an experimental session where one of the following were imposed during the contraction: a difficult mental math task (counting backward by 13, cognitive stressor), easy mental math (dual) or brief electric shocks to the back of the non-exercising hand (E. Stim). A. Shown is the maximal voluntary isometric strength performed prior to the fatiguing contraction by young men and young women. B. Shown is the relative reduction in time to task failure (between the control and stressor contraction, i.e. the Stressor, Dual or E. Stim) for each study. Women had greater reductions than men for the cognitive stressor (study 1, n = 20) (Yoon et al., 2009b); but not when matched for strength (study 2, n = 10) (Keller-Ross et al., 2014). Study 3 showed minimal changes in time to failure when the subjects performed easy mental math (Dual, n = 20)(Yoon et al., 2009b). In study 4, reductions in time to failure were observed when the arousal was induced with unpredictable brief electric shocks to the back of the hand during the contraction (E.Stim, n = 20) (Hunter and Yoon, unpublished findings). * P<0.05 between men and men, # P = 0.07 although, not included in the results, are 2 women who failed to complete the fatiguing contraction because of increased levels of anxiety.
Figure 3
Figure 3. Potential physiological mechanisms for the sex difference in muscle fatigue
(or time to task failure). The figure shows those potential mechanisms that can contribute to women being more fatigue resistant than men. The strength of a potential mechanism will vary with the task conditions so that one dominant mechanism does not fully explain the sex difference in performance of a fatiguing contraction. 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. Ultimately, the differences in fatigue between men and women can be due to differences in: 1) motor neuron activation; 2) contractile function of the activated fibres; and 3) the magnitude of metabolites accumulating that interfere with contractile function. These mechanisms are stipulated with the large arrows. Black boxes indicate processes within the muscle, white boxes are processes in the nervous system, and the grey are hormonal and sympathetic actions.
Figure 4
Figure 4
Young men (n = 9) and young women (n = 8) performed an isometric fatiguing protocol with the elbow flexor muscles. The protocol involved 6 × 22 s maximal voluntary contractions (MVC) with submaximal contractions at 60% and 80% MVC before, after and between the sustained MVCs. A. Representative torque data of a man. Arrows at the bottom of the panel show the timing of transcranial magnetic stimuli (Stim). B. MVC torque (mean ± SEM) relative to baseline control values for the men (closed circles) and women (open circles) during, and in recovery from, the fatiguing task. Relative torque is shown at the start and end of each sustained 22-s MVC, and during brief MVCs at the start and end of 10-min recovery. The men exhibited larger reductions in torque than the women during the intermittent fatiguing contractions (65% vs 52%). C. Peak relaxation rate of muscle measured from the fall in force immediately after the superimposed twitch during the MVC. Plotted are the mean (± SEM) from the 5 brief control MVCs, and then values at the start and end of each 22-s maximal contraction, and for the brief MVCs at the start and end of recovery. Peak relaxation rate became slower for both men and women as the muscle became more fatigued and then recovered during the 10-min recovery. However, the men had greater reductions in the peak relaxation rate than the women (P <0.05). Note that the y-axis is inverted. Larger negative numbers indicate faster relaxation. Adapted from (Hunter et al., 2006a).
Figure 4
Figure 4
Young men (n = 9) and young women (n = 8) performed an isometric fatiguing protocol with the elbow flexor muscles. The protocol involved 6 × 22 s maximal voluntary contractions (MVC) with submaximal contractions at 60% and 80% MVC before, after and between the sustained MVCs. A. Representative torque data of a man. Arrows at the bottom of the panel show the timing of transcranial magnetic stimuli (Stim). B. MVC torque (mean ± SEM) relative to baseline control values for the men (closed circles) and women (open circles) during, and in recovery from, the fatiguing task. Relative torque is shown at the start and end of each sustained 22-s MVC, and during brief MVCs at the start and end of 10-min recovery. The men exhibited larger reductions in torque than the women during the intermittent fatiguing contractions (65% vs 52%). C. Peak relaxation rate of muscle measured from the fall in force immediately after the superimposed twitch during the MVC. Plotted are the mean (± SEM) from the 5 brief control MVCs, and then values at the start and end of each 22-s maximal contraction, and for the brief MVCs at the start and end of recovery. Peak relaxation rate became slower for both men and women as the muscle became more fatigued and then recovered during the 10-min recovery. However, the men had greater reductions in the peak relaxation rate than the women (P <0.05). Note that the y-axis is inverted. Larger negative numbers indicate faster relaxation. Adapted from (Hunter et al., 2006a).
Figure 5
Figure 5
Type I fibre area (%, proportional area) of skeletal muscle histochemically analysed for myosin ATPase activity from muscle biopsy samples of vastus lateralis (VL), tibialis anterior (TA) and biceps brachii (BB) in young men (closed symbols) and women (open symbols) that were sampled in the same study. Shown are the mean proportional areas of the men and women in each of the 12 studies (Simoneau et al., 1985, Simoneau and Bouchard, 1989, Miller et al., 1993, Esbjornsson-Liljedahl et al., 1999, Staron et al., 2000, Carter et al., 2001b, Esbjornsson-Liljedahl et al., 2002, Porter et al., 2002, Toft et al., 2003, Roepstorff et al., 2006, Maher et al., 2009, Esbjornsson et al., 2012). The mean (± SEM) per cent area of type I fibres of all the muscles from the 12 studies is plotted on the right side. Women had greater type I fibre area (%) than men (P<0.05).
Figure 6
Figure 6
Maximal rates of sarcoplasmic reticulum Ca2+ATPase activity for whole muscle homogenates (obtained via needle biopsies of the vastus lateralis) of young men (n = 27) and women (n = 31) at rest. Men are represented in the closed symbols and women in the open symbols. Data plotted as circles, are from 4 different studies that examined men only (Booth et al., 1997, Li et al., 2002), women only (Hunter et al., 1999, Thom et al., 2001). The triangles are men and women in the same study (Harmer et al., 2014). The mean (±SEM) of the men and women from all the studies are plotted on the right side of the figure (squares) showing that men have faster maximal Ca2+ATPase activity than women.

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