Fatigue Resistance: An Intriguing Difference in Gender

Muscle fatigue is a multifaceted phenomenon resulting from a combination of impairments throughout the human neuromuscular system (Hicks, Kent-Braun & Ditor 2001; Russ et al. 2008). The definition of muscle fatigue has been modified throughout the years as research has brought forth more understanding of the components contributing to fatigue.

Traditionally, muscle fatigue has been defined as the muscle’s inability to maintain an expected force (Barry & Enoka 2007). In the past decade, Barry and Enoka have written that it corresponds to an exercise-induced decline in the capability of the muscle to generate force or power, regardless of whether or not the task can be continued. According to this description, muscle fatigue slowly starts after the onset of sustained activity, even though an individual can continue performing a muscular task.

Numerous studies have shown that women have a greater resistance to fatigue than men; therefore, women are able to sustain continuous and intermittent muscle contractions at low to moderate intensities longer than men (Clark et al. 2003; Fulco et al. 2001; Hunter & Enoka 2001; Hunter et al. 2004; Russ et al. 2008; Russ & Kent-Braun 2003; Thompson et al. 2007; Wust et al. 2008; Yoon et al. 2007). This trend has been observed in a variety of muscles using assorted training protocols; however, the physiological mechanisms for the differences between males and females are not completely understood. Differences in muscle mass, exercise intensity, utilization of foodstuffs during metabolism (reactions that produce ATP) and neuromuscular activation have all been suggested as contributing factors for the fatigue differences between the sexes (Russ et al. 2008; Hicks, Kent-Braun & Ditor 2001; Russ & Kent-Braun 2003; Wust et al. 2008; Thompson et al. 2007; Yoon et al. 2007).

Muscle Mass and Exercise Intensity

Generally, men can generate a higher absolute muscle force when performing the same relative (percent of maximal voluntary contraction) workload as women during a muscle contraction (Hicks, Kent-Braun & Ditor 2001). Several researchers have suggested that this higher absolute muscle force during the same relative workload causes intramuscular pressures, compressing the blood vessels that feed the muscles and slightly inhibiting oxygen supply to the working muscles (Russ & Kent-Braun 2003; Thompson et al. 2007; Yoon et al. 2007). To delay fatigue in working muscles, oxygen is necessary during sustained contractions to allow for the continuation of oxidative phosphorylation (aerobic metabolism). The constriction of blood vessels also delays the removal of metabolic byproducts (carbon dioxide, hydrogen ions, lactate) from the muscle, thus contributing to fatigability.

Researchers have shown that women are capable of longer endurance times than men when performing low- to moderate-intensity isometric contractions in several muscle groups, including the adductor pollicis, elbow flexors, extrinsic finger flexors and knee extensors (Hunter & Enoka 2001). As the intensity of the contraction increases above moderate levels, the difference in gender fatigability is less observable. Thus the intensity of the exercise is a major discerning factor in the fatigue resistance differences seen between females and males.

Other researchers have also shown differences in the time to fatigue between men and women when they are matched for maximal voluntary contraction of the target muscle site. When testing the elbow flexor muscles, Hunter et al. (2004) showed that women had a greater time to task failure during intermittent submaximal muscle contractions than their strength-matched male counterparts. These findings are consistent with Fulco et al. (1999) for intermittent contractions of the adductor pollicis muscle performed by strength-matched males and females. These authors showed that women had a longer time to task failure at 50% of maximal voluntary contraction of the adductor pollicis muscle. Note that the differences in time to fatigue between men and women are most apparent in submaximal (not maximal) contractions.

Mean Arterial Blood Pressure and Blood Flow

Some investigations have studied the blood flow to the working muscles and the mean arterial pressure (MAP). MAP is the average blood pressure during a cardiac cycle and is estimated by the following equation: diastolic pressure + ⅓ (systolic pressure – diastolic pressure). Yoon et al. (2007) found that women had lower MAP than men during submaximal contractions of the forearm muscles but not at 80% of voluntary maximal contraction. Other researchers have also found that females had lower MAP than men, even when subjects were matched for absolute strength of the target muscles (Hunter & Enoka 2001; Thompson et al. 2007; Hunter et al. 2004).

There are several possible explanations for the differences in MAP responses between males and females:

  1. less muscle mass involvement in females than males (at same relative workload)
  2. lower absolute muscle contraction differences, resulting in less blood flow constriction, in females
  3. gender differences in motor unit activation of the nervous system
  4. gender differences in utilization of substrates (foodstuffs such as carbohydrates and fats)
  5. lower production of metabolite byproducts (i.e., hydrogen ions, carbon dioxide and lactate) in females (Hunter & Enoka 2001; Hicks, Kent-Braun & Ditor 2001; Hunter et al. 2004)

Some studies have tried to control for blood flow constriction to the working muscles by placing the muscles in ischemic conditions (where blood vessels are constricted). Russ and Kent-Braun (2003) studied men and women performing intermittent submaximal muscle contractions of the dorsiflexor muscles of the ankle during both free-flow and ischemic conditions. They found that women had less fatigue than men during the free-flow condition, but the difference was eliminated during the ischemic condition. Similarly, Wust et al. (2008) tested the quadriceps muscles for fatigue differences between males and females under normal-blood-flow and ischemic-blood-flow conditions. To achieve ischemia, a pneumatic (compressed-air) thigh cuff was placed around the upper thigh and inflated to 240 millimeters of mercury to impede blood supply to the leg before and during the fatigue tests. For both the normal-blood-flow condition and the ischemic condition, women showed less fatigability than men during quadriceps contraction.

Neuromuscular Activation

Some investigators have looked at electromyography (EMG) during muscle contraction to assess the patterns of muscle contraction and recruitment (Clark et al. 2003; Hunter & Enoka 2001; Hunter et al. 2004; Thompson et al. 2007; Yoon et al. 2007). During sustained muscle contraction, the neuromuscular system strives to maintain force production by recruiting additional nonfatigued motor units, recruiting larger motor units and increasing the firing rate of activated motor units (Thompson et al. 2007; Yoon et al. 2007). An EMG is able to detect muscle contraction and recruitment by the electrical impulses sent through the body for muscle contraction. Differences in the activation of recruitment patterns within a target muscle and its agonists affect the fatigue rate of that muscle group.

Some investigators have observed gender differences in the way muscles are used and in their recruitment patterns, whereas other researchers have found no differences between the sexes. During higher-intensity exercise (≥ 80% maximal voluntary contraction), there is usually no difference between the sexes in either muscle activation or the recruitment of muscles (Yoon et al. 2007). More gender comparison studies are needed to elucidate this area of the neuromuscular-activation and fatigue debate.

Practical Considerations

Some fascinating physiological and metabolic fatigability characteristics exist in the submaximal muscle-force-producing capacity of women, which are illustrated in Figure 1. It should be noted that the fatigue differences between men and women are more apparent with fit females, as “low-fit” individuals (males and females) tend to fatigue rather rapidly owing to the untrained state of their musculature. However, as many personal trainers and fitness professionals have observed in their professional experience, these physiological phenomena help to explain scientifically why moderately to highly trained females are very capable of doing advanced multiple-set and multiple-exercise program designs as well as completing frequent resistance training workouts on a weekly basis.

SIDEBAR: Figure 1. Contributing Mechanisms of Fatigue Resistance Characteristics in Females

SIDEBAR: Substrate Utilization and Estrogen

Differences in metabolism exist between males and females. Several studies have shown that males have greater glycolytic (carbohydrate) capacity and rely more on glycolytic pathways, whereas females rely more on oxidative phosphorylation (fat and carbohydrate) during sustained cardiovascular exercise (Braun & Horton 2001; Tarnopolsky et al. 1990). During continuous aerobic exercise, women have been found to have a lower respiratory exchange ratio (a laboratory measurement used during aerobic exercise to determine foodstuffs being used for fuel), indicating that women rely more on fat for fuel during this submaximal exercise (Braun & Horton 2001; Tarnopolsky et al. 1990). Muscle biopsy research shows that the common glycolytic enzymes (phosphofructokinase, pyruvate kinase and lactate dehydrogenase) that break down carbohydrate are less active in women, possibly decreasing their potential for glycolytic-pathway energy production (Tarnopolsky 2008). Thus, it is proposed that females will make greater use of the longer-lasting fat metabolism pathway during cardiovascular exercise.

Estrogen has been shown to influence the utilization of different fuels (i.e.,fats, proteins and carbohydrates), especially during long endurance exercise (Tarnopolsky 2008). Females typically rely less on carbohydrate and muscle glycogen stores and more on fat oxidation during endurance exercise, even with carbohydrate-loading diets. This finding has led researchers to believe that estrogen has glycogen-sparing characteristics (Braun & Horton 2001; Tarnopolsky 2008; Tarnopolsky et al. 1990).

Brenda Critchfield, ATC, LAT, CSCS, is completing her master’s degree in exercise science at the University of New Mexico in Albu­querque (UNMA). She is a teaching assistant in the UNM athletic training education program, in charge of women’s volleyball, swimming and diving.

Len Kravitz, PhD, is the program coordinator of exercise science and a researcher at UNMA, where he recently won the Outstanding Teacher of the Year Award. In 2006 he was honored as the Can-Fit-Pro International Presenter of the Year and as the ACE Fitness Educator of the Year.

References

Barry, B.K., & Enoka, R.M. 2007. The neurobiology of muscle fatigue: 15 years later. Integrative and Comparative Biology (June 6), 1–9.

Braun, B., & Horton, T. 2001. Endocrine regulation of exercise substrate utilization in women compared to men. Exercise and Sport Sciences Reviews, 29 (4), 149–54.

Clark, B.C., et al. 2003. Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. Journal of Applied Physiology, 94, 2263–72.

Fulco, C.S., et al.1999. Slower fatigue and faster recovery of the adductor pollicis muscle in women matched for strength with men. Acta Physiologica Scandinavica, 167 (3), 233–39.

Fulco, C.S., et al. 2001. Gender alters impact of hypobaric hypoxia on adductor pollicis muscle performance. Journal of Applied Physiology, 91, 100–108.

Hicks, A.L, Kent-Braun, J. & Ditor, D.S. 2001. Sex differences in human skeletal muscle fatigue. Exercise and Sport Sciences Reviews, 29 (3), 109–12.

Hunter, S.K., & Enoka, R.M. 2001. Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. Journal of Applied Physiology, 91, 2686–94.

Hunter, S.K., et al. 2004. Men are more fatigable than strength-matched women when performing intermittent submaximal contractions. Journal of Applied Physiology, 96, 2125–32.

Kent-Braun, J.A., et al. 2002. Human skeletal muscle responses vary with age and gender during fatigue due to incremental exercise. Journal of Applied Physiology, 93, 1813–23.

Russ, D.W., & Kent-Braun, J.A. 2003. Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. Journal of Applied Physiology, 94, 2414–22.

Russ, D.W., et al. 2008. Contrasting influences of age and sex on muscle fatigue. Medicine & Science in Sports & Exercise, 40 (2), 234–41.

Tarnopolsky, L.J., et al. 1990. Gender differences in substrate for endurance exercise. Journal of Applied Physiology, 68 (1), 302–308.

Tarnopolsky, M.A. 2008. Sex differences in exercise metabolism and the role of 17-beta estradiol. Medicine & Science in Sports & Exercise, 40 (4), 648–54.

Thompson, B.C., et al. 2007. Forearm blood flow responses to fatiguing isometric contractions in women and men. American Journal of Physiology—Heart and Circulatory Physiology 293, H805–12.

Wust, R.C.I., et al. 2008. Sex differences in contractile properties and fatigue resistance of human skeletal muscle. Experimental Physiology. In press. First published online Feb. 22, 2008; http://ep.physoc.org/cgi/content/abstract/expphysiol.207.041764v1.

Yoon, T., et al. 2007. Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle & Nerve, 36, 515–24.

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