Article Page
Fatigue Resistance: An Intriguing Difference in Gender
Brenda Critchfield, M.S. and Len Kravitz, Ph.D.

Muscle fatigue is a multifaceted phenomenon resulting from a combination of impairments throughout the human neuromuscular system (Hicks et al. 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 is defined as the muscle's inability to maintain an expected force (Barry & Enoka 2007). In the past decade, Barry and Enoka expand that the definition of muscle fatigue in research 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 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 to produce ATP), and neuromuscular activation have all been suggested as contributing factors for the fatigue differences between the sexes (Russ et al. 2008; Hicks et al. 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) work load as women during a muscle contraction (Hicks et al. 2001). It has been suggested by several researchers that this higher absolute muscle force during the same relative work load causes intramuscular pressures compressing the blood vessels feeding the muscles; therefore, oxygen supply is slightly inhibited 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 will also delay the removal of metabolic byproducts (carbon dioxide, hydrogen ions, lactate) in the muscle, thus contributing to fatiguability. Researchers have shown that women are capable of longer endurance times compared to men when performing low to moderate intensity isometric contractions in several muscles 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 intensities the difference in gender fatiguability is less observable. Thus the intensity of the exercise is a major discerning factor to the fatigue resistance differences seen between females and males.
In addition, other researchers have 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% maximal voluntary contraction of the adductor pollicis muscle (Fulco et al., 1999). Note that the time to fatigue differences 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 blood pressure (MAP). MAP is the average blood pressure during a cardiac cycle and is estimated by the following equation: diastolic pressure + 1/3(systolic pressure - diastolic pressure. Yoon et al. 2007 looked at the MAP during submaximal contractions of the forearm muscles and found women had lower arterial pressure than men during intermittent submaximal contractions, but not at 80% of voluntary maximal contraction. Other researchers have also found females had a lower MAP than men, even when the subjects were matched for absolute strength of the target muscles (Hunter & Enoka 2001; Thompson et al. 2007; Hunter et al., 2004). Possible explanations for the differences in the MAP responses between males and females are, 1) less muscle mass involvement in females (at same relative work load), 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, 3) different utilization of substrates (foodstuffs such as carbohydrates and fats), and 4) lower metabolite byproduct production (i.e., hydrogen ions, carbon dioxide, and lactate) between men and women (Hunter & Enoka 2001; Hicks et al. 2001; Hunter et al. 2004).

Some studies have tried to control for the blood flow constriction to the working muscles by placing the muscles in ischemic (constriction of blood vessels) conditions. 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 blood conditions 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 (Russ and Kent-Braun, 2003). 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 mmHg 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 fatiguability than men during quadriceps contraction.

Substrate Utilization and Estrogen
Differences between males and females exist in metabolism. Several studies show that males have greater glycolytic (carbohydrate) capacity and rely more on glycolytic pathways, while females rely more on oxidative phosphorylation (fat and carbohydrate) during sustained cardiovascular exercise (Braun & Horton 2001; Tarnopolsky et al. 1990). Women have been shown to have a lower respiratory exchange ratio (a laboratory measurement during aerobic exercise to determine foodstuffs being used for fuel) during continuous aerobic exercise, 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 women have lower activities of the common glycolytic enzymes (phosphofructokinase, pyruvate kinase, and lactate dehydrogenase) that break down carbohydrate, possibly decreasing their potential of glycolytic pathway production of energy (Tarnopolsky 2008). Thus, it is proposed that females will have greater utilization 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, carbohydrates), especially during long endurance exercise (Tarnopolsky 2008). It has been shown that 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).

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 increasing the recruitment of additional non-fatigued motor units, recruiting larger motor units, and increasing the firing rate of activated motor units (Thompson et al. 2007; Yoon et al. 2007). Electromyography 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 will affect the fatigue rate of that muscle group. Some investigators have found a difference in the way muscles were utilized, and that the recruitment patterns are different in men than in women; whereas others have found no difference between the sexes. However, during higher intensity exercise (&Mac179; 80% maximal voluntary contraction) there is usually no difference between the sexes in the muscle activation or the recruitment of muscles (Yoon et al. 2007). This area of neuromuscular activation and fatigue factors needs to be elucidated with more gender comparison studies.

Practical Observations to the Personal Trainer and Fitness Professional
Some fascinating physiological and metabolic fatiguability characteristics exist in the submaximal muscle force producing capacity of women. 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 due to the untrained state of their musculature. However, as many personal trainers and fitness professionals have observed in their professional experience, these physiological phenomenon help to scientifically explain why moderately to highly trained females are very capable of doing more advanced multiple-set and multiple-exercise program designs, as well as completing more frequent resistance training workouts during the week.

Brenda Critchfield, ATC, LAT, CSCS completed 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, Ph.D., is the Program Coordinator of Exercise Science and Researcher at the University of New Mexico where he recently won the "Outstanding Teacher of the Year" award. Len was honored with the 1999 Canadian Fitness Professional “International Presenter of the Year” and the 2006 Canadian Fitness Professional “Specialty Presenter of the Year” awards and chosen as the American Council on Exercise 2006 "Fitness Educator of the Year”.

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

Braun, B & Horton, T (2001). Endocrine regulation of exercise substrate utilization in women compared to men. Exercise and Sport Sciences Reviews, 29(4), 149-154.

Clark, B.C., Manini, T.M., The, D.J., Doldo, N.A., & Ploutz-Snyder, L.L. (2003). Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. Journal of Applied Physiology, 94, 2263-2272.

Fulco, C.S., Rock, P.B., Muza, S.R., Lammi, E., Braun, B., Cymerman, A., Moore, L.G., & Lewis, S.F. (2001). Gender alters impact of hypobaric hypoxia on adductor pollicis muscle performance. Journal of Applied Physiology, 91, 100-08.

Fulco, C.S., Rock, P.B., Muza, S.R., Lammi, E., Cymerman, A., Butterfield, G., Moore, L.G., Braun, B., & Lewis, S.F. (1999). Slower fatigue and faster recovery of the adductor pollicis muscle in women matched for strength with men. Acta Physiologica Scandanavica 167:233-239.

Hicks, A.L, Kent-Braun, J., & Ditor, D.S. (2001). Sex differences in human skeletal muscle fatigue. Exercise and Sports 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: 2686-2694.

Hunter, S.K., Critchlow, A., Shin, I.S., & Enoka, R.M (2004). Men are more fatigable than strength-matched women when performing intermittent submaximal contractions. Journal of Applied Physiology, 96, 2125-2132.

Kent-Braun, J.A., Ng, A.V., Doyle, J.W., & Towse, T.F. (2002). Human skeletal muscle responses vary with age and gender during fatigue due to incremental exercise. Journal of Applied Physiology, 93,1813-1823.

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, 2414-2422.

Russ, D.W., Towse, T.F., Wigmore, D.M., Lanza, I.R., Kent-Braun, J.A. (2008). Contrasting influences of age and sex on muscle fatigue. Medicine & Science in Sports & Exercise 40 (2), 234-41.

Tarnopolsky, L.J, MacDougall, S.A., Atkinson, M.A., Tarnopolsky, M.A., & Sutton, J.R. (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), 648-654.

Thompson, B.C., Fadia, T., Pincivero, D.M., & Scheuermann, B.W. (2007). Forearm blood flow responses to fatiguing isometric contractions in women and men. American Journal of Physiology: Heart and Circulatory Physiology 293:H805-H812.

Wust, R.C.I., Morse, C.I., de Haan, A., Jones, D.A., & Degens, H. (2008). Sex differences contractile properties and fatigue resistance of human skeletal muscle. Experimental Physiology, February 22, 2008.

Yoon, T., Delap, B.S., Griffith, E.E., & Hunter, S.K. (2007). Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women, Muscle & Nerve, 36, 515-524.