Aging is characterized by sarcopenia, decreased number of muscle fibers, and selective type II fiber atrophy (19). These morphologic transformations are accompanied by functional changes such as decreased muscle strength and contraction speed, which may lead to a reduction in gait speed, poor balance, and a reduced ability to perform activities of daily living (ADL) (16,24,29).
However, the effects of aging on muscle fatigue are discrepant. It has been reported that older individuals fatigue more (2,4,5,18,21,22,25), less (3,6,10,14), or similarly to young individuals (1,12,17,20). Potentially, the effects of aging on muscle fatigue are unclear because of differences in muscle groups studied, voluntary vs. electrically evoked contractions, continuous vs. intermittent contractions, exercise duration, duty cycle, and contraction speed. Schwendner and colleagues (27) reported that nonfallers have greater muscle endurance (maximal knee extensions until force output <50% of maximal voluntary contraction [MVC] for two consecutive repetitions) than fallers (95 vs. 81 sec). Thus, muscle fatigability may be an important determinant of physical function.
Physiologically, there is evidence to support the theory that older muscle is less fatigable than younger muscle. With aging, there is an increased reliance on oxidative phosphorylation and a decreased reliance on glycolysis (13). In addition, lactate dehydrogenase is reduced in older muscle (17). Lanza et al. (14) reported that intermittent contractions may favor replenishment of oxygen, and, because phosphocreatine resynthesis is an aerobic process, it could be hypothesized that older individuals would have enhanced fatigue resistance during repeated bouts of intense contractions. In fact, the enhanced fatigue resistance of older muscle may be most easily detectable during repeated contractions.
Although a great deal of research on age-associated differences in muscle fatigue is available, much of it is difficult to compare because of differences in methodology. To broaden our knowledge of the effects of aging on muscle fatigue during repeated contractions, without adding confusion to the literature, studies were separated that examined different muscle groups (e.g., knee extensors vs. adductor pollicis), used dissimilar exercise modalities (isokinetic vs. isometric), and used divergent types of contractions (voluntary vs. evoked). Several groups were identified that examined the effects of age on dynamic contractions of the knee extensors using isokinetic exercise (1,12,17,20), but none had examined muscle fatigue during repeated sets. Aniansson et al. (1) reported no difference in fatigability between young and old adults performing 30 repetitions at 180° sec−1. LaForest and colleagues (12) and Larsson and Karlsson (17) reported no difference in fatigability between young and old individuals after 50 repetitions at 180° sec-1. Finally, Lindstrom et al. (20) reported no difference in fatigability between old and young men and women after 100 repetitions at 90° sec-1. To extend the work of these previous studies and allow for more definitive conclusions regarding age-associated differences in muscle fatigue, the purpose of this investigation was to compare muscular fatigue induced by multiple sets of intermittent isokinetic mode knee extensions in older and younger males. The hypothesis of this investigation was that older muscle would be more resistant to fatigue than younger muscle.
Experimental Approach to the Problem
Participants were instructed to report to the laboratory having abstained from physical activity for at least 24 hours and having fasted from the previous night to control for the acute effects of exercise or food on muscle glycogen. Height and body mass were assessed during visit one. To establish a reliable measure, volunteers performed the muscle fatigue test on two occasions separated by approximately 7 days. Exercise tests were conducted within 1 hour of the previous appointment time to minimize diurnal variations. Because of potential sex differences in muscle fatigue (reviewed in (7)), only males were recruited for this study.
Nineteen older (mean ± SD) (66 ± 6 yr; range 60-82 yr) and 16 younger (21 ± 2 yr; range 18-26 yr) males were recruited from the local community. Before the study, all volunteers read and completed a physical activity readiness questionnaire (PAR-Q), and an informed consent document was approved by the institutional review board. No participants had orthopedic conditions that could influence performance on the fatigue test. In addition, the older men received physician clearance to participate. Older and younger participants were similar in terms of height (old vs. young: 178.2 ± 8.1 vs. 175.9 ± 6.9 cm; p = 0.38), body mass (85.6 ± 11.6 vs. 79.2 ± 7.9 kg; p = 0.07), and body mass index 26.9 ± 2.8 vs. 25.6 ± 2.7 kg/m2; p = 0.19).
Participants performed 5 sets of 30 concentric knee extensions at 180° sec−1 on an isokinetic dynamometer (Biodex Medical Systems, Shirley, NY) with a 60 second rest between sets. Each contraction began with the knee at 90° flexion, continued to a point of full knee extension, and concluded with the leg actively returned (500° sec−1) to the starting position. There was approximately 0.70 seconds between repetitions. During the exercise test, participants folded their arms across their chest, and waist, torso, and thigh belts were used to reduce unnecessary movement. The first repetition was considered spurious and was not used in the analysis. Using the Biodex windowing function, 29 peak torques for each set were summed and used to a represent absolute fatigue. Relative fatigue was determined by calculating the difference between the sum of 29 peak torques for each set and set 1, dividing by set 1, and multiplying by 100 (e.g., [sum of peak torquesset 1 - sum of peak torquesset 2/sum of peak torquesset 1] × 100, etc.…).
Reliability of absolute fatigue for old and young subjects (intraclass coefficient) was R = 0.95 and R = 0.87, respectively. Participant characteristics were compared using independent t-tests. A 5 × 2 (sets X age) mixed factor repeated measures analysis of variation (ANOVA) was used to compare absolute and relative muscle fatigue between old and young men. Tukey's post hoc tests were used to locate differences when ANOVA revealed a significant interaction. The level of significance was set a priori at p ≤ 0.05.
Figure 1 depicts the decline in peak torque production before calculation of absolute and relative muscle fatigue. In the analysis of absolute fatigue, there was a significant group by set interaction (p < 0.001), indicating that total peak torque production decreased across sets and was different between young and old men (Figure 2). Post hoc analyses revealed that (a) total peak torque production was significantly greater in young men during all five sets, and (b) total peak torque production was significantly decreased from set 1 during sets 2 through 5 in both young and old men.
In the analysis of relative fatigue, there was a significant group by set interaction (p < 0.001) (Figure 3). Post hoc analyses revealed that relative fatigue was significantly greater in young participants during sets 2 through 5 (old vs. young: set 2: 17.1 vs. 26.6%; set 3: 25.5 vs. 39.7%; set 4: 28.1 vs. 45.1%; set 5: 29.3 vs. 46.4%; overall relative fatigue: old 22.2%; young 38.1%).
Previous investigations using a single set of isokinetic mode knee extensions have shown that muscle fatigue is similar between young and old adults (1,12,17,20); the additional aspect of intermittent/multiple sets is a unique aspect of the current study. It was hypothesized that the enhanced fatigue resistance of older muscle may only be revealed during repeated bouts of intermittent isokinetic mode knee extensions, which favor the more oxidative nature of older muscle (13,14,17). The result of the current study, that older males demonstrated enhanced fatigue resistance during repeated bouts of intermittent contractions, supports the hypothesis.
There are several factors to consider when determining why some people report age-related enhanced fatigue resistance, whereas others do not. First, the duty (contract/relax) cycle in studies of muscle fatigue can vary considerably. The exercise protocol in the current study consisted of 30 seconds of intermittent contractions interspersed with 60 seconds of rest or approximately 150 seconds of total work. Lanza and colleagues (14) noted that studies using fatigue protocols with a duty cycle less than 50% show increased fatigue resistance with age (3,10), whereas those using a test with a duty cycle greater than 50% show no effect of age on muscle fatigue (4,28). The exercise protocol used in the current study could be viewed as 30 seconds of exercise to 60 seconds of rest or approximately 0.40 seconds per contraction to approximately 0.70 seconds rest between repetitions. Either perspective characterizes the exercise test as low duty cycle, which supports the finding of enhanced fatigue resistance in older men in the current study. Potentially, using the same number of sets and repetitions with a different duty cycle could influence the results. However, Russ et al. (26) used a dorsiflexion exercise challenge with a 70% duty cycle to test the hypothesis that a high duty cycle would eliminate age-related differences in fatigue resistance. Contrary with their hypothesis, older men and women (n = 16; 73 yr) demonstrated enhanced fatigue resistance compared with young men and women (n = 16; 25 yr). Thus, it is currently unclear what the role of the work to rest ratio is when examining age-related changes in muscle function.
The type of contraction and the number of sets may also influence the outcomes of studies of the effects of age on muscle fatigue. For instance, Petrella et al. (25) assessed muscle fatigue in older (n = 24; ≈64 yr) and younger (n = 28; ≈27 yr) adults after 10 repetitions of knee extensions at 40% of 1 repetition maximum. Older adults experienced a 24% decrease in maximum concentric velocity, whereas the young adults only tended to decrease (not significant). These data indicate that younger adults are more resistant to fatigue during a single set of isotonic contractions. Interestingly, there was no effect of age on performance of a fatiguing sit to stand test. Baudry and colleagues (2) also reported that older men and women (n = 16; ≈77 yrs) are more fatigable than young men and women (n = 16; ≈30 yrs), but their tests were during 5 sets of 30 concentric contractions of the dorsiflexor muscles at 50° sec−1. Although the exercise protocol used by Baudry et al. (2) is similar to the current study, data from dorsiflexion fatigue may not approximate knee extensor fatigue. Force production and contractile properties may not follow a similar pattern of change between muscle groups with increasing age (8,9). In older individuals, the proportion of type II fibers in the dorsiflexors and knee extensors are 16% and 45%, respectively. In terms of function, isometric strength of the knee extensors may decrease 40% in older adults up to 70 years, whereas dorsiflexor strength may decline more slowly (21,22). Evidence for age-associated differences between muscle groups was also provided by Lanza et al. (15), who showed 16% less concentric torque of the dorsiflexors and 36% less torque in the knee extensors in older, relative to younger, men. Similarly, peak power of the knee extensors was 41% less, and peak power of the dorsiflexors was 28% less in older relative to young men. Although it is informative to study aging in several muscle groups, collectively, these data indicate that it may not be appropriate to compare the dorsiflexors and the knee extensors between studies. For instance, young and old dorsiflexors may have similar dorsiflexor characteristics but dissimilar knee extensor properties, which could explain the divergent findings of Baudry et al. (2) with the current study. If it is the case that the knee extensors undergo changes that make this muscle group more oxidative in nature, then perhaps the dorsiflexors need several more years to undergo significant age-associated transformation.
Although the current study used a 2-group (old vs. young) design and found age-associated differences in fatigue resistance, a potentially influencing factor is the age of the older subjects. In two recent studies, a 3-group study design was used with young (26 yr), old (65 yr), and very old (84 yr) categories (22,23), because muscle properties in some muscle groups may change more rapidly than others (22,23). Older adults were more fatigable relative to young adults, but this only became statistically significant in the very old group (84 yr) (22). Thus, older adults in some studies may have been too young for any differences in fatigability to be detected.
Although the exercise mode investigated in the current study (isokinetic) builds upon previous studies, new data support the argument that isokinetic modes of exercise and isometric muscle contractions may not be the best choice when studying the fatigability of older muscle. For instance, McNeil and Rice (22) recently demonstrated that older adults are more fatigable than young adults when tested with a velocity-dependent (i.e., isotonic) power task. Across 25 repetitions (20% MVC), muscle power decreased 13%, 19%, and 24% in young (26 yr), old 64 yr), and very old (84 yr) subjects, respectively. The authors acknowledged that using the isokinetic mode allows the assessment of muscle power, but that isotonic contractions better reflect activities of daily living (22). In a related study, the same group showed that, in older adults, the reduction in muscle power (assessed with isotonic contractions) was 2 to 3 times greater than the loss of isometric strength (23).
Finally, neural drive could be reduced in older individuals, and this may also explain why some report an effect of aging on fatigue resistance, whereas others do not. However, there is no consensus on an inability of older adults to maximally activate their muscles (11). Differences in the methodology used to assess voluntary muscle activation (i.e., interpolated torque (IT) ratio vs. central activation ratio), muscle groups studied (e.g., quadriceps vs. dorsiflexors), and habitual physical activity levels all influence comparisons of voluntary activation between young and older adults. As an example, Yoon et al. (30) recently reported that aging increases central fatigue immediately after a low-force (20% MVC) fatiguing contraction but not after an 80% MVC. It is known that older adults are able to reach target velocity during isokinetic exercise ranging from 60 to 270° sec−1 (12), so it is not surprising that subjects in the current study were able to reach the target velocity of 180° sec−1. In the current study, an extra evoked force was not used and electromyography measurements were not performed, so any discussion of age-associated differences in neural drive is speculative.
Previous studies of the effects of aging on muscle fatigue using a single set of isokinetic mode knee extensions have reported no differences in fatigability between young and old muscle (1,12,17,20). The current study extends the findings of these previous investigations by demonstrating that older muscle is less fatigable than younger muscle during repeated sets of intermittent contractions (old vs. young: set 2: 17.1 vs. 26.6%; set 3: 25.5 vs. 39.7%; set 4: 28.1 vs. 45.1%; set 5: 29.3 vs. 46.4%; overall relative fatigue: old 25.7%; young 45.4%). Older muscle has an increased reliance on oxidative phosphorylation and a decreased reliance on glycolysis (13,14,17). Reportedly, intermittent contractions favor the replenishment of oxygen and, because phosphocreatine resynthesis is an aerobic process, this could be one reason that the older adults had enhanced fatigue resistance compared with young adults (14). The study of age-related changes in muscle fatigability remains complex and is influenced by a myriad of factors. In the future, when designing studies to assess muscle function in older individuals, researchers should consider (a) using multiple duty cycles across several exercise tests, (b) testing several muscle groups (i.e., knee extensors and dorsiflexors), (c) using different types of muscle contractions/exercise modes (isotonic in addition to the more commonly used isometric and isokinetic), and (d) the inclusion of two groups of older subjects (i.e., 60 to 79 and >80 yr).
The current study indicates that the knee extensors of older men are less fatigable than younger men during repeated sets of intermittent contractions, possibly as a result of the more oxidative nature of older muscle. The isokinetic exercise mode used in the current study builds upon previous investigations with the addition of repeated sets. The results of the current study, however, are specific to the isokinetic mode of exercise, the speed (180° sec−1), duty cycle, and the exercise protocol (5 sets of 30 repetitions). Therefore, conclusions about enhanced fatigue resistance in older muscle may not extend to other exercise modes, protocols, or contraction types. It could be argued that isotonic contractions better approximate activities of daily living, so the results of the current study should be verified using concentric/eccentric actions in a controlled laboratory setting as well as practical field tests (e.g., sit to stand, stair climb, get up and go tests). Although the exercise challenge used in the current study is not commonly performed in everyday life, these data indicate that exercise prescription in older adults need not focus primarily on resistance to fatigue. Resistance to muscle fatigue is only one component of healthy aging muscle, and enhanced fatigue resistance in the knee extensors of older men should be incorporated into resistance training program prescriptions. Perhaps exercise interventions targeted toward prevention of falls should focus on balance or power training, which may be more closely associated with performance of ADLs, rather than fatigability/sustainability of contractions.
The author wishes to thank the dedicated subjects who participated in this research study, Ian Lanza, PhD, for his data management expertise, and Priscilla Clarkson, PhD, for her support of this article. No external financial support is declared. The results of the present study do not constitute endorsement by the authors or the NSCA.
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