With advancing age, there are significant changes in body composition such that body fat increases although modest losses are observed in muscle mass (23). The age-associated loss of muscle mass (sarcopenia) seems to be consistent in cross-sectional studies in sedentary subjects of approximately 0.5–1.0% per year past the age of 50 years (25). Approximately 13–24% of adults older than 65 years have lost enough muscle mass (>2 SD from the mean of a young adult reference population) to be considered sarcopenic, and this number increases to >50% of adults older than 80 years (2). The consequences of sarcopenia in sedentary adults includes decreased strength (21), metabolic rate (37), and maximal oxygen consumption (12). There is also a clear relationship between loss of muscle strength (dynapenia) and a loss of independence that contributes to falls, fractures, and nursing home admissions (11). Sarcopenia seems to affect both men and women similarly, although women tend to be at greater risk for loss of independence (26).
The etiology of sarcopenia and strength loss is multifactorial and has been reviewed recently (25,26). Concentric muscle strength is often observed to decrease equal to or to a greater extent than isometric force in most studies, whereas eccentric muscle strength is often conserved in older adults. The loss of peak concentric force is usually observed at higher contraction velocities, whereas the loss in eccentric muscle strength is often attributed to accumulation of noncontractile tissue changing the passive stiffness of the muscle (25,29,31). Fat and connective tissue infiltration of skeletal muscle (myosteatosis) can represent up to 15% of the total muscle cross-sectional area (CSA) in sedentary adults and is related to the physical activity levels of the subject (34). Thus the net muscle contractile tissue is less than what is determined by CSA measurements and contributes to the greater decline in strength relative to muscle mass. The increase in fat infiltration of muscle also promotes a proinflammatory condition accelerating functional decline of muscles (8,26). However, Wroblewski et al. (39) demonstrated that chronic intense exercise maintains thigh muscle mass and prevents fat infiltration in cross-sectional comparison of older master athletes (39). It is suggested that regular physical activity and structured exercise can help offset the losses in physical function described in older adults. However, our research group has previously demonstrated a loss in maximal aerobic capacity (19), muscle strength (35,36), and power (10) in a cross-sectional group of older adults who exercise regularly, with their losses similar to that of their sedentary peers.
Exercise recommendations for older adults have progressed over the past several years with recent physical activity guidelines including recommendations for resistance training and intensity, whereas earlier versions focused solely on low intensity walking activities. Starting in 1995, public health oriented guidelines (Centers for Disease Control/ACSM, Surgeon General Report, National Institute of Health consensus panel) suggested that the accumulation of ≥30 minutes of physical activity on most days of the week would reduce the risk and progression of cardiovascular disease (17). However, resistance exercise was not part of these core recommendations. Recent evidence-based Physical Activity Guidelines for Americans (2007, 2008, 2011) present a consensus that all adults, including older adults, should have an aerobic activity goal (500–1000 metabolic equivalents [MET] minutes per week), which can be accumulated in bouts of 10 minutes or longer (14). Resistance exercise was also included in these guidelines to be performed twice a week to improve bone strength and muscular fitness (30).
Although these revised recommendations emphasize higher exercise intensity and resistance training for older adults, a survey of physical activity trends in 2008 demonstrated that only 43.5% of US adults were aerobically active, 21.9% met the muscle strengthening guideline, and only 18.2% met both the muscle strengthening guideline and were aerobically active (6). Our laboratory has previously collected longitudinal data on highly active seniors who have exclusively participated in running as a form of exercise. We have reanalyzed this data to evaluate whether running alone was sufficient to prevent age-associated loss of muscle mass and muscle strength. Therefore, the purpose of this study was to investigate the effect of habitual endurance exercise on muscle mass (sarcopenia) and function (dynapenia) in active older adults.
Experimental Approach to the Problem
This is a longitudinal analysis of muscle strength in older master and active runners. Independent variables include the change in fat-free mass (lean body mass) and training volume over time.
Ninety-five very active older men (n = 59) and women (n = 35) were selected from a population of 237 master athletes participating in a longitudinal study at the University of Southern California, Los Angeles, CA. Data collection for the main study began in May of 1987 and continued through December of 2001; subjects attended the laboratory biannually for comprehensive physiologic testing. Subjects were tested during the same university term (i.e., fall or spring semester) to reduce seasonal variation in training and fitness. Of the possible 150 male and 87 female subjects, 38 men and 13 women were excluded because they never participated in the strength assessments, which began in November 1991. An additional 11 men and 14 women were excluded because they were not >50 years of age at the beginning of the study. Nine men and one woman were excluded because they routinely cross-trained with weights, and we did not want any confounding effects of resistive training. This left a pool of 92 men and 58 women for our cross-sectional analysis of strength.
Of these subjects, 29 men and 19 women did not complete a second strength assessment for a longitudinal comparison, and another 4 men and 3 women were excluded because their 2 strength assessments were less than 500 days (16 months) between tests. This left 59 men and 35 women for longitudinal comparisons of muscle mass, strength, and training volume (age range: 50–80 yrs men and 50–78 yrs women at the time of initial testing). The reason that some of the subjects were unwilling to complete additional isokinetic testing included muscle soreness experienced during initial testing or fear of injury.
All subjects gave written informed consent according to guidelines established by the Institutional Review Board of the University of Southern California. Methods have been described in detail previously (38) and will be briefly described here.
Subjects were prescreened by medical history questionnaire, resting 12-lead electrocardiogram (EKG), blood pressure measurement, and physical examination by a board-certified physician. Individuals with medical conditions precluding full participation in the study were excluded. The exclusion criteria included prior myocardial infarction, coronary artery disease, undiagnosed arrhythmia, or uncontrolled hypertension. Subjects with previously diagnosed arrhythmia, hypertension, diabetes, or other metabolic disease who had received clearance from their personal physicians were included as study participants.
Subjects self-reported years of training, distance run per week (kilometers), days run per week, and if they cross-trained in swimming, cycling, resistance exercise, and any periods of inactivity due to injury/illness since their previous test. Subject responses were confirmed by oral interview on the day of testing. Height was measured with a stadiometer, and weight was determined on a calibrated Homs beam scale. Residual lung volume was assessed by oxygen dilution, and body composition was determined by hydrodensitometry utilizing the Brozek equation (4).
Maximal Aerobic Capacity
The V[Combining Dot Above]O2max was determined using a continuous incremental protocol on a motorized treadmill, whereas the volume of expired air, oxygen, and carbon dioxide were determined by indirect calorimetry, as described in greater detail previously (38). A 12-lead EKG was monitored continuously throughout the exercise.
Peak voluntary isokinetic knee extension strength and isometric knee extension and flexion strength were assessed using a KinCom dynamometer (Chattecx Corp., Hixson, TN, USA). In most cases, strength testing followed V[Combining Dot Above]O2max testing which served as a warm-up; the treadmill test was approximately 12–14 minutes in length, and sufficient time was allowed between fitness testing and strength testing to avoid fatigue during the strength testing. When this was not the case, subjects rode a bicycle ergometer for 5 minutes to warm-up. For all follow-up testing, the same protocol was used so that if fatigue was present due to the treadmill test it would have similar effect on the subsequent strength tests and should not impact the longitudinal nature of the data. Subjects were seated on the dynamometer with the dominant leg in the testing position and the seat position and seat back adjusted to ensure the thigh was completely supported. Subjects were stabilized using chest, waist, and thigh straps with the hip angle at 90-degree angle. The axis of the lever arm was aligned with the axis of the knee joint and the lever arm pad adjusted so that it was directly above the ankle with the subject’s foot in dorsiflexion; the leg was strapped to the lever arm using an ankle strap. Length of the lever arm, seat position, and dynamometer head elevation were recorded to insure uniformity on retest. Subjects were instructed on the testing procedures, performed several repetitions as practice and warm-up, and then were verbally encouraged to perform each exercise maximally for 3 separate efforts, with 1-minute recovery between efforts. The best effort was recorded.
After gravity correction, maximal isokinetic knee extension strength (torque) of the quadriceps was measured concentrically and eccentrically between angles of 15 and 80 degrees of knee flexion (0-degree angle = full extension). Isokinetic strength was calculated as the peak torque achieved at an angular velocity of 60-degree angle per second (1.05 rad·s−1) corrected for lever arm length and is presented in Newton meters (Nm). Average force and time to peak force were also recorded.
Maximal isometric knee extension (quadriceps) strength was measured at angles of 30, 45, and 60 degrees of knee flexion although knee flexion (hamstrings) strength was measured at angles of 15, 30, and 45 degrees of knee flexion. Isometric muscle strength (torque) is the product of force multiplied by its moment arm and is also presented in Newton meters. Based on the peak isometric knee flexion at 15-degree angle and the peak isometric knee extension at 60-degree angle, the hamstrings-to-quadriceps (H:Q) ratio was determined.
Values are expressed throughout the results as mean ± SD. For statistical analysis by sex at baseline (between subjects), the data were analyzed by independent t-tests where 95% confidence intervals (CIs) were determined. For the longitudinal comparison of time (within subjects), each sex was analyzed separately using a dependent t-test. The absolute value of the change in score was compared between sexes, and its significance is indicated by the 95% CI. Due to large variations in the time between testing (range: 20.8–112.7 months; 1.75–9.4 years), comparisons of the absolute change in variables between test/retest were also done relative to time elapsed. As an example, to evaluate the longitudinal changes in knee strength, force production was expressed as the percent change (%) and as the percent change per year (%·yr-1) to control for the possible confounding effects of the variation in time between tests (33). To further evaluate changes in strength among the cohorts and to determine if strength losses were greater among the oldest individuals, the subjects were separated into 2 groups (50–59 years and 60–80 years) classified by their age at initial testing and by sex, and within subjects comparisons were done by dependent t-tests, whereas the change in variable scores between sex or age were compared by independent t-test. Pearson-product correlations between the change scores were also completed that help determine the variables used in the stepwise multiple regression analysis. All statistics were carried out via Statistical Package for Social Sciences software (IBM v 19.0, Chicago, IL, USA), and significance was set a priori at p < 0.05.
Descriptive and training variables are located in Table 1, whereas the strength values for the 59 men and 35 women can be seen in Table 2. There were no significant differences between initial age at baseline between the men and women, whereas the men had greater total body weight (p = 0.001), height (p = 0.001), fat-free mass (p = 0.001), and less percent body fat (p = 0.001) than the women at the time of initial testing. At baseline, men had a higher V[Combining Dot Above]O2 (p = 0.001) and had been training longer (p = 0.001) than the women, although their training volume was similar (p = 0.16) due to large variability in training distances. Men also had greater isometric extension (p = 0.001), isometric flexion (p = 0.001), and peak concentric isokinetic knee strength (p = 0.001) than women, as measured during their initial evaluations. The hamstrings-to-quadriceps ratio was not statistically different in the men and women during initial testing.
Longitudinal changes in descriptive variables and training indices over the study in the men and women can be observed in Table 1. The time between visits was 57.9 ± 23.9 months (4.8 years) in the men and 56.9 ± 23.8 months (4.7 years) for the women, and there was no statistical difference in the duration from test to retest (95% CI: −9.8 to 10.5 months) between the men and women. There was a small but significant decline in height although body weight increased in both sexes. The increase in body fat did not reach statistical significance in either sex although there was no appreciable loss or significant changes in fat-free mass. There were significant declines in both absolute (L·min−1) and relative (ml·kg−1·min−1) V[Combining Dot Above]O2 max and training distance (km·wk−1) and frequency (d·wk−1) in both the men and women between test and retest (Table 1). However, the longitudinal changes in the absolute value of these descriptive and training variables over the follow-up period were not statistically different between the men and women (data not shown); suggesting the rate of loss was not different between the sexes.
Longitudinal changes in strength values over the study period in the men and women are located in Table 2. Peak isometric knee flexion muscle strength (hamstrings) declined significantly in both the men (≈20 Nm) and women (≈15 Nm) at all 3 angles measured (15, 30, and 45 degrees; Table 1) over time, although the mean loss in flexion strength was not statistically different between the men and women. This loss in flexion strength amounted to 3–4% per year (12–18% total) in both the men and women (Table 3). Peak isometric knee extension muscle strength (quadriceps) also declined significantly in both men (≈50 Nm) and women (≈30 Nm) at all 3 angles (60, 45, and 30 degrees), with the men losing significantly more knee extension strength (Nm) than the women (95% CI between sex: −39.8, −10.1 Nm at 60-degree angle, −40.0, −12.3 Nm at 45-degree angle, and −28.6, −3.4 Nm 30-degree angle). The loss in extension strength amounted to 4–5% per year (20–25% total) in the men and women (Table 3). The rate of loss in the absolute (%) or annualized (%·yr−1) change in isometric strength loss was not significantly different between the men and women for either flexion or extension (Table 3). The change in peak isometric leg flexion strength (15-degree angle) was significantly correlated (r = 0.50; p = 0.001) with the change in isometric leg extension strength (60-degree angle) among the combined group of men and women. A stepwise linear regression demonstrated that only the change in age (or passage of time) explained the loss in peak isometric leg extension strength (r = 0.30; F = 6.91, p = 0.011), whereas the change in fat-free mass or distance run per week (km·wk−1) were excluded from the analysis.
The longitudinal comparison of isokinetic concentric knee extension strength (quadriceps) did not change appreciably over the follow-up period (Table 2), with the data demonstrating large variability both within and between subjects. The angle of knee flexion at which peak concentric knee extension strength occurred was 57 degree in men and 53 degree in women, did not change significantly over time, and was not statistically different between the men and women. The observed decline in isokinetic eccentric extension strength (quadriceps), the resistance to forced knee flexion, was not statistically significant in men (95% CI: −32.3 to 7.3 Nm), but the decline in eccentric torque was significant in women (95% CI: −74.4 to −12.1 Nm; p = 0.022). The absolute change in concentric and eccentric strength over time was not different between the men and women. The annualized change in isokinetic strength (%·yr−1) demonstrated large standard deviations (variability) and was not significantly different between the men and women for the concentric phase of knee extension, whereas the women demonstrated greater losses in eccentric torque then the men (Table 3).
Age Group Comparisons
The pretest and posttest descriptive characteristics, training variables, and strength data for the men are in Table 4, whereas the data for women are in Table 5. The time between pretest and posttest was not different between age groups or sex. Longitudinal changes in height were small and only significant in the older group of men. The increase in body weight was significant in the younger group of men, whereas there were no significant longitudinal changes in height or weight in either group of women. Similarly, a small increase in body fat was only observed in the older group of men. It should be noted that the BMI and body fat (%) values for both men and women in both age groups would be classified as “normal” and within the 75th percentile for men and the 85th percentile for women (1). Fat-free mass was greater in the men as compared with the women and did not decrease longitudinally in either sex or age group.
As we have reported previously (19), the longitudinal measure of maximal fitness decreased in both absolute (L·min−1) and relative (ml·kg−1·min−1) terms in the younger group of men although only relative V[Combining Dot Above]O2max declined in the older men. There were no changes in V[Combining Dot Above]O2 max in the younger women, whereas both absolute and relative V[Combining Dot Above]O2max declined in the older group of women. Training load (km·wk−1 and d·wk−1 run) were both consistent in the younger men whereas both declined significantly in the older group of men (Table 5), with the rate of change being significantly different for kilometers run per week (95% CI: −21.7, −0.6 km·wk−1) between the age groups in the men. However, in the women, the distance run per week was reduced for both the younger and older women at follow-up and was not different between age groups.
The loss of isometric flexion and extension strength was significant for all angles measured in both the younger and older men, whereas the rate of loss was not different between the age groups for the men (Table 4). In the women, the loss of isometric extension strength was also significant for all angles measured in both the younger and older groups, but the loss in isometric flexion strength was only significant in the younger but not for the older women (Table 5); the rate of change was not different between age groups. As observed in the whole group (Table 2), there were no consistent longitudinal changes in the concentric or eccentric knee extension in the men or women in either age group (Tables 4, 5). The lack of significant numbers of female runners over the age of 60 years, or those willing to complete the isokinetic testing, limits our power and may have masked changes as being significant.
The most important finding of this study was that these older adults who used habitual aerobic activity as their sole means of exercise demonstrated no changes in fat-free mass but significant losses in peak isometric muscle strength (≈5% per year). Several longitudinal studies in sedentary adults have demonstrated that the loss of muscle strength exceeds that of muscle mass (8,15,21), suggesting a loss of muscle quality. Goodpaster et al. (15) demonstrated that over a 3-year period muscle strength was lost about 3 times faster (2.6–4.1%·yr−1) than muscle mass (15) with the changes in leg lean mass only explaining about 5% of the changes in muscle strength. Furthermore, maintenance of muscle mass does not necessarily prevent the loss in strength (8). Our data are unique in the large number of men and women, their longitudinal nature, and the high activity levels of the subjects. However, our data suggest that running alone may prevent sarcopenia (loss of muscle mass with age) but not dynapenia (loss of muscle strength). These findings are relevant to current exercise recommendations for older adults that now emphasize resistance training as a critical component of the exercise regime.
Several limitations to the current study need to be addressed including not having a direct measure of running intensity, that this study is limited by the lack of a sedentary control group, the large differences in follow-up time, and subject mortality effecting follow-up. The lack of a direct measure of exercise/running intensity is important, and a decline in intensity may have contributed to the loss of muscle strength over time. If we assume an average 7:30 to 10:30 minutes per mile training pace combined with the self-reported running volumes (Table 1), we could estimate a total exercise time in this group of subjects would be 175–250 minutes per week in the men and 128–180 minutes per week in the women. According to the current Physical Activity Guidelines for Americans (14,18), adults need to engage in at least 150 minutes per week of moderate-intensity activity or its equivalent (defined as aerobically active) to obtain substantial health benefits and more than 300 minutes per week (defined as highly active) to obtain more extensive health benefits. Based on this pace and intensity of the current subjects running activity, this would be classified as vigorous-intensity physical exercise (≥6 METs) and would meet or exceed the current exercise recommendations for older adults of 10 MET hours·wk−1. This level of physical activity has been associated with significant reduction of various clinical outcomes in sedentary adults (14), and we have previously reported that these subjects have extremely high cardiorespiratory fitness (19) and decreased cardiometabolic risk profiles (38). However, despite these significant exercise levels, this aerobic activity was not sufficient to maintain the muscle strength of the majority of the group and changes in the distance run per week was not correlated to changes in muscle strength.
In our study, the loss of peak isometric strength was consistent at all angles measured in both the men and women; however, isokinetic torque changes were not. The larger losses observed in isometric extension strength as compared with isometric flexion strength may explain why a significant portion of our subjects may be at risk for potential knee injuries as determined by the hamstring-to-quadriceps ratio; a H:Q ratio of less than 2:3 indicates increased risk for knee injuries in young athletes (20). Our finding that isometric knee flexion strength decreases with increasing joint angles (15–45 degrees) although isometric knee extension strength increases with an increase in joint angle (30–60 degrees) has been demonstrated previously in sedentary older men and women (32). Our mean values for peak isometric knee extension strength are similar to those previously reported in a large group of sedentary subjects (16); however, our isokinetic knee extension data are considerably less than those reported by Harbo et al. (16) and Borges (3). Both of those studies measured isokinetic torque at 90-degree angle per second (3,16) In the current study, concentric isokinetic torque was measured at a contraction velocity of 60-degree angle per second, and this may have contributed to our lack of consistent findings for this measure of strength. Other studies have demonstrated that strength is more affected at higher contraction velocities (5,22). Frontera et al. (13) have demonstrated significantly greater losses in muscle torque at fast angular velocities (240-degree angle per second vs. 60-degree angle per second) in a group of sedentary men (13). An important limitation to the isokinetic measures in our study is the small number of subjects that participated in the isokinetic testing at follow-up. The total number of subjects was reduced by 14 men and 16 women between the isometric and isokinetic testing primarily because of the participants’ fear of potential injury and their unwillingness to participate in these tests. It is possible that if all subjects had been tested at follow-up, the concentric strength changes would have been significant.
Another important change observed in skeletal muscle with age is a loss of motor units (MU) and a remodeling of skeletal muscle and the preferential loss of the type II (fast-twitch) muscle fibers, which may contribute to strength losses (7,9). When one considers the size principle of motor unit recruitment and the fiber types required to sustain endurance running as an activity, the required strength output is low, cyclic in nature, and requires predominantly type-1 fibers (24). When these muscle mass and recruitment patterns are combined with the reduction in total training volume (and most likely intensity) observed in our older runners, it is possible that our subjects (who used running as their sole means of exercise) may have sustained enough MU activity to maintain muscle mass but not enough high-threshold MU activity to sustain the faster type-2 muscle fibers that may contribute to the strength losses observed in this group. In support of this concept, Power et al. (27,28) have demonstrated that the estimated number of MUs seems to be preserved in the active tibialis anterior but not the biceps brachii of highly competitive Master (>65 years) runners.
Our data demonstrated a significant decline in isometric knee extensor and knee flexor strength, whereas there were no changes in LBM in this group of very active older men and women. It is worth noting that these outcomes may only be applicable to very active healthy older adults. However, our data do support the newer exercise guidelines for older Americans suggesting resistance training be an integral component of a fitness program and that running alone was not sufficient to prevent the loss in muscle strength (dynapenia) with aging. Physical activity and exercise programs for older adults should follow recent guidelines (14) and include specific recommendations for days per week, number of exercises, sets and reps, and the intensity of the exercises performed.
The authors wish to thank all the students and athletes who have participated over the past 14 years in this study at the University of Southern California. Funding provided by the Pickford Foundation, Malibu, CA; and the R.M. Wadt Memorial Research Fund, Los Angeles, CA. There are no conflicts of interest with any company or product used in the data collection of this study. Furthermore, the results of the present study do not constitute endorsement of the product by the authors or the National Strength and Conditioning Association.
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Keywords:Copyright © 2014 by the National Strength & Conditioning Association.
muscle strength; aging; isometric; master athletes; isokinetic