Normal aging is associated with a decrement in strength and functional ability of the leg extensor muscles. It has been reported that maximal voluntary concentric torque of the quadriceps reaches peak values at ∼30 yr of age, and then plateaus and remains relatively stable with only slight reductions for the next 20 yr (4,14,16,17). An accelerated decline in strength becomes apparent after age 50, where it decreases at a rate of approximately 12–15% per decade (11,16), with older individuals demonstrating 20–40% lower maximal torque output values in comparison with individuals in the third decade of life (21). Much of the research attributes this decrease in peak force to age-associated reductions in muscle mass (sarcopenia) with a selective atrophy and reduction in Type II fiber area and number being the primary factors (19).
It is well-documented that strength training can reduce muscle atrophy associated with aging. A number of investigations (2,11,12,20) have reported the ability of older men to not only maintain but increase strength and muscle fiber cross-sectional area consequent to a resistance-training regimen. However, the influence that chronic endurance training has upon age-associated changes in muscular strength and muscle morphology is largely undetermined. Results published by Klitgaard et al. (15) suggest that although strength training can prevent and/or counteract the decreases in function and morphology of aging muscle, endurance training does not influence the age-related changes in muscular size and strength. According to Klitgaard and coworkers, endurance training will mainly increase the aerobic capacity of the muscles involved but have no or only a minor effect on the maintenance of muscle mass and strength with aging. However, the work of Klitgaard et al. (15) compared groups of different body size with old control, old strength-trained, and young control subjects weighing 5, 6, and 11 kg more (respectively) compared with the old run-trained subjects. In addition, this study did not assess body composition, and therefore strength was not corrected for differences in lean body mass (LBM).
The purpose of this investigation was to examine the influence of long-term endurance training and age on strength, and muscle morphology characteristics of the leg extensor muscles. It was hypothesized that in this group of older master athlete runners, chronic endurance training would delay the age at which a significant decline in peak torque, and change in muscle fiber size and type distribution of the m. vastus lateralis occur.
Male master athlete runners (N = 107, age range = 40–88 yr) were recruited from the greater Los Angeles area. The subjects are participants in a 20-yr longitudinal study of older athletes, currently in its 17th yr, examining the effects of chronic endurance training on aerobic capacity, muscle strength, body composition, bone mineral density, and health risk factors such as blood chemistry, nutrition, and blood pressure. Over 200 master athletes (male and female) have been tested as part of this study. Subjects are considered master athletes if they are 40 yr or older, have trained for at least 5 yr, run at least 15 km·wk−1, and compete at least once per year in an organized running competition. Subjects are tested once every 2 yr. This cohort has been reported on at length in a previous publication (25). Subjects completed medical histories and a brief physical examination before participation in the study to ensure they were free from hypertension or cardiovascular disease. Subjects reported exercise history by questionnaire, and responses were confirmed by oral interview. Written informed consent was obtained from each subject after all procedures were explained in detail. This study was approved by the University of Southern California Human Subjects Committee.
Subjects reported to the laboratory in the morning after an 8-h fast. They were medically screened by a resting 12-lead EKG, physical exam, and medical history. Maximal aerobic capacity (O2max) was determined via multistage treadmill testing with continuous EKG monitoring. The treadmill protocol began at a speed of 2.5 miles·h−1 and 0% grade with increases of 0.5 miles·h−1 and 2% grade every 2 min to subjective fatigue. At least three of the four standard criteria for O2max were achieved in each subject (8). Expired air was analyzed continuously via an Ametek metabolic system with 30-s averaging of expiratory gas from a mixing chamber. All treadmill tests were medically uneventful, and no untoward symptoms were observed.
Residual lung volume was determined by oxygen dilution (24), and hydrostatic weighing was utilized to determine body density (5). Percent body fat (%fat) and LBM were calculated using the equation of Siri (22).
Maximal isokinetic strength of the leg extensor muscles was measured using the Kin-Com Dynamometer (Chattanooga Group, Inc., Chattanooga, TN). Strength testing was preceded by the O2max test in all cases, serving as a warm-up. To obtain strength measures, the subject sat with the torso and upper leg stabilized and the hip angle at 90°. The knee joint was aligned with the axis of rotation of the dynamometer, and the angular movement of the knee joint was from 15° to 80° (0° = full extension). Peak torque generated during isokinetic contraction was measured at an angular velocity of 60°·s−1. Subjects were verbally encouraged to perform at maximal effort with three attempts made and the highest value taken for subsequent data analysis. Peak torque values were reported in both absolute and relative (normalized for LBM) terms.
Muscle biopsy and analyses.
A subpopulation of subjects (N = 30) in this study volunteered to participate in biopsy testing. Muscle biopsy samples of 20–50 mg were obtained by needle biopsy from the m. vastus lateralis using the technique of Bergstrom as modified by Evans et al. (10). The specimen was longitudinally oriented in embedding medium, frozen in isopentane maintained at its freezing point with liquid nitrogen, and stored at −80°C until analysis. Serial transverse sections of approximately 10 μm were cut with a cryostat at −16°C and stained for myofibrillar adenosine-triphosphate (ATPase) at a pH of 9.3 after preincubation at a pH of 9.75, 4.65, or 4.3. Fiber type distribution for Type I and II fibers using the classification of Brooke and Kaiser was determined by direct microscopy (7). An average of 840 ± 470 fibers per biopsy sample was counted (range 254–2129 fibers). Fiber areas for Type I and Type II fibers were determined via the IM-Series morphometric system, a video digitizer interfaced with a PC computer (IMAGE 5000, Analytical Imaging Concepts, Irvine, CA). An average of 206 ± 105 fibers per fiber type was measured on each transverse section (range 69–615 fibers). The number of fibers counted and measured was maximized to decrease possible error due to variability within the muscle biopsy sample (18).
For the purpose of comparing age with regard to physical characteristics and performance variable, subjects were divided into five distinct cohorts by decade of life (40s, 50s, 60s, 70s, 80s). One-way ANOVA was used to determine age differences. When a difference was found, a Tukey post hoc test was used to determine the specific comparisons that were significant. Regression analysis was used to assess age-related differences in normalized peak concentric isokinetic torque. Data were entered into a personal computer and statistical procedures performed using the SPSS statistical package (v. 11.5). Statistical significance was preset at the P < 0.05 level.
Physical and performance characteristics.
General characteristics of the subjects are displayed in Table 1. No significant differences were noted between age-group cohorts for height, body weight, or percent body fat. Additionally, the five groups were not different for years of training or distance run per week. However, both the 70s and 80s yr groups displayed significantly less LBM than both the 40s and 50s yr groups. Further, significant differences were observed for aerobic capacity (O2max expressed in mL·kg−1·min−1) for the 60s-, 70s-, and 80s-yr- old groups compared with the 40s and 50s yr olds.
Results from ANOVA for normalized isokinetic concentric torque of the leg extensor muscles are displayed in Figure 1. This analysis found that a significant (P < 0.05) decrease in strength did not occur until the eighth decade (70 yr of age) of life. The outcome from regression analysis for normalized isokinetic concentric torque of the leg extensor muscles is displayed in Figure 2. Results reveal a significant (P < 0.05, r2 = 0.1838) age-associated decrease in relative strength (N·m·kg−1 LBM). Although there was a substantial interindividual variability, age accounted for only 18% of the variance in peak torque.
Muscle fiber type distribution and fiber areas.
Fiber area and distributions for Type I and Type II fibers are depicted in Table 2. No differences attributed to age were found for mean Type I and Type II fiber area for this sample of male master runners. As well, fiber type % showed no differences between age groups.
The influence of chronic endurance training upon age-associated changes in fiber characteristics of the m. vastus lateralis and peak torque generated during isokinetic contractions of the leg extensors has been largely undetermined. The major finding of the present investigation was that, in this sample of master athlete runners ranging from 40 to 88 yr, a significant age-associated decline in leg strength and muscle fiber area and type distribution did not appear until after the age of 70 yr. These findings are in contrast to previous cross-sectional studies of sedentary males reporting a decline in leg strength (14,16,17,21) and decrements in muscle fiber area (3,9,16) beginning in the fifth decade. The finding is also contrary to the report by Klitgaard et al. (15) suggesting that endurance training has little or no effect on the age-associated decline in muscle mass and strength. The results of the present investigation suggest that chronic endurance training can delay the age at which a significant decline in peak torque and change in muscle morphology characteristics of the vastus lateralis occur.
When expressed in both absolute and relative (normalized for LBM) terms, leg strength was maintained at the level of the youngest group (age 40s) through the seventh decade (70 yr of age). This observation is seemingly contrary to a cross-sectional retrospective study by Klitgaard et al. (15), which suggested that although strength training can improve muscle function and morphology with aging, chronic endurance training was not a sufficient stimulus to maintain muscle strength. Klitgaard et al. (15) reported that after 12–17 yr of training, 68-yr-old strength-trained men had similar knee and elbow maximal isometric strengths, both of the quadriceps femoris and elbow flexor muscles as did 28-yr-old men who were active in aerobic sports. On the other hand, men aged 68 yr, who were run trained (12–17 yr, 3 d·wk−1, 9–12 km each session) had significantly lower muscle strengths in comparison with the 28-yr-old control subjects. Yet, when normalized for quadriceps CSA, the strength of the old running-trained men was not significantly different from the young control group or old strength-trained group and was greater than that of the elderly control group. The master runners in the present sample aged 40–69 were found to have leg extension torque values similar to normally active men 20–35 yr of age (16,17) and young aerobic sportsmen 28 yr of age (15). Further, both the 70s and 80s age groups displayed torque values greater than age-matched sedentary counterparts reported by Larsson et al. (16) and Lindle et al. (17). However, regression analysis revealed that once a significant decrease in strength became apparent, the rate of decline between the sedentary individuals and trained runners was not different.
Our result of maintained fiber area and fiber type distribution across age groups (through the eighth decade) in master runners is also in contrast to previous investigations involving sedentary subjects in which significant decrements, particularly in Type II fibers, have been observed (3,9,16). Larsson et al. (16) reported fiber area atrophy of 6.9% and 8.4% per decade for Type I and Type II fibers, respectively, from age 40 to 65. This investigation also reported a 14% decrease in the relative number of Type II fibers with increasing age over the same period (5.6 per decade). On the other hand, Trappe et al. (23) reported that although a 20-yr follow-up study of formerly elite distance runners who continued to train showed a decrease in Types I and II muscle fiber size of the gastrocnemius muscle, the changes in fiber area were not statistically significant. Interestingly, the master runners in the present sample were found to have Type I and Type II mean fiber areas for the vastus lateralis greater than those reported in similarly aged sedentary to moderately active subjects (3,9) and fiber areas similar to those reported by Gollnick et al. (13) in trained distance runners aged 19–33 yr (4900.85 ± 340.85 μm2 and 5449.28 ± 591.83 μm2 for Type I and II fibers, respectively). This finding of maintained fiber morphology is consistent with the findings of Coggan et al. (6), who reported no difference in fiber areas or fiber composition between master runners (63 yr old) and younger (26 yr old) performance-matched runners. Therefore, it seems that preservation of both fiber area and fiber type distribution could be attributed to the extensive exercise histories of these older athletes.
An interesting observation in the present investigation was that whole-body LBM declined with the older age groups despite the maintenance of muscle fiber area and type distribution of the vastus lateralis. This may imply that endurance training alone may be inadequate for whole-body maintenance of LBM, as only prime movers are influenced. Further, muscular strength of the leg extensors decreased after the age of 70 in spite of the maintenance of muscle histological characteristics. This may imply that muscle quality (force per unit muscle mass) declines with aging. In a study examining muscle function in men and women aged 20–84 yr, Akima et al. (1) reported that muscle strength losses are due to a decline in muscle mass in both genders, whereas the age-related decline in muscle function in men may also be the result of neural factors, such as muscle recruitment and/or specific tension. However, neurological evidence supporting this proposition in this sample of master athlete runners remains to be elucidated.
Several limitations exist to the present investigation. A major limitation is lack of a control group—either young exercisers or older sedentary (or both). Within the primary focus of the cohort study, which is describing the physiologic changes in master athletes over 20 yr, we on occasion develop hypotheses of a cross-sectional nature. Although we recognize the limitation accompanying lack of control groups in these substudies, we believe these data provide comparative information to results in the literature and may contribute to our understanding of the role exercise can play in diminishing age-related reduction in physical capacity.
In summary, our findings support the maintenance of isokinetic leg extension strength associated with chronic endurance training through the seventh decade of life (as depicted in Figs. 1 and 2). Further, with this group of chronically endurance-trained older athletes, there does not seem to be an age effect on fiber area and fiber type distribution in a biopsy sample of the vastus lateralis through the eighth decade. It is important to point out that our results do not suggest endurance training is a sufficient stimulus to increase muscle strength and mass of the leg extensors but rather a stimulus to maintain muscle function. Therefore, as hypothesized, chronic endurance training can delay the age of significant decline in peak torque and change in muscle morphology characteristics of the vastus lateralis.
This research was supported by the R. M. Wadt Memorial Fund, Department of Biokinesiology and Physical Therapy, University of Southern California, and the Pickford Foundation, Beverly Hills, CA.
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Keywords:©2004The American College of Sports Medicine
MASTER ATHLETE; MUSCLE FIBER AREA; MUSCLE FIBER TYPE DISTRIBUTION; ISOKINETIC CONCENTRIC TORQUE