Contraction time parameters.
The time to reach one-sixth MVC was significantly shorter in S (26.6 ± 6.0 ms) compared with U (34.1 ± 8.4 ms) (P < 0.05) (Table 4). In contrast, the time to reach one-half and two-thirds MVC did not differ statistically between S (84.4-161.4 ms), E (95.3-163.3 ms), and U (105.9-177.5 ms) (Table 4).
Muscle fiber area.
Type I muscle fiber CSA was greater in S (6300 ± 1474 μm2) (± SD) but not in U (5753 ± 1194 μm2) compared with E (5072 ± 1120 μm2) (P < 0.05) (Fig. 4). Similarly, type IIA fiber CSA was greater in S (6786 ± 1901 μm2) but not in U (5068 ± 1126 μm2) compared with E (4844 ± 1168 μm2) (P < 0.05) (Fig. 4). Type IIX fiber CSA was greater in S (5224 ± 436 μm2) than E (3892 ± 1782 μm2) and U (3974 ± 344 μm2) (P < 0.05) (Fig. 4). Likewise, S demonstrated greater type II mean fiber CSA (6027 ± 1242 μm2) than E (4609 ± 1221 μm2) and U (4579 ± 857 μm2) (P < 0.05). Mean type II fiber CSA was smaller than type I fiber CSA in U (P < 0.05). In S, fiber CSA differed in the following order: IIX < I, IIA (P < 0.01). In U, fiber area differed in the following order: IIX < IIA < I (P < 0.001). In contrast, E showed similar fiber CSA for all fiber types.
Muscle fiber type distribution.
Based on fiber number, the proportion of type I fibers was greater in E (67.4 ± 13.6%) than U (46.7 ± 15.6%) and S (61.0 ± 14.7%) (P < 0.05). Furthermore, U showed a larger number of type II fibers (53.3 ± 15.6%) than E (32.6 ± 13.6%) (P < 0.05) but not S (39.1 ± 14.6%). Specifically, the proportion of type IIX fibers differed in the following order: U (29.8 ± 7.2%) > S (12.0 ± 6.7%) > E (7.6 ± 4.5%) (P < 0.01). Type IIA fiber composition did not differ between subject groups (U: 23.5 ± 13.2%, E: 25.0 ± 11.5%, S: 27.1 ± 10.6%).
Based on fiber area, the proportion of type I muscle fibers was greater in E (69.3 ± 13.5%) than U (50.1 ± 17.0%) and S (58.7 ± 11.6%) (P < 0.05) (Fig. 5). In addition, U demonstrated a greater area percentage of type II fibers (50.0 ± 17.1%) than E (30.7 ± 13.5%) (P < 0.05), but not S (41.3 ± 11.6%) (Fig. 5). Moreover, U showed a greater area percentage of IIX fibers (24.6 ± 6.0%) than S (10.5 ± 5.4%), and both were greater than E (6.1 ± 4.8%) (P < 0.01). The area percentage of IIA fibers was similar between subject groups (U: 25.4 ± 15.8%, E: 24.6 ± 11.1%, S: 30.8 ± 10.6%) (Fig. 5).
The present study demonstrates that elderly subjects chronically (i.e., for life) exposed to either endurance or strength training activities have higher maximal muscle strength (isometric MVC) than do untrained, age-matched individuals. Importantly, however, only strength trained individuals demonstrated enhanced rapid muscle strength characteristics (elevated RFD, impulse) and increased muscle fiber size (type IIA and IIX CSA) compared with untrained elderly. Several additional findings were observed regarding the effect of lifelong training on muscle morphology and fiber type composition: endurance trained elderly master athletes showed a greater proportion of type I muscle fibers than untrained individuals, whereas fiber CSA did not differ between fiber types. Importantly, type II muscle fiber CSA were elevated in the strength trained elderly individuals but not in the endurance trained individuals compared with the untrained, age-matched individuals, which suggests that chronic strength (resistance) training is superior to endurance training in delaying the age-related loss in muscle mass, and it is especially effective in counteracting the preferential reduction in type II fiber area that is typically observed with aging. Consequently, mechanical muscle performance, evaluated as the capacity for rapid muscle force exertion, seemed to be retained at a higher level in aged individuals exposed to chronic (i.e., lifelong) strength training.
The aging process is characterized by muscle fiber atrophy and loss in skeletal muscle mass (sarcopenia), reduced physiological cross-sectional area, loss in maximum muscle contraction strength, reductions in rapid muscle force capacity (i.e., RFD) and contractile power generation, reduced maximal movement speed, and reduced, maximal, isolated muscle fiber shortening speed (12,16,22,25,26,29,33). At the same time, age-related alterations in nervous system function contribute to the decline in maximal muscle force and power (40). These inevitable changes have important functional consequences, as reflected by a gradually impaired ability to handle stairs and chair rising tasks (36), reduced capacity for level walking (11), and a diminished ability to correct sudden perturbations in postural balance (18).
The decrement in maximal contractile muscle strength and power observed with increasing age is closely linked to the age-related loss in muscle mass (10,27). Notably, the reduction in leg muscle strength and power represents a significant risk factor for falls (41). The age-related loss in muscle mass is caused by a reduced number of muscle fibers as well as a reduction (i.e., fiber atrophy) in the cross-sectional area (CSA), particularly of the type II fibers (6,40).
Longitudinal studies have indicated that strength training may be used to regain a substantial portion of the muscle mass and function that is lost with aging (13,14,34), although these improvements may often be limited in absolute terms while the corresponding enhancement in functional capacity sometimes also is lacking (17). For these reasons, it has been suggested that it is of importance to investigate the effects of lifelong training on skeletal muscle mass and function, and the aging master athlete was proposed as an ideal model to determine the physiological limits for successful aging because of the chronic involvement of high-intensity exercise (17,37). However, only few studies have evaluated the physiological effects of chronic strength or endurance training in aging individuals (17,37). The available data consistently demonstrate significantly greater muscle mass and enhanced mechanical muscle function in the chronically strength trained elderly compared with nonactive, age-matched individuals (present data (31,32)), which strongly supports the notion that chronic strength training is an effective means to delay and diminish the age-related decline in human skeletal muscle mass and function (17).
In the present study it was observed that maximum quadriceps contraction strength (i.e., MVC) was greater in chronically trained compared with untrained elderly, in accordance with previous reports (31); however, no statistical difference was observed between the endurance and strength trained elderly (Fig. 1). In contrast, previous data obtained in lifelong endurance trained elderly males (79 yr) show no difference in quadriceps MVC relative to untrained, age-matched (76 yr) controls (15). Greater quadriceps MVC strength has previously been observed in long-term (12-17 yr) strength trained but not endurance trained elderly males compared with untrained, age-matched subjects (mean age 68-70 yr) (19).
The capacity for rapid muscle force exertion reflects the ability to rapidly reach a given magnitude of muscle force during the initial phase of rising muscle force (0-200 ms), as measured by the contractile rate of force development (RFD) (1,3,7,34). It typically takes 300-500 ms to reach maximal contractile force in human skeletal muscle during maximal voluntary contraction (3). In contrast, rapid limb movements and fast locomotion tasks (i.e., potential fall situations) may be characterized by substantially faster contraction times of 75-250 ms (1). In this perspective, a high RFD seems functionally more relevant than high maximal contraction strength to achieve high initial acceleration of limb segments and the body center of mass, as well as to avoid falls (1). Contractile RFD is reduced with aging (12,23,35), and this age-related drop in rapid muscle force capacity seems also to be present when RFD is normalized to the maximum isometric muscle strength (MVC) (12,23), indicating that the decrement in RFD with aging is attributable not only to quantitative factors (muscle mass loss) but also to qualitative factors (e.g., decrease in MU firing rates, type II fiber atrophy, reduced fiber pennation angle, reduced tendon stiffness, etc). In the present study, both absolute and relative RFD (and impulse) were elevated in lifelong strength trained (S) but not in endurance trained (E) elderly subjects compared with untrained age-matched individuals (U) (Figs. 2 and 3), indicating that lifelong strength training may effectively conserve physiological factors of importance for rapid muscle force capacity. On the other hand, the observation that there was no statistically significant difference in RFD or contractile impulse between S and E, despite the reduced fiber CSA in E (discussed below), suggests that lifelong endurance training may, to some extent, preserve factors of importance for contractile RFD that are not related to muscle fiber CSA (i.e., neuromuscular activation and/or tendon stiffness).
In the present study, the muscle fiber type composition observed in the aging elite athletes differed substantially from that of the nontrained, age-matched elderly (Fig. 5). Although the proportion of type IIA muscle fibers was remarkably similar in the all subject groups, the endurance trained elderly showed a significantly greater proportion of oxidative, slow-twitch type I fibers. In terms of the fastest-contracting fiber type, type IIX fiber proportions differed in the following order: endurance trained < strength trained < nontrained subjects (Fig. 5). The untrained elderly examined in the present study demonstrated a high proportion of type IIX fibers (~25%) compared with that previously reported in untrained elderly males of about similar age (10-16%) (19,44). This finding may reflect a large number of muscle fibers coexpressing the MHC IIA/IIX isoforms, as previously reported in untrained elderly (4,20,44). Alternatively, the elevated amounts of type IIX fibers in the untrained elderly could be the result of a general decrease in physical activity levels in these subjects, because inactivity is known to be associated with upregulated MHC IIX and downregulated IIA proportions (5). A reduced proportion of type I fibers (45%) was previously observed in long-term strength trained elderly males (mean age 68-70 yr; 12- to 17-yr training background) compared with age-matched runners (61%) but not untrained elderly (53%) (19). Notably, the present group differences in type I and IIX muscle fiber composition, respectively, were observed both when based on fiber area (Fig. 5) or fiber number. In other words, the present fiber type differences could not be explained by the differences in muscle fiber CSA observed between the subject groups.
The chronically strength trained individuals examined in the present study demonstrated elevated quadriceps muscle fiber area (type I, IIA, and IIX fibers) compared with the endurance trained individuals, and greater type II muscle fiber CSA (type IIA and IIX fibers) compared with the untrained elderly. Long-term strength trained elderly previously have demonstrated greater overall fiber area than nontrained elderly (type I, IIA, and IIX), and greater type II fiber area (IIA, IIX) than endurance trained elderly (19). However, the individuals examined by Klitgaard et al. (19) were younger (~69 yr) than the present subjects. Further, their strength trained individuals performed strength (body-building types of) strength training (19), whereas the present strength trained subjects were track and field master athletes who regularly, albeit less intensively, used strength training concurrently with their athletic training. Importantly, however, these data strongly suggest that long-term (12-14 yr) (19) as well as lifelong endurance training (present data) does not prevent the age-related loss in muscle fiber cross-sectional area. Consequently, ultra-long-term or chronic endurance training with aging may be accompanied by similar muscle atrophy compared with that normally observed in untrained, aging individuals. In support of this notion, decreases in muscle fiber CSA after endurance training have been observed in young individuals (21,38), whereas accelerated fiber atrophy was reported for aged runners compared with sedentary, age-matched individuals (42). In contrast, the present data suggest that type I, IIA, and IIX muscle fiber area is retained at high levels in elderly individuals exposed to chronic (i.e., lifelong) strength training as compared with untrained, age-matched individuals. Preservation of muscle size with aging likely has important functional consequences. For instance, preventing the normal age-related loss in skeletal muscle mass may protect against the development of metabolic conditions such as reduced glucose tolerance and impaired insulin sensitivity (type II diabetes).
Some limitations may be observed with the present study. Firstly, the cross-sectional nature of the study inherently restraints the conclusions that can be made about the longitudinal physiological adaptation to chronic, lifelong training in the elderly. However, because longitudinal lifelong studies are very difficult, if not impossible to conduct, important information may still be gained from the cross-sectional study of aging master elite athletes regarding the range of human physiological adaptation induced by chronic (lifelong) training (17). Because of the highly sparse number of individuals in this population, only a limited number of aging elite athletes could be recruited for inclusion in the present study. This may potentially have increased the risk of statistical type II errors in the present study, which could explain the lack of difference in type I muscle fiber area between untrained and strength trained individuals, or between untrained and endurance trained individuals, respectively. On the other hand, type I fiber CSA seemed much more similar among U, E, and S than type II CSA (Fig. 4), suggesting that the observed lack of difference may represent a true physiological finding.
In conclusion, muscle fiber size and mechanical muscle function, particularly rapid muscle force capacity (RFD), seem to be elevated in aged individuals exposed to lifelong strength training compared with untrained, age-matched subjects. The gain in muscle mechanical function and muscle morphology with chronic strength training is suggested to be functionally important because it may provide a safety capacity in rapid movement tasks (i.e., during perturbed postural balance) and because it potentially provides a physical reserve that may retard the age-related loss in muscle mass and function below the critical threshold for independent living. Notably, muscle fiber CSA and RFD, respectively, did not differ between lifelong endurance trained master athletes and untrained age-matched subjects, which may suggest that long-term training aimed at increasing muscle fiber size (i.e., strength training) should be preferred over aerobic training to countermeasure the loss of muscle mass and contractile RFD with increasing age.
This study was supported in parts by The Danish National Research Foundation (Grant 504-14), the Danish Health Science Research Board (Grant 22-04-0191), and the Lundbeck Foundation. The authors would like to acknowledge Hanne Overgaard at Team Danmark Testcentre, Bispebjerg Hospital, and Ingelise Kring at the August Krogh Institute, for valuable help during the project. Also, we wish to thank Rudolf Ahrenkiel and Henning Møller for help to recruit the subjects.
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Keywords:©2007The American College of Sports Medicine
LIFELONG TRAINING; CONTRACTILE STRENGTH; RATE OF FORCE DEVELOPMENT; AGING