Secondary Logo

Mechanical Muscle Function, Morphology, and Fiber Type in Lifelong Trained Elderly

AAGAARD, PER1; MAGNUSSON, PETER S.2; LARSSON, BENNY3; KJÆR, MICHAEL2; KRUSTRUP, PETER4

Medicine & Science in Sports & Exercise: November 2007 - Volume 39 - Issue 11 - p 1989-1996
doi: 10.1249/mss.0b013e31814fb402
BASIC SCIENCES: Original Investigations
Free

Purpose: Maximal muscle contraction force and muscle mass are both reduced during the natural aging process. Long-term training may be used to attenuate this age-related loss in muscle function and muscle size.

Methods: Maximum isometric quadriceps strength (MVC), rate of force development (RFD), and muscle fiber composition and size (CSA) were studied in elderly individuals (68-78 yr) chronically exposed (> 50 yr) to either endurance (E) or strength (S) training, and in age-matched, untrained (U) elderly group.

Results: E and S showed greater MVC than did U. Contractile RFD was elevated in S compared with U, and S also demonstrated greater type II fiber CSA than did U and E. The proportion of type I fibers was greater in E compared with U and S.

Conclusions: Muscle fiber size and mechanical muscle performance, particularly RFD, were consistently elevated in aged individuals exposed to chronic (i.e., lifelong) strength training. This relative preservation in muscle morphology and function may provide an important physical reserve capacity to retain muscle mass and function above the critical threshold for independent living at old age.

1Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark, Odense, DENMARK; 2Institute of Sports Medicine Copenhagen, Copenhagen, DENMARK; 3Team Danmark Testcentre, Bispebjerg Hospital, University of Copenhagen, Copenhagen, DENMARK; and 4Institute of Exercise and Sport Sciences, University of Copenhagen, Copenhagen, DENMARK

Address for correspondence: Per Aagaard, Ph.D., Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark, Campusvej 55, DK-5230, Odense, Denmark; E-mail: paagaard@health.sdu.dk.

Submitted for publication January 2007.

Accepted for publication July 2007.

Muscle mass as well as maximal contractile muscle strength (MVC) and power are markedly reduced with aging. For the sedentary elderly individual, the loss in muscle mechanical function may represent a serious risk for loss of independence, because it results in an impaired ability to perform chair rises and stair and level walking (11,36) while also reducing the capacity to counteract unexpected perturbations in postural balance (18).

While aging is accompanied by a gradual deterioration in mechanical muscle function, the capacity for rapid muscle force exertion (contractile rate of force development (RFD)) is particularly compromised (12,23,35). In functional terms, RFD is a highly important mechanical muscle parameter because rapid movements typically involve muscle contractions within 50-200 ms, which is considerably less than the time it takes to reach maximal muscle force (~350 ms) (3). Hence, a fast RFD plays an important role for the ability to perform rapid and forceful movements, both in highly trained athletes and in elderly individuals who need to control unexpected perturbations in postural balance (1).

The age-related decline in RFD represents an impairment in contractile muscle function, which may have significant functional consequences as it decreases the ability to counteract unexpected perturbations in body posture and postural balance, hence potentially increasing the risk for falls. Further, because a reduced RFD represents a potential risk factor for falls and impaired functional ability, it becomes important to examine to which extent long-term training can prevent the age-related decrease in RFD.

The impairment in maximal muscle strength and rapid force capacity (i.e., RFD) with increasing age seems to occur because of loss in both muscular and neural function, which comprise reductions in muscle fiber number (26), muscle fiber size (6,19,23,26), specific tension (Po/CSA) (8), reduced maximal fiber shortening speed (8,22-24), reduced muscle fiber pennation angle and decreased tendon stiffness (30). Because of their fast cross-bridge cycling rate, type II muscle fibers demonstrate a greater intrinsic RFD compared with type I fibers (28). Therefore, the reduction in RFD observed with aging (12,23,35) likely is accelerated by the preferential reduction in cross-sectional area (CSA) of fast-twitch type II muscle fibers typically observed in elderly subjects (6,40) because of the selective loss and/or a general disuse of these muscle fibers at increasing age. However, aging sprint-trained athletes also demonstrate reduced type II muscle fiber area (23), which suggests that reduced physical activity may not solely explain the preferential type II fiber atrophy with aging. Other factors comprise the progressive deinnervation of type II muscle fibers driven by neuropathic changes leading to cell apoptosis and motoneuron death at increasing age, which seem to occur independently of activity level (30,40).

In young to middle-aged males (20-40 yr of age), the CSA of type II fibers exceeds that of type I fibers by 10-20% (VL muscle) (2,5,21,38). Conversely, with advanced age (85+), the CSA of type II fibers is reduced to about 50% of that of the type I fibers (6), as also recently observed when comparing sprint-trained young and old individuals (23). Consequently, fast-contracting type II fibers contribute relatively less to force generation at increasing age, thereby causing maximal contractile RFD and power to markedly decrease with aging.

Physical training-namely, strength training-seems to be highly effective for eliciting increases in muscle size (fiber CSA), efferent neural motor drive, maximal muscle strength (MVC), and RFD-not only in young subjects (2,3,13,14,39), but also in elderly individuals (7,13,14,34). Further, strength training results in elevated tendon stiffness in the elderly (30), which likely also contributes to the training-induced rise in RFD, given that the stiffness of the force-transmitting structures by itself affects the magnitude of contractile RFD (43). It seems particularly important to employ lifelong training regimes that can attenuate the age-related decline in MVC and RFD by reducing the age-related decrease in muscle fiber CSA, particularly for the type II muscle fibers. Whereas strength training typically leads to muscle hypertrophy in both young (2,5,13,14) and elderly individuals (10,13,14), the hypertrophy effect of endurance training is more questionable. Longitudinal decreases in muscle fiber CSA in response to endurance training have been demonstrated in young individuals (21,38) and have also been indicated by cross-sectional data obtained in aging endurance athletes (42). Hence, it is questionable whether lifelong endurance training will show similar effectiveness as strength training in preserving muscle fiber CSA and mechanical muscle function throughout the age span.

Therefore, the aim of the present study was to evaluate maximum muscle contraction strength, rapid muscle force capacity, and muscle fiber characteristics in elderly master athletes exposed to either lifelong endurance (E) or strength (S) training compared with untrained (U), age-matched subjects. Using a cross-sectional study design, it was hypothesized that muscle fiber area (particularly that of type II fibers) and rapid force capacity (RFD) would be elevated in elderly individuals engaged in lifelong strength training (S) compared with untrained (U) or chronically endurance trained (E) elderly individuals.

Back to Top | Article Outline

METHODS

Subjects.

Twenty-four elderly (70.5-73.9 yr) male individuals exposed to either lifelong endurance training (E, N = 9), strength training (S, N = 7), or no training (U, N = 8) volunteered to participate in the study, which was approved by the local ethics committee of Copenhagen. Written informed consent was obtained from all participants. Age and anthropometric characteristics are shown in Table 1. Body composition (percent body fat) was evaluated by use of skinfold measurements (9), and cardiovascular fitness (V˙O2max) was obtained during a standardized graded ergometer cycling protocol to exhaustion (Table 1).

TABLE 1

TABLE 1

Back to Top | Article Outline

Training background.

The untrained subjects (U) had not engaged in any kind of regular physical training during the last 50 yr. About half of the subjects in U occasionally use a bike for individual transport over shorter distances (< 5 km). The endurance trained subjects had been engaged in endurance training (long-distance running, cross-country running, road cycling) during the last 50 yr, at a training frequency of three to four sessions per week (range: two to six times per week). The strength trained subjects had been engaged in track and field athletics (sprint running, shotput, high- and long jumping) during the last 50 yr, which involved systematic strength training at a regular training frequency of two to three sessions per week (range: two to five times per week). The trained subjects (E, S) all participated in National Master Athlete Championships in their respective events, and some of them also participated in the Master Athlete World Games, Master Athlete Olympics, and European Master Athlete Championships.

Back to Top | Article Outline

Muscle strength assessments.

As previously described in detail (3), maximal isometric quadriceps contraction strength (MVC) and rapid force capacity evaluated as contractile RFD (dForce/dt) and impulse (∫Force dt) were obtained at a 70° knee joint angle (0° = full knee extension) using an isokinetic dynamometer (KinCom, Kinetic Communicator, Chattecx Corp., Chattanooga, TN) at a 1000-Hz A/D data-sampling rate. In brief, subjects were reclined 10° in a rigid chair and firmly strapped at the hip and distal thigh. The rotational axis of the dynamometer was visually aligned to the lateral femoral epicondyle of the subject, and the lower leg was attached to the dynamometer lever arm 2 cm above the lateral malleolus. All strength measurements were preceded by a thorough warm-up that included 5 min of ergometer biking at 100 W followed by five to seven maximal vertical jumps. Subsequently, a number of submaximal isometric quadriceps contractions were performed in the dynamometer, which were followed by three to five maximal isometric quadriceps contractions (45-s pause), using strong verbal encouragement. Furthermore, online visual feedback of the dynamometer force signal was provided to the subjects on a PC screen. Subjects were carefully instructed to contract "as hard and as fast as possible." MVC was obtained as the maximal moment of force (N·m), and the rate of force development (dMoment/dt) and contractile impulse (∫Moment dt) were assessed as previously described (3). Whereas MVC was obtained from the trial with maximal peak moment, all RFD and impulse parameters were obtained from the trial with largest contractile impulse at 0-200 ms relative to force onset. Relative RFD was calculated as RFD normalized to MVC (i.e., RFD/MVC × 100%) (3,34). All recorded moments were corrected for the effect of gravity on the lower leg (3).

Back to Top | Article Outline

Muscle morphology and fiber type composition.

Muscle biopsies (100-150 mg) obtained from m. vastus lateralis of the dominant limb were analyzed as described in detail previously (2,5). In brief, fiber type composition was established using myofibrillar ATPase staining at pH 9.4 after both alkaline (pH 10.3) and acid (pH 4.3 and 4.6) preincubation (5). Fiber type distribution (fiber number, fiber area percentage) and fiber cross-sectional area for each of the three major fiber types (I, IIA, IIX) were determined using digital image analysis (TEMA 1.04, Scanbeam, Hadsund, Denmark) (5). On average, 105 ± 15, 99 ± 14, and 122 ± 15 fibers were examined per biopsy in U, E, and S, respectively.

Back to Top | Article Outline

Statistical analysis.

To enable comparisons between subjects of varying body size, all muscle strength data (MVC, RFD, contractile impulse) were expressed relative to body mass. Differences between subject groups were analyzed using nonparametric ANOVA (Kruskal-Wallis test) with post hoc group contrasts evaluated by Mann-Whitney tests (two tailed). Level of significance was set at α= 0.05. All data are expressed as group mean values ± SD, unless otherwise stated.

Back to Top | Article Outline

RESULTS

Maximal isometric muscle strength.

Maximal isometric quadriceps moment normalized to body mass (MVC) was greater in S (2.88 ± 0.63 N·m·kg−1; range 1.86-3.83) and E (2.88 ± 0.49; range 2.12-3.66) than U (2.21 ± 0.52; range 1.43-3.13) (P < 0.01) (Fig. 1). When expressed in absolute units, maximal isometric quadriceps strength was 222.2 ± 43.7 N·m (range 149.6-283.7) (S), 219.0 ± 39.9 N·m (range 153.7-256.7) (E), and 182.6 ± 33.9 (range 114.1-221.7) N·m (U), respectively.

FIGURE 1

FIGURE 1

Back to Top | Article Outline

Rapid muscle force capacity.

The capacity for rapid muscle force exertion was assessed as the contractile rate of force development (RFD) at 0-30, 50, 100, and 200 ms relative to the onset of force. RFD was greater in S (9.98-19.08 N·m·s−1·kg−1) but not in E (9.80-16.74) compared with U (7.23-12.62) (P < 0.05) (Fig. 2; Table 2). Likewise, the cumulated contractile impulse measured as the area under the moment-time curve at 0-30, 50, 100, and 200 ms were greater in S (8.24-267.93 N·m·s−1·kg−1) but not in E (7.50-256.16) compared with U (5.59-188.31) (P < 0.05) (Table 2). Relative RFD, that is, contractile RFD normalized relative to MVC (RFD/MVC), was greater in S (638 ± 177% MVC·s−1) but not E (596 ± 300% MVC·s−1) compared with U (451 ± 111% MVC·s−1) (± SD) in the most initial contraction phase (determined at one-sixth MVC) (Fig. 3; Table 3). In contrast, relative RFD obtained in the later phase of rising muscle force (at one-half and two-thirds MVC) did not differ between S (633-839% MVC·s−1), E (574-766% MVC·s−1), and U (459-613% MVC·s−1) (Fig. 3; Table 3).

FIGURE 2-Ca

FIGURE 2-Ca

FIGURE 3-Ca

FIGURE 3-Ca

TABLE 2

TABLE 2

TABLE 3

TABLE 3

Back to Top | Article Outline

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).

TABLE 4

TABLE 4

Back to Top | Article Outline

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.

FIGURE 4

FIGURE 4

Back to Top | Article Outline

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).

FIGURE 5

FIGURE 5

Back to Top | Article Outline

DISCUSSION

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.

Back to Top | Article Outline

REFERENCES

1. Aagaard, P. Training-induced changes in neural function. Exerc. Sports Sci. Rev. 31:61-67, 2003.
2. Aagaard, P., J. L. Andersen, A. M. Leffers, et al. A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J. Physiol. 534:613-623, 2001.
3. Aagaard, P., E. B. Simonsen, J. L. Andersen, P. Magnusson, and P. Dyhre-Poulsen. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J. Appl. Physiol. 93:1318-1326, 2002.
4. Andersen, J. L., G. Terzis, and A. Kryger. Increase in the degree of coexpression of myosin heavy chain isoforms in skeletal muscle of the very old. Muscle Nerve 22:449-454, 1999.
5. Andersen, J. L., and P. Aagaard. Myosin heavy chain IIX overshooting in human skeletal muscle. Muscle Nerve 23:1095-1104, 2000.
6. Andersen, J. L. Muscle fibre type adaptation in the elderly human muscle. Scand. J. Med. Sci. Sports 13:40-47, 2003.
7. Barry, B. K., G. E. Warman, and R. G. Carson. Age-related differences in rapid muscle activation after rate of force development training of the elbow flexors. Exp. Brain Res. 162:122-132, 2005.
8. D'Antona, G. D., M. A. Pellegrino, R. Adami, et al. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J. Physiol. 552:499-511, 2003.
9. Durnin, J. V. G. A., and J. Womersley. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br. J. Nutr. 32:77-97, 1974.
10. Frontera, W. R., C. N. Meredith, K. P. O'Reilly, and W. J. Evans. Strength training and determinants of V˙O2max in older men. J. Appl. Physiol. 68:329-333, 1990.
11. Guralnik, J. M., L. Ferrucci, E. M. Simonsick, M. E. Salive, and R. B. Wallace. Lower-extremety function in persons over the age of 70 years as a predictor of subsequent disability. N. Engl. J.Med. 332:556-561, 1995.
12. Häkkinen, K., U. M. Pastinen, R. Karsikas, and V. Linnamo. Neuro-muscular performance in voluntary bilateral and unilateral contraction and during electrical stimulation in men at different ages. Eur. J. Appl. Physiol. 432:913-920, 1995.
13. Häkkinen, K., M. Kallinen, M. Izquierdo, et al. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J. Appl. Physiol. 84:1341-1349, 1998.
14. Häkkinen, K., W. J. Kraemer, R. U. Newton, and M. Alen. Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiol. Scand. 171:51-62, 2001.
15. Harridge, S., G. Magnusson, and B. Saltin. Life-long endurance-trained elderly men have high aerobic power, but have similar muscle strength to non-active elderly men. Aging Clin. Exp. Res. 9:80-87, 1997.
16. Harridge, S. D. E., M. J. White, C. A. Carrington, M. Goodman, and P. Cummins. Electrically evoked torque-velocity characteristics and isomyosin composition of the triceps surae in young and elderly men. Acta Physiol. Scand. 154:469-477, 1995.
17. Hawkins, S. A., R. A. Wiswell, and T. J. Marcell. Exercise and the master athlete-a model of successful aging? J. Gerontol. Med. Sci. 58:1009-1011, 2003.
18. Heitmann, D. K., M. R. Gossmann, S. A. Shaddeau, and J. R. Jackson. Balance performance and step width in noninstitutionalized elderly female fallers and nonfallers. Phys. Ther. 69:923-931, 1989.
19. Klitgaard, H., M. Mantoni, S. Schiaffino, et al. Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol. Scand. 140:41-54, 1990.
20. Klitgaard, H., M. Zhou, S. Schiaffino, R. Betto, G. Salviati, and B. Saltin. Ageing alters the myosin heavy chain composition of single muscle fibers from humans skeletal muscle. Acta Physiol. Scand. 140:55-62, 1990.
21. Kraemer, W. J., J. F. Patton, S. E. Gordon, et al. Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J. Appl. Physiol. 78:976-989, 1995.
22. Krivickas, L. S., D. Suh, J. Wilkins, V. A. Hughes, R. Roubenoff, and W. R. Frontera. Age- and gender-related differences in maximum shortening velocity of skeletal muscle fibers. Am. J.Phys. Med. Rehabil. 80:447-455, 2001.
23. Korhonen, M. T., A. Cristea, M. Alén, et al. Aging, muscle fiber type, and contractile function in sprint-trained athletes. J.Appl. Physiol. 101:906-917, 2006.
24. Larsson, L., X. Li, and W. R. Frontera. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am. J. Physiol. 272:C638-C649, 1997.
25. Larsson, L., and R. L. Moss. Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J. Physiol. 472:595-614, 1993.
26. Lexell, J., C. C. Taylor, and M. Sjöström. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in the whole vastus lateralis muscle from 15 to 83 year-old men. J. Neurol. Sci. 84:275-294, 1988.
27. Macaluso, A., M. A. Nimmo, J. E. Foster, M. Cockburn, N. C. McMillan, and G. DeVito. Contractile muscle volume and agonist-antagonist coactivation account for difference in torque between young and older women. Muscle Nerve 25:858-863, 2002.
28. Metzger, J. M., and R. L. Moss. Calcium-sensitive cross-bridge transitions in mammalian fast and slow skeletal muscle fibres. Science 247:1088-1090, 1990.
29. Morse, C. L., J. M. Thom, N. D. Reeves, K. M. Birch, and M. Narici. In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men. J. Appl. Physiol. 99:1050-1055, 2005.
30. Narici, M. V., and C. N. Maganaris. Adaptability of elderly human muscles and tendons to increased loading. J. Anat. 208:433-443, 2006.
31. Sipila, S., and H. Suominen. Ultrasound imaging of the quadriceps muscle in elderly athletes and untrained men. Muscle Nerve 14:527-533, 1991.
32. Sipila, S., J. Viitasalo, P. Era, and H. Suominen. Muscle strength in male athletes aged 70-81 years and a population sample. Eur. J.Appl. Physiol. 63:399-403, 1991.
33. Skelton, D. A., C. A. Greig, J. M. Davies, and A. Young. Strength and power related functional ability of healthy people aged 65-89 years. Age Ageing 23:371-377, 1994.
34. Suetta, C., P. Aagaard, A. Rosted, et al. Training-induced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. J. Appl. Physiol. 97:1954-1961, 2004.
35. Thelen, D. G., A. B. Schultz, N. B. Alexander, and A. Ashton-Miller. Effects of age on rapid ankle torque development. J.Gerontol. 51:M226-M232, 1996.
36. Tinetti, M. E., and M. Speechley. Risk factors for falls among elderly persons living in the community. N. Engl. J. Med. 319:1701-1707, 1988.
37. Trappe, S. Master athletes. Int. J. Sport Nutr. Exerc. Metab. 11:S194-S205, 2001.
38. Trappe, S., M. Harber, A. Creer, et al. Single muscle fiber adaptations with marathon training. J. Appl. Physiol. 101:721-727, 2006.
39. Van Cutsem, M., J. Duchateau, and K. Hainaut. Changes in single motor unit behavior contribute to the increase in contraction speed after dynamic training in humans. J. Physiol. 513.1:295-305, 1998.
40. Vandervoort, A. A. Aging of the human neuromuscular system. Muscle Nerve 25:17-25, 2002.
41. Whipple, R. H., L. I. Wolfson, and P. M. Amerman. The relationship of knee and ankle weakness to falls in nursing home residents: an isokinetic study. J. Am. Geriatr. Soc. 35:13-20, 1987.
42. Widrick, J. J., S. W. Trappe, D. L. Costill, and R. H. Fitts. Force-velocity and power-velocity properties of single muscle fibers from elite master runners and sedentary men. Am. J. Physiol. 271:C676-C683, 1996.
43. Wilkie, D. A. The relation between force and velocity in human muscle. J. Physiol. 110:249-280, 1950.
44. Williamson, D. L., M. P. Godard, D. A. Porter, D. L. Costill, and S. W. Trappe. Progressive resistance training reduces myosin heavy chain coexpression in single muscle fibers from older men. J. Appl. Physiol. 88:627-633, 2000.
Keywords:

LIFELONG TRAINING; CONTRACTILE STRENGTH; RATE OF FORCE DEVELOPMENT; AGING

©2007The American College of Sports Medicine