The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 58:B889-B894 (2003)
© 2003 The Gerontological Society of America
Differential Effectiveness of Low-Intensity Exercise in Young and Old Rats
Marybeth Brown1,2,3,
Jennifer Taylor1 and
Rob Gabriel1
1 Program in Physical Therapy, Washington University School of Medicine, St. Louis, Missouri.
2 Physical Therapy Program
3 Veterinary Biomedical Sciences, University of Missouri–Columbia.
 |
Abstract
|
|---|
Low-intensity exercise increases strength and function in old adults, but it is unclear if change occurs secondary to "neural adaptation" or to intrinsic muscle adaptation. Whether function and strength change concomitantly is also unclear. We examined effects of a modest intensity, 10-session exercise program on muscle mass, contractile force, and function (gait) in 6-month-old and 30-month-old rats. Animals underwent 45 minutes of activity (e.g., ramp walking, balancing) 5 days/week. In old animals, a significant increase in muscle mass and peak contractile force occurred with exercise in soleus, plantaris, extensor digitorum longus, and peroneus longus compared with controls, but did not restore values to those for young controls. The increase in muscle force in old rats was accompanied by a significant lengthening of stride (90 ± 9 to 103 ± 15 mm), which was still 23% less than stride values for young rats. Changes in muscle function and gait with exercise were not apparent in young rats. Results suggest that (a) rapid and significant changes in muscle mass and strength in an aged organism can occur with a modest activity program, (b) the threshold for muscle adaptation may differ in young versus old rats, and (c) changes in strength and function in old rats may occur concomitantly.
IT has been recognized for more than a decade that skeletal muscle in an aging and aged organism has the capacity to increase strength and muscle mass in response to a high-intensity training stimulus. Landmark studies of elderly men and women have demonstrated that enormous increases in strength, expressed as a percentage of gain, are possible even in the oldest old (1–4). Findings also indicate that strength increases are associated with an increase in muscle mass and improvements in functional tasks such as stair-climbing (1–4). It has been noted that older adults are capable of making similar improvements in functional ability, as those noted with traditional strength training, with less rigorous exercise protocols (5–7). It has generally been assumed that in an aged individual, any strength gains associated with low-to-moderate-intensity exercise are the consequence of neural adaptation, not hypertrophy (8,9).
Most debilitated elders with muscle weakness receive rehabilitation services for 1–2 weeks with the expectation (supported by observation) that strength and function will improve. Few seniors are actually capable of performing a traditional weight-training protocol and rarely are supervised strength-training programs available for 2–3 months, particularly within a rehabilitation setting. Frequently, low-to-moderate-intensity exercise regimens are implemented for rehabilitation as they are easier to perform, are within the client's capability, require little equipment, and are less likely to cause injury. There is evidence to indicate that long-duration (e.g., 3 months) low-intensity programs produce gains in strength and function (5,6). Whether meaningful change in strength and function is possible within a shorter time frame, a time frame consistent with current rehabilitation limitations, has not been thoroughly examined. Consequently, this study was undertaken to comprehensively examine the effects on skeletal muscle of a relatively low-intensity, short-duration exercise program in young and old rats. The primary aim of the study was to determine if a modest exercise stimulus could result in a significant gain in strength, due to an increase in muscle mass, in an aged animal. Additionally, it was also the intent of this study to determine if low-intensity exercise resulted in modification of function (gait characteristics), particularly in old rats, within a 2-week exercise period.
|
METHODS
|
|---|
Animals
An animal model was used to permit an in-depth examination of 4 individual muscles with different functional demands (i.e., postural vs locomotor vs nonpostural) and differing proportions of muscle fiber types I and II. Forty-eight (n = 12/group) male Fisher 344/Brown Norway hybrid rats from the specific pathogen-free colony maintained by the National Institutes on Aging were used. Young animals aged 6 months and old rats aged 30 months were randomly assigned to control (no exercise) or exercise conditions. Upon receipt, rats were placed in a barrier facility under conditions that were matched as closely as possible to those provided for the animals previously. Temperature (22–23°C) and hours of light (7:00 AM to 7:00 PM) were consistently maintained and rats were provided with water and chow ad libitum. Prior to experimentation, all animals were allowed 2 weeks of recovery time following shipping to adjust to the new facility. Old rats in particular were closely monitored for signs of failure to thrive (e.g., weight loss). Given time to adapt to the new facility and 2 weeks of exercise (or control conditions), rats were 7 and 31 months of age when tested. All protocols were followed in accordance with the Guide for Care and Use of Laboratory Animals as approved by the Council of the American Physiological Society and the Animal Use Boards of the University of Missouri and Washington University.
Exercise Protocol
A modest exercise program was used to determine if this approach would result in a gain in muscle strength and mass in an aged organism. A general conditioning program of moderate intensity was chosen for several reasons. First, a general conditioning program is consistent with the exercise capabilities of most older adults and thus the results would be reasonably applicable to humans. Second, a general conditioning exercise program requires little equipment, which is consistent with the needs of most older people interested in exercise. An exercise approach that provides the greatest benefit for the investment and is safe for older adults is the ultimate goal. The short 2-week exercise duration was chosen, as this time frame is consistent with current third-party payer constraints for modifying frailty or functional loss for older adults.
The exercise program consisted of 10 sessions (5 d/wk) with each group exercise session lasting 
45 minutes. Four exercise animals at a time were placed in a "gymnasium" consisting of a 48-inch plastic circular (child's) swimming pool filled with objects to climb on, through, and around. Most of the time, rats were spontaneously active exploring their new environment. If animals stopped exercise to groom or visit, they were moved to another location in the gymnasium to stimulate more walking and climbing activity. In addition to spontaneous activity, all rats were required to climb out of a 6-inch-high box 20 times, walk up and down a 3-foot-long 30° incline 6 times, and hold onto an 18-inch square of stout metal mesh, which was continuously repositioned by an investigator to require uphill, downhill, and side-to-side bracing motion. Finally, all rats were placed in a clear plastic ball (8 inches diameter) for 5 minutes, and during that time they had to balance as the ball was rolled in all directions. Thus, exercise activities were designed to recruit lower extremity musculature and facilitate standing on the hind limbs. The only resistance encountered by the lower extremities, however, was body weight. Control rats were also brought to the laboratory daily and handled 4–5 times during the time the exercise rats were undergoing their program.
Gait Analysis
Prior to and following the 2-week exercise period, rat stride length, step length, and stride width were obtained as an index of functional capacity. To obtain reliable data, rats were trained for several days to walk the length of a 3-foot-long clear Plexiglass tube that was 4 x 4 inches (width, height). Once rats walked the length of the tube at a consistent and reliable self-selected speed, without stopping or turning, data were collected. Black stamp pad ink was applied to the forepaws and red ink was applied to the hind paws before each walking trial. White paper cut to the dimensions of the tube was inserted prior to all trials to obtain a permanent walking record. To determine stride length, the distance from the heel strike of one paw to the heel strike of the same paw was measured, i.e., left heel strike to the next left heel strike. For step length, the distance from heel strike on one paw to the heel strike of the opposite paw was measured (Figure 1). For stride width, a perpendicular line was drawn from a line bisecting each paw and the distance of that line was measured to the nearest millimeter. Three to five walking trials yielded a minimum of 25 strides (mode = 40 strides) for each rat.
View larger version (10K):
[in this window]
[in a new window]
|
Figure 1. Typical gait record from a young control animal. Stride: the distance from heel strike to heel strike on the same side of the body. Step: heel strike to heel strike on opposite sides of the body (e.g., left heel strike to right heel strike). Stride width: the perpendicular distance from the left and right metatarsal pads. An average of 25 strides was measured for each animal
|
|
Contractile Properties
The day after the final exercise bout, rats were deeply anesthetized with an i.p. injection of sodium pentobarbital (65 mg/kg) with 0.05 ml injections (3.25 mg) given as needed (45–60 min) to maintain deep anesthesia. Body temperature was maintained by keeping the anesthetized rat on a water-jacketed heating pad. The distal tendons of the soleus (SOL), extensor digitorum longus (EDL), plantaris (PLA), and peroneus longus (PLO) muscles were surgically exposed and attached in turn to a Grass force transducer with 2.0 silk. The tibial and common peroneal nerves were isolated and placed on a bipolar stimulating electrode. The exposed portion of the muscle was bathed continuously with 37°C rat Ringer's solution. Nerves were bathed with 37°C mineral oil. Before contractile properties were obtained, animals were allowed to thermoequilibrate for 15 minutes.
The left leg was rigidly immobilized. The force transducer was attached to the muscle being tested and adjusted so that passive tension was zero grams. Muscle length was progressively increased using a micromanipulator until Lo was reached. At Lo, a peak tetanic contraction (Po) was elicited by 0.5 ms supramaximal pulses delivered at 100 Hz (400 ms duration) for the SOL, and 150 Hz for the EDL (250 ms train duration), PLA (300 ms train duration), and PLO (350 ms train duration), respectively. These stimulation intensities and durations were determined in a previous study (10), and parameters selected elicit peak values for both young and old animals. Muscles were consistently tested in the same order: PLA, SOL, PLO, and then EDL to minimize potential fatigue.
Muscle Mass and Total Protein
Once experiments were complete, animals were given an overdose of pentobarbital, weighed, and all muscles of interest were dissected out bilaterally and weighed. In addition to the SOL, PLA, PLO, and EDL, the gastrocnemius was removed and weighed. Values for total protein were determined for the gastrocnemius, SOL, EDL, and plantaris using the bicinchoninic acid method (Sigma Chemical, St. Louis, MO).
Data Management
Values for gait parameters, body mass, muscle mass, total protein, and peak tetanic tension were compared using a 2 x 2 analysis of variance. If significance was achieved ( p <.05), a Bonferroni post hoc test was performed to determine where significant differences existed. T tests were also used to determine differences between old control and exercise rats.
|
RESULTS
|
|---|
Body Weight and Muscle Mass
Old rats significantly outweighed both groups of younger animals. Young exercise rats were thinner (not significant, NS) than controls at the beginning of the study (402 ± 20 vs 435 ± 22 g), and following an exercise-related loss of 18 g, a significant difference in body weights for young but not old rats was observed (Table 1). Old exercise rats gained 15 g during the 2 weeks of increased physical activity.
The decline in muscle mass observed with aging (range, 14%–25%) was significant for all muscles studied: EDL, PLA, SOL, PLO, and gastrocnemius. Exercise had an influence on muscle mass in the old rats by abolishing the significant age-related differences in the SOL, EDL, PLO, and PLA (Table 1).
Gait Analysis
A significant age-related increase in stride width (38 ± 5 vs 59 ± 5 mm) and a significant reduction in stride length (134 ± 18 vs 94 ± 11 mm) and step length (67 ± 11 vs 47 ± 8 m) were observed when young to old comparisons were made. Part of the increase in stride width for old animals was due to their larger body size (R2 =.50). Exercise resulted in a significant improvement in stride and step length for old but not young rats (Figure 2). No changes occurred in stride width with exercise in either young or old animals.
View larger version (22K):
[in this window]
[in a new window]
|
Figure 2. Stride length before and after exercise for young and old rats. *Stride length was significantly longer for young rats compared with old (p <.01).  Stride length with exercise significantly improved for old rats (p <.05). Gait data for controls were obtained at two time points, at the same time and day as exercise rats
|
|
Contractile Properties
The expected age-related decline in peak tetanic tension (Po) was seen in all 4 of the muscles studied. The magnitude of contractile tension decline ranged from 25% (PLO) to 38% in the plantaris (Table 2). For old animals, the 2-week exercise protocol resulted in a 20% increase in Po, which was significant when comparisons were made to old controls. Exercise failed to abolish the significant differences seen between the young (both groups: control and exercise) and old exercise rats. Exercise had no effect on Po in young rats.
Total Protein
Old exercise rats had less EDL protein than young rats. An age-associated decline in total protein was noted for the PLA (Table 3). Exercise resulted in a significant increase in protein content in the SOL (young rats only) and gastrocnemius in young and old animals.
|
DISCUSSION
|
|---|
The major findings in this study were that, with 10 sessions of exercise, (a) a differential effect of exercise for young versus old animals was observed with the same activity program, (b) a reversal of age-associated atrophy occurred in 4 of 5 muscles studied in old exercise rats, and (c) a significant increase in peak contractile force occurred (old rats only) in all 4 muscles studied and in muscles with different fiber type proportions and functional demands (locomotor vs postural). Moreover, these changes occurred within 14 days with an exercise program of seemingly modest intensity. A concomitant improvement in gait stride and step length was also noted, supporting an association between the increase in muscle strength and walking speed (stride length is one determinant of gait speed).
For an increase in strength to occur, there must be a stimulus intensity above "threshold" to promote an increase in muscle protein synthesis (11). Although the exercise program was the same for young and old rats, there is a high probability that the exercise stimulus was not the same for young and old animals. Old rats weighed almost 100 g more than young animals and had 20% less muscle mass. Thus, the relative demand on the leg muscles in old exercise rats, just to counteract body weight, was approximately one-third again as much as the muscular demand in young rats. Old rats needed stronger muscle contractions than young rats to perform each exercise and walk. Exercise in this study was not intended to be resistance training per se, but it appears that counteracting body weight during exercise was a sufficient stimulus for a strength increase in old animals.
Strength increases have been noted with low-intensity exercise programs for elders (5–7), and a similar mechanism for strength change may occur in old adults with sarcopenia. Atrophic lower extremity musculature in frail older adults may be required to contract at maximum or near maximum to successfully counteract body weight when getting up from a chair or climbing stairs. Even though the activity is high demand, getting up from a chair once or twice a day with many inactive hours in between may not be a stimulus sufficient to maintain muscle mass and strength. An exercise program that requires standing up and sitting down 10 times, twice a day, may be adequate to promote significant change. "Low intensity" exercise programs that result in strength increases may not be low intensity at all because of the high muscular demand of some activities. Unclear is whether the strength increases in older frail adults, with low-intensity exercise, are associated with muscle hypertrophy, neural activation as suggested, or both (8).
Rats may have gained muscle mass and strength because they became more physically active. The observation that routine daily activity did not maintain muscle mass (and strength) in old rats suggests that these animals were quite sedentary. Theoretically, the demands of the activity program did not exceed the physical demands of routine cage activity. A reduction in spontaneous activity with age has been noted for old rats, although not specifically for the F344/Brown Norway strain (12,13). A previous study of Long Evans rats indicated a progressive decline in activity level between 3 and 27 months with few animals engaging in any spontaneous wheel-running activity in later life (14). At 6 months, however, there was no evidence of atrophy in response to the reduction in spontaneous wheel-running. By 27 months, age and inactivity combined were associated with significantly reduced muscle mass and fiber area in the Long Evans strain. The finding in this study, that exercise eliminated nearly half of the difference in muscle mass between young and old rats, suggests that inactivity was a major causative factor.
This study also points to the possibility that older animals may be more responsive than young animals to the amount of exercise needed to induce both intrinsic adaptations (e.g., muscle hypertrophy, increased force production) and functional adaptation (e.g., stride length). Perhaps the threshold or minimum stimulus required for promoting an increase in contractile protein was lowered by inactivity in the old rats. A greater sensitivity to low-intensity resistance exercise has been reported for bone (15). Alternatively, the stimulus for change may differ for old animals. If the stimulus for an increase in muscle strength is in part mechanical, possibly the age-associated increases in intramuscular connective tissue (14,16), or the increase in stiffness noted by Gosselin and others (17–19), increased the mechanical demand on old skeletal muscle. More intramuscular connective tissue would increase passive tension at shorter muscle lengths. In vitro mechanical stimulation can stimulate muscle cell growth (20). Potentially, passive tension was the stimulus for the increase in muscle strength that occurred, but further study is indicated to explore this possibility.
If the stimulus for change in muscle mass and strength is different in an old organism, microarray studies would help elucidate this distinction. There is already evidence for a differential effect of exercise in old versus young human subjects. Roth and colleagues recently resistance-trained young and older (aged 65–75 years) men and women and found 5% of the 1000 genes expressed above background to be different with age (21). The functional significance of this finding is unclear at this time, but age-associated differences were observed in structural, metabolic, and regulatory domains.
The increase in peak tetanic tension in old exercise rats was consistent with the increase in muscle mass for all but the plantaris muscle. Po went up 23% whereas muscle mass increased 11%. This finding may indicate that factors other than quantity of contractile protein were responsible for the improvement in contractile tension. Possibilities include enhanced Ca++ release from the sarcoplasmic reticulum with exercise (22) or an increase in tension produced per cross-bridge (23). Studies to amplify specific individual muscle changes with exercise in an aging organism are needed.
Whether exercise resulted in an increase in muscle mass secondary to damage and swelling should be addressed, since muscle from an older organism is more susceptible to exercise-induced damage (24). Findings do not support the possibility of damage for two reasons. First, the increase in muscle mass was associated with a concomitant increase in peak tetanic tension. The ratio of Po to muscle mass remained constant before and after exercise. Second, the exercise resulted in functional (gait) improvements as well. Stride length would not likely improve if animals were using muscles that were painful and sore.
The rapid increase in muscle mass and strength was matched by an equally rapid improvement in stride and step length. Whether changes in gait were directly associated with the observed strength increases is not known, but studies of older adults suggest a relationship between gait speed and muscle force (25). Whether strength had to change before functional differences could occur, suggesting a strength "threshold," is not known. The rapid modification in strength and function seem to indicate that both changed simultaneously. The increase in stride and step length could be the consequence of improved motor control if rats were as sedentary as suspected. This result has rehabilitation overtones, as there are few opportunities to intervene for much longer than 2 weeks for elders who are deconditioned and have muscle weakness.
Studies of resistance exercise effects on old rats have not been particularly encouraging. Tamaki and colleagues, for example, found protein synthesis and proliferative capacity in response to one bout of exhaustive resistance exercise to be decreased in old versus young rats (26). When synergist ablation is performed, old rats do not show the marked increase in muscle mass that young rats do (27). Findings for older adults, however, do not support a reduced adaptive response to weightlifting exercise. Two weeks and 3 months of resistance exercise were both found to increase the fractional rate of muscle protein synthesis and synthetic rate of myosin heavy chain (28). Using imaging techniques, muscle volume increases have been noted following 8–12 weeks of resistance exercise even in very old adults, suggesting that an adaptive response to exercise is intact at all ages (1,2). Findings from this study support the observations made in older humans and support the hypothesis that adaptive potential remains intact in an older organism. Because injury can occur more readily in an old versus young muscle, perhaps some of the discordance in the literature is due to the potential confound of injury (24).
The reduction in contractile function in the old controls occurred both with and without a concomitant reduction in total protein. The increase in muscle contractile force with exercise also occurred with and without a corresponding change in total protein concentration. This observation is consistent with previous findings that total protein content does not reflect age-related changes in proportion of contractile and noncontractile protein. There is evidence for a reduction in myosin heavy chain with age, and examining total quantity of myosin may be a more-sensitive measure to identify changes in contractile function than total protein (29,30). Given a 7–10-day half-life of myosin heavy chain and the significant increases in peak muscle force, any increase in contractile protein was likely obscured by the total protein values.
In summary, 10 sessions of modest exercise resulted in a partial reversal of age-associated declines in muscle mass and contractile function. The improvement in contractile function was associated with an increase in gait stride and step length, which further supports the efficacy of exercise for an aged organism. Results also suggest that the stimulus required to promote positive change in old skeletal muscle differs from that required for a younger organism.
|
Acknowledgments
|
|---|
This study was funded by National Institute on Aging grant AG15796.
Address correspondence to Marybeth Brown, PT, PhD, Physical Therapy Program, University of Missouri-Columbia, 106 Lewis Hall, Columbia MO 65211. E-mail: brownmb{at}health.missouri.edu
|
Footnotes
|
|---|
Decision Editor: James R. Smith, PhD
Received May 5, 2003
Accepted May 8, 2003
|
References
|
|---|
- Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians: effects on skeletal muscle. JAMA.. 1990;263:3029-3034.[Abstract]
- Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol.. 1988;64:1038-1044.[Abstract/Free Full Text]
- Sullivan DH, Wall PT, Bariola JR, Bopp MM, Frost YM. Progressive resistance muscle strength training of hospitalized frail elderly. Arch Phys Med Rehabil.. 2001;80:503-509.
- Fiatarone MA, O'Neill EF, Ryan ND, et al. Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med.. 1994;330:1769-1775.[Abstract/Free Full Text]
- Lord SR, Castell S. Physical activity program for older persons: effect on balance, strength, neuromuscular control, and reaction time. Arch Phys Med Rehabil.. 1998;75:648-652.
- Chandler JM, Duncan PW, Korchersberger G, Studenski S. Is lower extremity strength gain associated with improvement in physical performance and disability in frail, community-dwelling elders? Arch Phys Med Rehabil.. 1998;79:24-30.[Medline]
- Binder EF, Brown M, Craft S, Schechtman KB, Birge SJ. Effects of a group exercise program on risk factors for falls in frail older adults. J Aging Phys Activ.. 1994;2:25-37.
- Moritani T, deVries HA. Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med.. 1979;58:115-130.[Medline]
- Cannon RJ, Cafarelli E. Neuromuscular adaptations to training. J Appl Physiol.. 1987;63:2396-2402.[Abstract/Free Full Text]
- Brown M, Hasser E. Complexity of age-related change in skeletal muscle. J Gerontol Biol Sci.. 1996;51A:B117-B123.
- Baldwin KM, Haddad F. Skeletal muscle plasticity: cellular and molecular responses to altered physical activity paradigms. Am J Phys Med Rehabil.. 2002;81:(Suppl): S40-S51.[Medline]
- Holloszy JO, Smith EK. Effects of exercise on longevity of rats. Fed Proc.. 1987;46:1850-1853.[Medline]
- Goodrick CL. Effects of long-term voluntary wheel exercise on male and female Wistar rats. I. Longevity, body weight and metabolic rate. Gerontology.. 1980;26:22-33.[Medline]
- Brown M, Ross TP, Holloszy JO. Effects of ageing on soleus and extensor digitorum longus muscles of female rats. Mech Ageing Devel.. 1992;63:69-77.[Medline]
- Buhl KM, Jacobs CR, Turner RT, Evans GL, Farrell PA, Donahue HJ. Aged bone displays an increased responsiveness to low-intensity exercise. J Appl Physiol.. 2001;90:1359-1364.[Abstract/Free Full Text]
- Inokuchi S, Ishikawa H, Iwamoto S, Kimura T. Age-related changes in the histological composition of the rectus abdominus muscle of the adult human. Hum Biol.. 1975;47:231-239.[Medline]
- Gosselin LE, Adams C, Cotter TA, McCormick RJ, Thomas DP. Effect of training on passive stiffness in locomotor skeletal muscle: role of extracellular matrix. J Appl Physiol.. 1998;85:1011-1016.[Abstract/Free Full Text]
- Blanpied P, Smidt GL. The difference in stiffness of the active plantar flexors between young and elderly human females. J Gerontol.. 1993;48:M58-M63.[Medline]
- Gajdosik RL, Vander Linden DW, Williams AK. Influence of age on concentric isokinetic torque and passive extensibility variables of the calf muscles of women. Eur J Appl Physiol Occup Physiol.. 1996;74:279-284.[Medline]
- Vandenburgh HH. Mechanical forces and their second messengers in stimulating cell growth in vitro. Am J Physiol.. 1992;262:R350-355.
- Roth SM., Ferrell RE, Peters DG, Metter EJ, Hurley BF, Rogers MA. Influence of age, sex and strength training on human muscle gene expression determined by microarray. Physiol Genomics.. 2002;10:181-190.[Abstract/Free Full Text]
- Klitgaard H, Ausoni S, Damiani E. Sarcoplasmic reticulum of human skeletal muscle: age-relatead changes and effect of training. Acta Physiol Scand.. 1989;137:23-31.[Medline]
- Lowe DA, Thomas DD, Thompson LV. Force generation, but not myosin ATPAse activity, declines with age in rat muscle fibers. Am J Physiol Cell Physiol.. 2002;283:C187-C192.[Abstract/Free Full Text]
- Brooks S, Faulkner JA. Skeletal muscle weakness in old age: underlying mechanisms. Med Sci Sport Exerc.. 1993;26:432-439.
- Brown M, Sinacore DR, Host HH. The relationship of strength to function in the older adult. J Gerontol.. 1995:;50A:55-59.
- Tamaki T, Uchiyama S, Uchiyama Y. Limited myogenic response to a single bout of weight-lifting exercise in old rats. Am J Physiol.. 2000;278:C1143-1152.
- Tomanek RJ, Woo YK. Compensatory hypertrophy of the plantaris muscle in relation to age. J Gerontol.. 1972;25:23-29.
- Schulte JN, Yarasheski KE. Effects of resistance training on the rate of muscle protein synthesis in frail elderly people. Int J Sport Nutr Exerc Metab.. 2001;11:(Suppl): S111-S118.
- Larsson L, Li X, Yu F, Degens H. Age-related changes in contractile properties and expression of myosin isoforms in single skeletal muscle cells. Muscle Nerve.. 1998;Suppl 5:S74-S78.
- Balagopal P, Rooyackers OE, Adley DOB, Ades PA, Nair KS. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am J Physiol.. 1997;273:E790-E800.
Top
Abstract
Methods
