Muscle function in 164 men and women aged 20–84 yr : Medicine & Science in Sports & Exercise (original) (raw)
It is well established that muscle strength and mass decrease with aging (7,8,14–16,28), and it has also been suggested that there are age-associated differences in muscle strength and force generating capacity, i.e., muscle force per unit of cross-sectional area (CSA) in some literature (9,11,17,20,31,32). For example, Frontera et al. (11) showed that, when isokinetic torque at the knee and elbow joints were adjusted to take into account muscle mass, no significant age-related differences were observed in any muscle groups, with the exception of the knee extensor muscles when tested at 240°·s-1. Young et al. (31,32) reported that, when compared with younger individuals, elderly individuals exhibited a lower maximum voluntary contraction (MVC) during knee extension and CSA of the quadriceps femoris (QF) muscle in both men and women. They further demonstrated that MVC to CSA ratios (MVC/CSA) for younger individuals were greater than those of elderly men but not women. Recently, Lindle et al. (24) showed that isokinetic concentric and eccentric knee extension strength decreased with aging. Furthermore, they demonstrated that muscle quality, determined as the peak torque during concentric and eccentric knee extension divided by thigh fat-free mass, also declined with aging.
Reductions in strength associated with advancing age are likely to be the result of quantitative and/or qualitative losses in skeletal muscles (9,11,17,20,27,31,32). Thus, although the studies outlined above have focused on changes in muscle strength and mass with advancing age, they fall short insofar as they employed only very crude estimates of muscle size, and they evaluated only a small range of age groups. To resolve these problems, we thus determined muscle size using a high resolution imaging technique, i.e., magnetic resonance (MR) imaging, in conjunction with measurements of muscle strength over a wide subject age-range. Therefore, the purpose of this study was to investigate muscle functional characteristics of the knee extensor and flexor muscles in 164 men and women aged from 20 to 84 yr.
METHODS
Subjects.
A total of 164 volunteers participated in this study. The procedures, purpose, and risks associated with the study were explained to all subjects, then we gave their written informed consent to participate in this investigation before starting of this project. They have no knee malfunction, back pain, hip pain sciatica, or abnormalities of skeletal muscles. Before the knee joint torque measurement, all subjects were measured their resting blood pressure under the supervision of a physician. When subjects who had higher blood pressure than their normal resting blood pressure was observed, they were judged by the physician to perform strength measurements. Because maximum knee joint torque measurement would induce increase in blood pressure. They were divided five groups: 20s (20–39 yr old), 40s (40–49 yr old), 50s (50–59 yr old), 60s (60–69 yr old), and 70s (70–84 yr old) depending on their chronological age (Table 1).
Physical characteristics of subjects.
MR imaging measurement.
MR imaging was collected by using a 1.5-T superconducting magnet (Signa MR Systems, General Electric Medical Systems, Waukesha, WI) with a body coil in supine position. Pillows were used under the subjects’ feet and buttocks to minimize any tissue compression in the thigh. We performed MR imaging and calculation of CSA of the QF according to our previous studies (3–6). In briefly, coronal images were taken to identify the anatomical markers, i.e., greater trochanter and the distal end of femur, and axial image (TR 900 ms, TE 20 ms, matrix 256 × 192, field of view 18 cm, slice thickness 10 mm, interslice gap 0 mm) of the right-thigh was taken at the center of two anatomical markers. Outlines of the QF according to a standard anatomical textbook (10) were traced using axial MR images. Traced images were transferred to a Macintosh computer (Power Macintosh 8600/200, Apple Computer, Cupertino, CA) for calculation of the CSA using a public domain National Institute of Health (NIH) image software package ver1.60/ppc (written by Wayne Rasband at the NIH and available from the Internet by anonymous ftp from zippy.nimh.nih.gov) after spatial calibration.
Peak torque measurements.
Peak torque during isometric (0°·s-1) and isokinetic knee extension and flexion at 60, 180, and 300°·s-1 were measured by using an isokinetic dynamometer (Cybex 770-NORM). The knee joint torque measurements were performed according to our previous studies (3,4,6). Calibration was performed before each testing session according to the Cybex systems. Subjects warmed up by light exercise such as walking and running for about 5 min and performed several stretching exercises for the knee extensor and flexor muscles before performing any of the strength tests. The subjects were stabilized during practice and testing via straps to the chest, hips, and middle of the thigh. Great care was taken to align the anatomical axis of the joint with the mechanical axis of the dynamometer before the tests. Knee extension and flexion torque measurement was performed separately at all conditions; thus, eight testing conditions were done: knee extension and flexion at 0, 60, 180, 300°·s-1, respectively. Two to four trials were performed before testing, and then three maximal voluntary knee extensions or flexions were performed to determine peak torque in the range of joint angles between 0° (full extension) and 90° (flexed position). The knee joint angle during isometric knee extension and flexion measurement was 80° and 40°, respectively. Two maximum contractions were performed during 4 s for isometric knee extension or flexion. Avoiding from repetitive maximum effort-induced high blood pressure, especially for elderly subjects, we chose “two repetitions” of maximum efforts for measuring isometric torque measurements. The torque was corrected for gravitational moments of the lower leg and the lever arm. A rest period of approximately a few minutes was allowed between trials to exclude the effect of fatigue.
To facilitate comparisons of muscle force to CSA ratio (force/CSA) with some previous studies, isometric knee extension peak torque in Newton meters (Nm) were converted to Newtons (N) by dividing by the length of the lower leg (m) of each subject (18,19).
Statistical analysis.
An analysis of variance (ANOVA) was used to compare age groups and gender differences in physical characteristics (height and body weight), knee joint torque. When a difference was found, a Scheffé’s post hoc test was used to determine the specific comparisons that were significant. Regression analysis was used to assess age-related relative peak torque and force/CSA changes. All statistical analysis was performed using Statview software for Macintosh computer. Values of P < 0.05 were considered to be statistically significant.
RESULTS
Table 1 shows physical characteristics of subjects. The subjects of 60s and 70s in men and women were significantly smaller than those of 20s (all P < 0.01), and the subjects of 60s and 70s in men were significantly lighter than those of 20s (both P < 0.01).
Figure 1 shows that age-associated peak torque change during isokinetic knee extension. Knee extension torque at all angular velocities in men and women gradually decreased associated with aging. In men, isokinetic peak torque during knee extension at all tested the velocities in 40s, 50s, 60s, and 70s was significant lower than that in 20s. In women, isokinetic peak torque during knee extension at almost all tested the velocities (0, 60, and 180°·s-1) in 40s, 50s, 60s, and 70s was lower than that in 20s.
Age-associated peak torque during isokinetic knee extension in men and women. * P < 0.05; ** P < 0.01; #P < 0.001 vs 20s.
Figure 2 shows that age-associated peak torque change during isokinetic knee flexion. Knee flexion torque at all tested the velocities in men and women gradually decreased associated with aging. In men, isokinetic peak torque during knee flexion at all tested the velocities in 60s and 70s was significantly lower than that in 20s. In women, isokinetic peak torque during knee flexion at almost all tested the velocities (0, 60, and 180°·s-1) in 60s and 70s was lower than that in 20s.
Age-associated peak torque during isokinetic knee flexion in men and women. * P < 0.05; ** P < 0.01; #P < 0.001 vs 20s.
Regression analysis of age-associated decline of peak torque during isokinetic knee extension in men and women expressed as a percentage of the mean of 20s are shown in Figure 3. Significant age-related torque losses for men and women were observed in knee extension at all tested the velocities. Correlation coefficients age-related knee extension torque losses at 0, 60, 180, and 300°·s-1 were r = −0.826 (P < 0.001), −0.832 (P < 0.001), −0.844 (P < 0.001), and −0.818 (P < 0.001) in men, and r = −0.518 (P < 0.001), −0.688 (P < 0.001), −0.640 (P < 0.001), and −0.562 (P < 0.001) in women, respectively. Regression analysis of age-associated decline of peak torque during isokinetic knee flexion in men and women expressed as a percentage of the mean of 20s are shown in Figure 4. Correlation coefficients age-related knee flexion torque losses at 0, 60, 180, and 300°·s-1 were r = −0.761 (P < 0.001), −0.697 (P < 0.001), −0.758 (P < 0.001), and −0.732 (P < 0.001) in men, and r = −0.726 (P < 0.001), −0.597 (P < 0.001), −0.631 (P < 0.001), and −0.501 (P < 0.001) in women, respectively. The slope of regression line is considered to be % decline in knee extension and flexion torque per year associated with aging. In all tested the velocities, the percentage decline per decade in knee extension torque in men and women was approximately 12% and 8%, respectively, and that in knee flexion torque in men and women was approximately 11% and 8%, respectively.
Regression analysis of age-associated decline of peak torque during isokinetic knee extension in men and women, represented as a percentage of mean of 20s. Solid lines, men;dotted lines, women.
Regression analysis of age-associated decline of peak torque during isokinetic knee flexion in men and women, represented as a percentage of mean of 20s. Solid lines, men;dotted lines, women.
There was a significant correlation between CSA of QF and maximum knee extension torque (0°·s-1) in men (r = 0.827, P < 0.001) and women (r = 0.657, P < 0.001).
Figure 5 shows that age-associated change in isometric knee extension force per unit of CSA (force/CSA) in men and women. Force/CSA decreased with advanced aging in men (r = −0.597, P < 0.001) but not in women (r = −0.207, NS).
Regression analysis of age-associated difference in force per unit of cross-sectional area (CSA) during isometric knee extension in men and women. •, men; ○, women.
DISCUSSION
Many studies have been reported that muscle function such as peak torque and force per unit of CSA in elderly individuals. However, most of such studies focused either solely on muscle strength or were performed using only rough measurements of muscle size on a narrow age-range (e.g., young vs old). As such, only a few studies have attempted to determine muscle function, e.g., peak torque and force/CSA, on a wide range of ages.
We found in this study that knee extension and flexion torque at all the tested velocities decreased with aging in both sexes. This agrees with previous studies by Larsson et al. (21), who reported that a decline in QF muscle strength commencing in the 50s group, and by Vandervoort and McComas (30), who likewise reported a decrease in voluntary plantarflexors and dorsiflexors torque commencing at 52 yr of age. Recently, Lindle et al. (24) showed that age-associated concentric (30°·s-1) strength losses begin to manifest in the 40s in both sexes. In the present study, knee extensors and flexors torque, at all the tested velocities, decreased linearly with aging in both sexes. Our results thus differ from those of previous studies that evaluated age-related human muscle strength. However, in this study, a significant relationship was observed between CSA of QF and the peak torque at 0°·s-1 in both sexes, thus supporting the notion of a linear decline in muscle strength with advancing age. Therefore, our results imply that muscle mass is the primary factor involved in an aged individual’s capacity to exert maximum force.
The strength losses associated with aging were observed under isometric and isokinetic conditions from low to high velocities. As shown in Figures 3 and 4, the linear regression slopes for knee extension and flexion, within 0–300°·s-1, were very similar in both sexes. This suggests that the effect of aging on the peak torque exerted during knee extension and flexion is likely to be very similar at low (including isometric contraction) to high angular velocities. Several studies have shown a preferential atrophy of Type II fibers with advancing age (20,23,28). Moreover, some studies have demonstrated that a significant correlation between muscle strength and either % Type II fibers or % area Type II fibers, with the correlation being higher at faster angular velocities (3,29). However, in spite of the selective reduction in the size and number of Type II fibers with advancing age reported in previous studies, such changes appear to have little affect on the peak torque. Thus, in this study, fiber types and/or fiber area are unlikely to be the main factors that determine peak torque during isometric and isokinetic knee extension and flexion in elderly men and women in this study.
Relatively few studies on force/CSA in elderly people have been reported (9,11,17,20,27,31,32). Young et al. (32) demonstrated that the force/CSA of the QF in elderly men was lower than that of younger men, however, reported that no differences between elderly and young women. In contrast, Overend et al. (26) reported no significant differences in the force/CSA of the QF when comparing between elderly and young men. In the present study, the force/CSA decreased linearly with increasing age in men; however, no age-related decreases in force/CSA were observed in women. Thus, our results in part support those of Young et al. (31,32) and further suggest that several factors contribute to age-related decline in force/CSA in men. Such factors fall into four categories as described below.
First, muscle recruitment of the QF during isometric and isokinetic contraction is a contributing factor. Recently, several studies have reported on muscle recruitment following a set exercise as detected by exercise-induced contrast shift in MR imaging (1,4). Adams et al. (1) suggested that only 71% of the CSA in the QF was activated during knee extension exercise, when induced by electrical stimulation to generate maximal isometric voluntary contraction force. Their results thus imply that 29% of CSA of QF may not be activated, even during electrical-induced maximum force. In our previous study, we reported that 13–16% increases in peak torque during isokinetic knee extension (0–240°·s-1) after only 2 wk of resistance training. Moreover, this increase in peak torque was accompanied by greater muscle recruitment (as determined by exercise-induced contrast shift in MR images) without hypertrophy of either the CSA of the QF, or the muscle fiber area in the vastus lateralis muscle (VL) in the trained leg (4). Furthermore, Moritani and deVries (25) demonstrated that 8 wk of resistance training induced muscle strength gain in elderly subjects, with neural factors mainly contributing to the strength gain throughout the training period. This suggests that elderly individuals have a greater trainability by resistance training-induced facilitation through neural factors. Taking these observations together, muscle recruitment would appear to have a substantial effect on the capacity to exert maximum muscle force.
Second, muscle architectural factors may have an effect on the force/CSA change associated with aging. In this study, the CSA was calculated from single slice images, and thus this CSA can be considered to be an anatomical CSA but not a physiological CSA. It has been demonstrated that the physiological CSA reflects its force production potential, and it can be derived from the following equation (4,5,11),MATHMATH
No association is apparent between fiber length and aging and thus physiological CSA would be affected by muscle volume and/or pennation angle of the muscle. The pennation angle of the VL at a knee joint angle of 80° (0°: full extension) in sedentary men was found to be 15°(13). Abe et al. (3) and Akima et al. (5) reported that pennation angle and muscle volume changes in the VL was found after 20 d of bed rest in 10 healthy men and women. The muscle volume in the VL decreased by 7.3%, however, no change was noted in pennation angle (pre: 16.5°, post: 16.9°) in the VL. Thus, it appears that changes in muscle size and pennation angle do not always occur simultaneously. In the atrophic or aged VL, the pennation angle decreased by about 5° compared with the young VL (Y. Kawakami, Ph.D., The University of Tokyo, personal communication). Hence, from the results of these findings (2), the aged muscle pennation angle can be calculated as approximately 12°, with the cosine of 12° being 0.98. This, therefore, implies that 98% of the force exerted by the individual muscle fibers would thence be transferred to the tendon; there is only a minuscule loss of the force exerted by the muscle. Therefore, the pennation angle does not appear to be a major factor affecting the age-related decline in force/CSA. From the above observations, muscle volume would appear to be the main factor affecting changes in physiological CSA associated with aging. However, thus far, there have been very few studies detailing muscle volume in the elderly. From our previous studies, % change in muscle CSA and volume in human thigh and leg muscles is similar, whether the results of sprint training (% changes in CSA; 8% and % changes in muscle volume; 6%) or after bed rest (% changes in CSA; −7%, % changes in muscle volume; −7%) (5,6). These data imply that age-related CSA changes would likely be reflected in muscle volume changes.
Third, nonmuscle tissue such as connective tissue might have an effect on the force/CSA. Skeletal muscle of elderly persons exhibits a greater proportion of nonmuscular tissue compared to that of younger subjects. Overend and colleagues (26) calculated nonmuscle tissue of the QF in a single slice of the mid-thigh image in young and elderly subjects to be 3.2 and 5.5 cm2, respectively. This nonmuscle tissue CSA was relatively lower in order to explain the aging related decline in force/CSA in men but not women.
Fourth, qualitative changes in contractile properties might be associated with age-related changes in force/CSA. Larsson et al. (22) reported that a significant decrease in the specific tension of single Type I and IIa fibers, characterized according to expression of myosin heavy chain of the VL, in young, elderly, and very physical elderly subjects. They determined the maximum tension per unit of CSA, i.e., specific tension, in Type I or IIa fibers and found that the specific tension of these fibers in young subjects was significantly higher than those of both elderly and very physical elderly subjects. Taking into account the study of Larsson et al. study, the force/CSA in aging men observed in this study may thus be due to a decline in the intrinsic muscle force potential.
With regard to sex-specific difference in force/CSA associated with aging, we have no data to support the result of the above study. However, the values of force/CSA in young and elderly women of 7.1 and 7.2 N·cm-2, respectively, reported herein are comparable to the force/CSA of the QF in young and elderly women of 7.1 and 6.9 N·cm-2, respectively, reported by Young et al. (31). In addition, the force/CSA in two age groups were also similar to those reported by Young et al. (32). Recently, Jubrians et al. (17) demonstrated that force/CSA during isokinetic contraction in the QF declined with age and declined by about 1.5% per year in 23- to 80-yr-old men and women. If one calculates the age-related force/CSA for all subjects in this study, a significant decline (y = 3.707–0.019x, r = −0.470, P < 0.001, data are not shown) in force/CSA is also observed. This represents a force/CSA decline of 1.9% per year from 20- to 84-yr-old subjects in this study, a value that is very similar to that reported by Jubrians et al. (17). The present study does not clarify the mechanisms behind the observed sex-specific decline in age-related force/CSA, and thus further studies will be required to elucidate this effect.
In summary, we investigated the effect of aging on muscle functional characteristics, i.e., peak torque and force/CSA, in 164 men and women aged 20-84, and we report that knee extension and flexion torque, under isometric and isokinetic conditions, decreased with aging in both sexes. A significant correlation was observed between CSA of QF and peak torque during isometric knee extension in men (r = 0.827, P < 0.001) and women (r = 0.657, P < 0.001). Furthermore, although the force/CSA decreased with aging in men, this was clearly not the case in women. These results thus suggest that muscle strength losses would be mainly due to a decline in muscle mass in both sexes whereas age-related decline in muscle function in men may also be the result of neural factors such as muscle recruitment and/or specific tension.
This study was supported by Basic Research for Life & Society. The special coordination funds for Promoting Science & Technology (SCF) and STA were partly supported by Descente Sports Promotion.
Address for correspondence: Hiroshi Akima, Ph.D., Department of Life Sciences (Sports Sciences), Graduate School of Arts and Sciences, The University of Tokyo, Komaba 3-8-1, Meguro, Tokyo 153-8902, Japan; E-mail; [email protected].
REFERENCES
1. Adams, G. R., R. T. Harris, D. Woodard, and G. A. Dudley. Mapping of electrical muscle stimulation using MRI. J. Appl. Physiol. 74: 532–537, 1993.
2. Abe, T., Y. Kawakami, Y. Suzuki, A. Gunji, and T. Fukunaga. Effects of 20 days bed rest on muscle morphology. J. Gravitat. Physiol. 4: S10–S14, 1997.
3. Akima, H., S. Kuno, H. Takahashi, H. Shimojo, and S. Katsuta. Effect of the different parts of cross-sectional areas in four heads of quadriceps femoris and muscle fiber composition on isokinetic knee extension. Jpn. J. Phys. Educ. 39:417–427, 1995 (in Japanese with English abstract).
4. Akima, H., H. Takahashi, S. Kuno, et al. Early phase adaptations of muscle use and strength to isokinetic training. Med. Sci. Sports Exerc. 31: 588–594, 1999.
5. Akima, H., S. Kuno, Y. Suzuki, A. Gunji, and T. Fukunaga. Effects of 20 days of bed rest on physiological cross-sectional area of human thigh and leg muscles evaluated by MRI. J. Gravitat. Physiol. 4: S15–S22, 1997.
6. Akima, H., S. Kuno, M. Inaki, H. Shimojo, and S. Katsuta. Effects of sprint cycle training on architectural characteris-tics, torque-velocity relationships, and power output in hu-man skeletal muscles. Adv. Exerc. Sports Physiol. 3: 9–15, 1997.
7. Aniansson, A., G. Grimby, and A. Rundgren. Isometric and isokinetic quadriceps muscle strength in 70-year-old men and women. Scand. J. Rehabil. Med. 12: 161–168, 1980.
8. Cunningham, D. A., D. Morrison, C. L. Rice, and C. Cooke. Aging and isokinetic plantar flexion. Eur. J. Appl. Physiol. 56: 24–29, 1987.
9. Davies, C. T., D. O. Thomas, and M. J. White. Mechanical properties and elderly human muscle. Acta Med. Scand. Suppl. 711: 219–226, 1986.
10. El-Khoury, G. Y., R. A. Bergman, and W. J. Montgomery. Sectional anatomy by MRI/CT. New York: Churchill Livingstone, 1990, pp. 505–518.
11. Frontera, W., V. A. Hughes, K. J. Lutz, and W. J. Evans. A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J. Appl. Physiol. 71: 644–650, 1991.
12. Fukunaga, T., R. R. Roy, F. G. Shellock, et al. Physiological cross-sectional area of human leg muscles based on MRI. J. Orthop. Res. 10: 926–934, 1992.
13. Fukunaga, T., Y. Ichinose, M. Ito, Y. Kawakami, and S. Fukashiro. Determination of fascicle length in contracting human muscle in vivo. J. Appl. Physiol. 82: 354–358, 1997.
14. Grabiner, M. D., and R. M. Enoka. Changes in movement capabilities with aging. In:Exercise and Sport Sciences Reviews, J. O. Holloszy (Ed.). Baltimore: Williams & Wilkins, 1995, pp. 65–104.
15. Harries, U. J., and E. J. Bassey. Torque-velocity relationships for the knee extensors in women in their 3rd and 7th decades. Eur. J. Appl. Physiol. 60: 187–190, 1990.
16. Holloszy, J. O., and W. M. Kohrt. Exercise. In:Handbook of Physiology, E. J. Masoro (Ed.). New York: American Physiological Society, 1996, pp. 633–666.
17. Jubrians, S. A., I. R. Odderson, P. C. Esselman, and K. E. Conley. Decline in isokinetic force with age: muscle cross-sectional area and specific force. Pflügers Arch. 434: 246–253, 1997.
18. Kanehisa, H., I. Nemoto, H. Okuyama, S. Ikegawa, and T. Fukunaga. Force generation capacity of knee extensor muscles in speed skaters. Eur. J. Appl. Physiol. 73: 544–551, 1996.
19. Kanehisa, H., and T. Fukunaga. Velocity associated characteristics of force production in college weight lifters. Br. J. Sports Med. 33: 116–116, 1999.
20. Klitgaard, H., M. Mantoni, S. Schiaffino, et al. Function, morphology and protein expression of aging skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol. Scand. 140: 41–54, 1990.
21. Larsson, L., G. Grimby, and J. Karlsson. Muscle strength and speed of movement in relation to age and muscle morphology. J. Appl. Physiol. 46: 451–456, 1979.
22. 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.
23. Lexell, J., C. C. Taylor, and M. Sjöström. What is the cause of the aging atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J. Neurol. Sci. 84: 275–294, 1988.
24. Lindle, R. S., E. J. Metter, N. A. Lynch, et al. Age and gender comparisons of muscle strength in 654 women and men aged 20–93 yr. J. Appl. Physiol. 83: 1581–1587, 1997.
25. Moritani, T., and H. A. deVries. Neural factors versus hypertrophy in the time course of muscle strength gains. Am. J. Phys. Med. 82: 521–524, 1979.
26. Overend, T. J., D. A. Cunningham, J. F. Kramer, M. S. Lefcoe, and D. H. Paterson. Knee extensor and knee flexor strength: cross-sectional area rations in young and elderly men. J. Gerontol. 47: M204–M210, 1992.
27. Phillips, S. K., S. A. Bruce, D. Newton, and C. Woledge. The weakness of old age is not due to muscle activation. J. Gerontol. 47: M45–M49, 1992.
28. Rogers, M. A., and W. J. Evans. Changes in skeletal muscle with aging: Effects of exercise training. In:Exercise and Sport Sciences Reviews, J. O. Holloszy (Ed.). Baltimore: Williams & Wilkins, 1993, pp. 65–102.
29. Thorstensson, A., G. Grimby, and J. Karlsson. Force-velocity relations and fiber composition in human knee extensor muscles. J. Appl. Physiol. 40: 12–16, 1976.
30. Vadervoort, A. A., and A. J. Mccomas. Contractile changes in opposing muscles of the human ankle joint with aging. J. Appl. Physiol. 61: 361–367, 1986.
31. Young, A., M. Stokes, and M. Crowe. Size and strength of the quadriceps muscles of old and young women. Eur. J. Clin. Invest. 14: 282–287, 1984.
32. Young, A., M. Stokes, and M. Crowe. The size and strength of the quadriceps muscles of old and young men. Clin. Physiol. 5: 145–154, 1985.
Keywords:
MUSCLE STRENGTH,; SKELETAL MUSCLE,; AGING,; HUMAN,; MAGNETIC RESONANCE IMAGING
© 2001 Lippincott Williams & Wilkins, Inc.