ART 1 Akima
ART 1 Akima
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ABSTRACT
AKIMA, H., Y. KANO, Y. ENOMOTO, M. ISHIZU, M. OKADA, Y. OISHI, S. KATSUTA, and S-Y. KUNO. Muscle function in
164 men and women aged 20 – 84 yr. Med. Sci. Sports Exerc., Vol. 33, No. 2, 2001, pp. 220 –226. Purpose: The purpose of the present
study was to investigate the effect of aging in men and women on muscle functional properties, i.e., muscle force and force per unit
of cross-sectional area (force/CSA). Methods: A total of 164 volunteers participated in this study and were divided into five groups
according to their chronological age as follows: 20s (20-39 yr old), 40s, 50s, 60s, and 70s (70-84 yr old). Isokinetic (0, 60, 180, and
300°䡠s-1) knee extensor and flexor peak torque, and CSA of the quadriceps femoris (QF) muscle of the mid-thigh were measured.
Results: Peak torque during knee extension and flexion was inversely related to age in both men and women. This was the case
irrespective of the speed of contraction in both genders (men: r ⫽ ⫺0.797 to ⫺0.756, all P ⬍ 0.001, women: r ⫽ ⫺0.639 to ⫺0.530,
all P ⬍ 0.001). 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). During isometric contraction, the force/CSA exhibited a significant decrease
with increasing age in men (r ⫽ ⫺0.518, P ⬍ 0.001) but not in women (r ⫽ ⫺0.207, NS). Conclusion: These results thus suggest
that muscle strength losses would be mainly due to a decline in muscle mass in both genders, 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. Key Words: MUSCLE
STRENGTH, SKELETAL MUSCLE, AGING, HUMAN, MAGNETIC RESONANCE IMAGING
I
t is well established that muscle strength and mass They further demonstrated that MVC to CSA ratios (MVC/
decrease with aging (7,8,14 –16,28), and it has also been CSA) for younger individuals were greater than those of
suggested that there are age-associated differences in elderly men but not women. Recently, Lindle et al. (24)
muscle strength and force generating capacity, i.e., muscle showed that isokinetic concentric and eccentric knee exten-
force per unit of cross-sectional area (CSA) in some litera- sion strength decreased with aging. Furthermore, they dem-
ture (9,11,17,20,31,32). For example, Frontera et al. (11) onstrated that muscle quality, determined as the peak torque
showed that, when isokinetic torque at the knee and elbow during concentric and eccentric knee extension divided by
joints were adjusted to take into account muscle mass, no thigh fat-free mass, also declined with aging.
significant age-related differences were observed in any Reductions in strength associated with advancing age are
muscle groups, with the exception of the knee extensor likely to be the result of quantitative and/or qualitative
muscles when tested at 240°䡠s-1. Young et al. (31,32) re- losses in skeletal muscles (9,11,17,20,27,31,32). Thus, al-
ported that, when compared with younger individuals, el-
though the studies outlined above have focused on changes
derly individuals exhibited a lower maximum voluntary
in muscle strength and mass with advancing age, they fall
contraction (MVC) during knee extension and CSA of the
short insofar as they employed only very crude estimates of
quadriceps femoris (QF) muscle in both men and women.
muscle size, and they evaluated only a small range of age
0195-9131/01/3302-0220/$3.00/0
groups. To resolve these problems, we thus determined
MEDICINE & SCIENCE IN SPORTS & EXERCISE® muscle size using a high resolution imaging technique, i.e.,
Copyright © 2001 by the American College of Sports Medicine magnetic resonance (MR) imaging, in conjunction with
Received for publication May 1999. measurements of muscle strength over a wide subject age-
Accepted for publication May 2000. range. Therefore, the purpose of this study was to investi-
220
TABLE 1. Physical characteristics of subjects.
20s (20–39 yr) 40s (40–49 yr) 50s (50–59 yr) 60s (60–69 yr) 70s (70–84 yr)
Men N ⫽ 28 N ⫽ 10 N⫽9 N ⫽ 26 N ⫽ 17
Age (yr) 30.2 ⫾ 6.1 44.6 ⫾ 2.9 56.8 ⫾ 1.7 64.3 ⫾ 3.1 75.1 ⫾ 4.1
Height (cm) 169.8 ⫾ 5.7 166.0 ⫾ 3.1 162.2 ⫾ 6.0 159.3 ⫾ 3.4** 159.4 ⫾ 5.4**
Weight (kg) 73.2 ⫾ 15.0 67.0 ⫾ 8.4 67.7 ⫾ 7.4 61.0 ⫾ 9.7** 58.5 ⫾ 7.8**
Women N⫽5 N⫽6 N ⫽ 21 N ⫽ 31 N ⫽ 16
Age (yr) 26.4 ⫾ 4.3 47.3 ⫾ 2.3 56.2 ⫾ 2.5 64.1 ⫾ 2.8 74.4 ⫾ 3.7
Height (cm) 157.6 ⫾ 3.6 154.4 ⫾ 6.0 152.1 ⫾ 4.5 149.7 ⫾ 6.5** 144.4 ⫾ 4.8**
Weight (kg) 52.7 ⫾ 3.2 55.7 ⫾ 5.0 55.1 ⫾ 8.2 54.9 ⫾ 7.8 52.6 ⫾ 7.5
Values are means ⫾ SD; N, no. of subjects.
** P ⬍ 0.01 vs 20s.
gate muscle functional characteristics of the knee extensor Peak torque measurements. Peak torque during
and flexor muscles in 164 men and women aged from 20 to isometric (0°䡠s-1) and isokinetic knee extension and flex-
84 yr. ion at 60, 180, and 300°䡠s-1 were measured by using an
isokinetic dynamometer (Cybex 770-NORM). The knee
joint torque measurements were performed according to
METHODS our previous studies (3,4,6). Calibration was performed
before each testing session according to the Cybex sys-
Subjects. A total of 164 volunteers participated in this
tems. Subjects warmed up by light exercise such as
study. The procedures, purpose, and risks associated with
the study were explained to all subjects, then we gave their walking and running for about 5 min and performed
written informed consent to participate in this investigation several stretching exercises for the knee extensor and
before starting of this project. They have no knee malfunc- flexor muscles before performing any of the strength
tion, back pain, hip pain sciatica, or abnormalities of skeletal tests. The subjects were stabilized during practice and
muscles. Before the knee joint torque measurement, all testing via straps to the chest, hips, and middle of the
subjects were measured their resting blood pressure under thigh. Great care was taken to align the anatomical axis of
the supervision of a physician. When subjects who had the joint with the mechanical axis of the dynamometer
higher blood pressure than their normal resting blood pres- before the tests. Knee extension and flexion torque mea-
sure was observed, they were judged by the physician to surement was performed separately at all conditions;
perform strength measurements. Because maximum knee thus, eight testing conditions were done: knee extension
joint torque measurement would induce increase in blood and flexion at 0, 60, 180, 300°䡠s-1, respectively. Two to
pressure. They were divided five groups: 20s (20 –39 yr four trials were performed before testing, and then three
old), 40s (40 – 49 yr old), 50s (50 –59 yr old), 60s (60 – 69 yr maximal voluntary knee extensions or flexions were per-
old), and 70s (70 – 84 yr old) depending on their chronolog- formed to determine peak torque in the range of joint
ical age (Table 1). angles between 0° (full extension) and 90° (flexed posi-
MR imaging measurement. MR imaging was col- tion). The knee joint angle during isometric knee exten-
lected by using a 1.5-T superconducting magnet (Signa sion and flexion measurement was 80° and 40°, respec-
MR Systems, General Electric Medical Systems, Wauke- tively. Two maximum contractions were performed
sha, WI) with a body coil in supine position. Pillows were during 4 s for isometric knee extension or flexion. Avoid-
used under the subjects’ feet and buttocks to minimize ing from repetitive maximum effort-induced high blood
any tissue compression in the thigh. We performed MR pressure, especially for elderly subjects, we chose “two
imaging and calculation of CSA of the QF according to repetitions” of maximum efforts for measuring isometric
our previous studies (3– 6). In briefly, coronal images torque measurements. The torque was corrected for grav-
were taken to identify the anatomical markers, i.e., itational moments of the lower leg and the lever arm. A
greater trochanter and the distal end of femur, and axial rest period of approximately a few minutes was allowed
image (TR 900 ms, TE 20 ms, matrix 256 ⫻ 192, field of between trials to exclude the effect of fatigue.
view 18 cm, slice thickness 10 mm, interslice gap 0 mm) To facilitate comparisons of muscle force to CSA ratio
of the right-thigh was taken at the center of two anatom- (force/CSA) with some previous studies, isometric knee
ical markers. Outlines of the QF according to a standard extension peak torque in Newton meters (Nm) were con-
anatomical textbook (10) were traced using axial MR verted to Newtons (N) by dividing by the length of the lower
images. Traced images were transferred to a Macintosh leg (m) of each subject (18,19).
computer (Power Macintosh 8600/200, Apple Computer, Statistical analysis. An analysis of variance
Cupertino, CA) for calculation of the CSA using a public (ANOVA) was used to compare age groups and gender
domain National Institute of Health (NIH) image soft- differences in physical characteristics (height and body
ware package ver1.60/ppc (written by Wayne Rasband at weight), knee joint torque. When a difference was found,
the NIH and available from the Internet by anonymous ftp a Scheffé’s post hoc test was used to determine the
from [Link]) after spatial calibration. specific comparisons that were significant. Regression
MUSCLE FUNCTION WITH AGING Medicine & Science in Sports & Exercise姞 221
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°䡠s-1) in 60s and 70s was lower than
that in 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 exten-
sion torque losses at 0, 60, 180, and 300°䡠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°䡠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
RESULTS
Table 1 shows physical characteristics of subjects. The
subjects of 60s and 70s in men and women were signifi-
cantly 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 de-
creased 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°䡠s-1) in 40s,
50s, 60s, and 70s was lower than that in 20s.
Figure 2 shows that age-associated peak torque change
during isokinetic knee flexion. Knee flexion torque at all FIGURE 2—Age-associated peak torque during isokinetic knee flex-
tested the velocities in men and women gradually decreased ion in men and women. * P < 0.05; ** P < 0.01; # P < 0.001 vs 20s.
flexion torque per year associated with aging. In all tested individuals. However, most of such studies focused either
the velocities, the percentage decline per decade in knee solely on muscle strength or were performed using only
extension torque in men and women was approximately rough measurements of muscle size on a narrow age-range
12% and 8%, respectively, and that in knee flexion torque in (e.g., young vs old). As such, only a few studies have
men and women was approximately 11% and 8%, attempted to determine muscle function, e.g., peak torque
respectively. and force/CSA, on a wide range of ages.
There was a significant correlation between CSA of QF We found in this study that knee extension and flexion
and maximum knee extension torque (0°䡠s-1) in men (r ⫽ torque at all the tested velocities decreased with aging in
0.827, P ⬍ 0.001) and women (r ⫽ 0.657, P ⬍ 0.001). both sexes. This agrees with previous studies by Larsson et
Figure 5 shows that age-associated change in isometric al. (21), who reported that a decline in QF muscle strength
knee extension force per unit of CSA (force/CSA) in men commencing in the 50s group, and by Vandervoort and
and women. Force/CSA decreased with advanced aging in McComas (30), who likewise reported a decrease in volun-
men (r ⫽ ⫺0.597, P ⬍ 0.001) but not in women (r ⫽ tary plantarflexors and dorsiflexors torque commencing at
⫺0.207, NS). 52 yr of age. Recently, Lindle et al. (24) showed that
age-associated concentric (30°䡠s-1) strength losses begin to
manifest in the 40s in both sexes. In the present study, knee
DISCUSSION
extensors and flexors torque, at all the tested velocities,
Many studies have been reported that muscle function decreased linearly with aging in both sexes. Our results thus
such as peak torque and force per unit of CSA in elderly differ from those of previous studies that evaluated age-
MUSCLE FUNCTION WITH AGING Medicine & Science in Sports & Exercise姞 223
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 follow-
ing 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°䡠s-1)
FIGURE 5—Regression analysis of age-associated difference in force after only 2 wk of resistance training. Moreover, this in-
per unit of cross-sectional area (CSA) during isometric knee extension crease in peak torque was accompanied by greater muscle
in men and women. F, men; 䡩, women.
recruitment (as determined by exercise-induced contrast
shift in MR images) without hypertrophy of either the CSA
related human muscle strength. However, in this study, a of the QF, or the muscle fiber area in the vastus lateralis
significant relationship was observed between CSA of QF muscle (VL) in the trained leg (4). Furthermore, Moritani
and the peak torque at 0°䡠s-1 in both sexes, thus supporting and deVries (25) demonstrated that 8 wk of resistance
the notion of a linear decline in muscle strength with ad- training induced muscle strength gain in elderly subjects,
vancing age. Therefore, our results imply that muscle mass with neural factors mainly contributing to the strength gain
is the primary factor involved in an aged individual’s ca- throughout the training period. This suggests that elderly
pacity to exert maximum force. individuals have a greater trainability by resistance training-
The strength losses associated with aging were observed induced facilitation through neural factors. Taking these
under isometric and isokinetic conditions from low to high observations together, muscle recruitment would appear to
velocities. As shown in Figures 3 and 4, the linear regression have a substantial effect on the capacity to exert maximum
slopes for knee extension and flexion, within 0 –300°䡠s-1, muscle force.
were very similar in both sexes. This suggests that the effect Second, muscle architectural factors may have an effect
of aging on the peak torque exerted during knee extension on the force/CSA change associated with aging. In this
and flexion is likely to be very similar at low (including study, the CSA was calculated from single slice images, and
isometric contraction) to high angular velocities. Several thus this CSA can be considered to be an anatomical CSA
studies have shown a preferential atrophy of Type II fibers but not a physiological CSA. It has been demonstrated that
with advancing age (20,23,28). Moreover, some studies the physiological CSA reflects its force production poten-
have demonstrated that a significant correlation between tial, and it can be derived from the following equation
muscle strength and either % Type II fibers or % area Type (4,5,11),
II fibers, with the correlation being higher at faster angular physiological CSA ⫽ 共muscle volume ⫻ cos 兲/fiber length
velocities (3,29). However, in spite of the selective reduc-
tion in the size and number of Type II fibers with advancing ; pennation angle of the muscle
age reported in previous studies, such changes appear to No association is apparent between fiber length and aging
have little affect on the peak torque. Thus, in this study, fiber and thus physiological CSA would be affected by muscle
types and/or fiber area are unlikely to be the main factors volume and/or pennation angle of the muscle. The pennation
that determine peak torque during isometric and isokinetic angle of the VL at a knee joint angle of 80° (0°: full
knee extension and flexion in elderly men and women in this extension) in sedentary men was found to be 15° (13). Abe
study. et al. (3) and Akima et al. (5) reported that pennation angle
Relatively few studies on force/CSA in elderly people and muscle volume changes in the VL was found after 20 d
have been reported (9,11,17,20,27,31,32). Young et al. (32) of bed rest in 10 healthy men and women. The muscle
demonstrated that the force/CSA of the QF in elderly men volume in the VL decreased by 7.3%, however, no change
was lower than that of younger men, however, reported that was noted in pennation angle (pre: 16.5°, post: 16.9°) in the
no differences between elderly and young women. In con- VL. Thus, it appears that changes in muscle size and pen-
trast, Overend et al. (26) reported no significant differences nation angle do not always occur simultaneously. In the
in the force/CSA of the QF when comparing between el- atrophic or aged VL, the pennation angle decreased by about
derly and young men. In the present study, the force/CSA 5° compared with the young VL (Y. Kawakami, Ph.D., The
decreased linearly with increasing age in men; however, no University of Tokyo, personal communication). Hence,
age-related decreases in force/CSA were observed in from the results of these findings (2), the aged muscle
women. Thus, our results in part support those of Young et pennation angle can be calculated as approximately 12°,
al. (31,32) and further suggest that several factors contribute with the cosine of 12° being 0.98. This, therefore, implies
224 Official Journal of the American College of Sports Medicine [Link]
that 98% of the force exerted by the individual muscle fibers and elderly women of 7.1 and 7.2 N䡠cm-2, respectively,
would thence be transferred to the tendon; there is only a reported herein are comparable to the force/CSA of the QF
minuscule loss of the force exerted by the muscle. There- in young and elderly women of 7.1 and 6.9 N䡠cm-2, respec-
fore, the pennation angle does not appear to be a major tively, reported by Young et al. (31). In addition, the force/
factor affecting the age-related decline in force/CSA. From CSA in two age groups were also similar to those reported
the above observations, muscle volume would appear to be by Young et al. (32). Recently, Jubrians et al. (17) demon-
the main factor affecting changes in physiological CSA strated that force/CSA during isokinetic contraction in the
associated with aging. However, thus far, there have been QF declined with age and declined by about 1.5% per year
very few studies detailing muscle volume in the elderly. in 23- to 80-yr-old men and women. If one calculates the
From our previous studies, % change in muscle CSA and age-related force/CSA for all subjects in this study, a sig-
volume in human thigh and leg muscles is similar, whether nificant decline (y ⫽ 3.707– 0.019x, r ⫽ ⫺0.470, P ⬍
the results of sprint training (% changes in CSA; 8% and % 0.001, data are not shown) in force/CSA is also observed.
changes in muscle volume; 6%) or after bed rest (% changes This represents a force/CSA decline of 1.9% per year from
in CSA; ⫺7%, % changes in muscle volume; ⫺7%) (5,6). 20- to 84-yr-old subjects in this study, a value that is very
These data imply that age-related CSA changes would likely similar to that reported by Jubrians et al. (17). The present
be reflected in muscle volume changes. study does not clarify the mechanisms behind the observed
Third, nonmuscle tissue such as connective tissue might sex-specific decline in age-related force/CSA, and thus fur-
have an effect on the force/CSA. Skeletal muscle of elderly ther studies will be required to elucidate this effect.
persons exhibits a greater proportion of nonmuscular tissue In summary, we investigated the effect of aging on mus-
compared to that of younger subjects. Overend and col- cle functional characteristics, i.e., peak torque and force/
leagues (26) calculated nonmuscle tissue of the QF in a CSA, in 164 men and women aged 20-84, and we report that
single slice of the mid-thigh image in young and elderly
knee extension and flexion torque, under isometric and
subjects to be 3.2 and 5.5 cm2, respectively. This nonmuscle
isokinetic conditions, decreased with aging in both sexes. A
tissue CSA was relatively lower in order to explain the aging
significant correlation was observed between CSA of QF
related decline in force/CSA in men but not women.
and peak torque during isometric knee extension in men (r
Fourth, qualitative changes in contractile properties might
⫽ 0.827, P ⬍ 0.001) and women (r ⫽ 0.657, P ⬍ 0.001).
be associated with age-related changes in force/CSA. Lars-
Furthermore, although the force/CSA decreased with aging
son et al. (22) reported that a significant decrease in the
in men, this was clearly not the case in women. These results
specific tension of single Type I and IIa fibers, characterized
thus suggest that muscle strength losses would be mainly
according to expression of myosin heavy chain of the VL, in
young, elderly, and very physical elderly subjects. They due to a decline in muscle mass in both sexes whereas
determined the maximum tension per unit of CSA, i.e., age-related decline in muscle function in men may also be
specific tension, in Type I or IIa fibers and found that the the result of neural factors such as muscle recruitment
specific tension of these fibers in young subjects was sig- and/or specific tension.
nificantly higher than those of both elderly and very phys-
ical elderly subjects. Taking into account the study of Lars-
This study was supported by Basic Research for Life & Society.
son et al. study, the force/CSA in aging men observed in this The special coordination funds for Promoting Science & Technology
study may thus be due to a decline in the intrinsic muscle (SCF) and STA were partly supported by Descente Sports
force potential. Promotion.
With regard to sex-specific difference in force/CSA as- Address for correspondence: Hiroshi Akima, Ph.D., Department
of Life Sciences (Sports Sciences), Graduate School of Arts and
sociated with aging, we have no data to support the result of Sciences, The University of Tokyo, Komaba 3-8-1, Meguro, Tokyo
the above study. However, the values of force/CSA in young 153-8902, Japan; E-mail; akima@[Link].
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