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1 Department of Kinesiology, To determine the differences between arm
and leg muscle quality (MQ) across the adult life span in men and
women, concentric (Con) and eccentric (Ecc) peak torque (PT) were
measured in 703 subjects (364 men and 339 women, age range 19-93
yr) and appendicular skeletal muscle mass (MM) was determined in the
arm and leg in a subgroup of 502 of these subjects (224 men and 278 women). Regression analysis showed that MQ, defined as PT per unit of
MM, was significantly higher in the arm (~30%) than in the leg
across age in both genders (P < 0.01). Arm and leg MQ declined at a similar rate with age in men,
whereas leg MQ declined ~20% more than arm MQ with increasing age in
women (P
concentric and eccentric peak torque; muscle strength; appendicular
skeletal muscle mass; gender differences
THE AGE-ASSOCIATED LOSS of muscle mass (MM) and muscle
function (sarcopenia) (7) has important health and economic
implications, because it is related to functional disabilities (3, 27), risk of falling (19, 20), and a higher rate of outpatient clinic visits
in the elderly (6). In the East Boston cohort of the Established
Populations for Epidemiologic Studies of the Elderly, 38% of the men
and 59% of the women >65 yr of age had difficulty stooping and 24%
of the men and 29% of the women had difficulty lifting their arm above
the shoulder (9). These findings suggest that older women have greater
muscular dysfunction than older men.
Muscle strength has been reported to reach peak values between 25 and
35 yr of age, is maintained or is slightly lower between 40 and 49 yr
of age, and then is ~12-14%/decade less after 50 yr of age (2,
16, 18, 22). These age-associated differences in strength are highly
correlated with age differences in MM (13, 21, 28). Although the
specific mechanisms for the age-related decline in strength have not
been identified, the major underlying factor appears to be the decrease
in MM with age (10, 28).
The importance of expressing age-related strength losses relative to MM
was emphasized by a panel of experts at the 1996 National Institute on
Aging workshop "Sarcopenia and Physical Performance in Old Age,"
in which it was concluded that there is a need for more comprehensive
evaluations of age-related changes in muscle quality (MQ) (7). MQ, also
known as specific tension, refers to strength per unit of MM and may be
a better indicator of muscle function than strength alone (7). We
recently reported an age-related decline in MQ of the leg in both
genders when determined by concentric (Con) peak torque (PT) (18).
However, in our previous study there was no measure of MQ in the arm
muscle groups. Investigators have emphasized the need to obtain more
information through aging research on muscle groups in the arm (7).
Information on age and gender differences in MQ of the arm vs. leg
muscle groups determined from Con and eccentric (Ecc) PT may help
target interventions for sarcopenia to specific muscle groups with
specific muscle actions.
A gender difference in MQ with age has been suggested in previous
cross-sectional studies. For example, no difference in MQ between young
and older women has been reported (33), but many studies have
reported an age-associated decline in MQ in men (13, 24, 28, 29, 34).
However, MQ in the arm and leg has not been compared in men and women
throughout the adult life span.
It has been reported that arm and leg muscle groups are ~30-50%
stronger in men than in women (2, 10, 23, 28) and that men tend to have
a greater proportion of their MM in the arms than women (14, 23).
Nonetheless, Frontera et al. (10) reported that strength, corrected for
total body fat-free mass (FFM) estimated by hydrodensitometry, remained
significantly higher in men than in women in the arm and leg. However,
in the same population the ratio of strength per kilogram of MM,
estimated by creatinine excretion, was higher in men than in women for
the arm but similar between the genders in the leg (10). These findings suggest that gender differences may exist in MQ, particularly in the
arm. Therefore, the purpose of this study was to describe the
age-associated differences in MQ in the arm and leg throughout the
adult life span and to determine whether gender or muscle group affects
the relationship between MQ and age.
Subjects.
Volunteers (n = 703, 364 men and 339 women, age range 19-93 yr) from the Baltimore Longitudinal Study
on Aging participated in the study. However, only 502 subjects (224 men
and 278 women) underwent assessment of arm and leg MM. The physical
characteristics and PT measurement of this subgroup did not deviate
significantly from the participants who did not undergo arm and leg MM
assessment. All subjects received a complete medical history and
physical examination. Those with clinical cardiovascular or
musculoskeletal disease were excluded. Also, subjects were excluded if
they had active neck and back pain, frequent and severe joint pain, any surgery in the past 6 mo, prior bone scan below normal for their age
(<0.72 g/cm2 for femoral neck
and lumbar spine bone mineral density in women and 0.59 and 0.76 g/cm2 for femoral neck and lumbar
spine bone mineral density, respectively, in men), or any other
condition that might be aggravated by strength testing. Subjects
responded to a questionnaire concerning weight training over the past 2 yr. The average number of minutes per week of weight training
participation was recorded, analyzed, and compared among various age
groups. Only a very small percentage of subjects (<1%) participated
in any type of regular weight training program, and there was no
significant difference in participation by age group or gender (18).
After receiving a complete explanation of the procedures and the risks
of the study, all subjects gave their written informed consent. The
experimental protocols of this study were approved by the Institutional
Review Board for Human Subjects at Johns Hopkins Bayview Medical Center
(Baltimore, MD) and the University of Maryland (College Park, MD).
Body composition assessment.
Body mass and height were measured to the nearest 0.1 kg and 0.5 cm,
respectively, with a Detecto medical beam scale. A total body scan was
performed using dual-energy X-ray absorptiometry (model DPX-L, Lunar
Radiation, Madison, WI) to determine percent body fat, nonosseous arm
FFM, and leg FFM of the dominant arm and leg. Arm FFM encompassed soft
tissue extending from the center of the arm socket to the phalange
tips, and leg FFM consisted of soft tissue extending from an angled
line drawn through the femoral neck to the phalange tips (11).
Nonosseous appendicular FFM derived from these regional measurements
was then assumed to be a valid estimation of appendicular skeletal MM
for the arm and leg on the basis of the work of Gallagher et al. (11)
and Wang et al. (30). All scans were analyzed using the LUNAR software program (version 3.6/1.3y) for body composition analyses. Reliability was assessed by performing two total body scans, 6 wk apart, on 12 older men (>65 yr). Serial values were 52.94 ± 1.23 vs.
53.03 ± 1.36 kg for MM and 22.99 ± 1.46 vs. 22.88 ± 1.43 kg for fat mass, representing a difference between the two
scans of ~0.01% for MM and fat mass. The scanner was calibrated
daily before testing.
PT assessment.
An isokinetic dynamometer (Kinetic Communicator model 125E Plus,
Chattecx, Chattanooga, TN; Kin-Com) was used to measure PT. Con and Ecc
PT (PTCon and PTEcc, respectively) were
measured in the dominant elbow flexors and elbow extensors at an
angular velocity of 0.79 rad/s (45°/s) and in the dominant knee
flexors and knee extensors at an angular velocity of 0.52 rad/s
(30°/s). Participants were positioned sitting with the backrest at
an angle of 1.83 rad (105°) and with hip angle between 1.40 and
1.48 rad (80 and 85°) and were stabilized using chest, waist, and
thigh straps. The rotational axis of the dynamometer was aligned to the
lateral epicondyle of the distal humerus with the resistance arm
positioned in alignment with the forearm. The rotational axis of the
dynamometer was aligned with the lateral femoral epicondyle of the
subject's knee with the resistance pad positioned proximally to the
lateral malleolus of the ankle joint. The length of the resistance arm was recorded for the elbow and knee. A goniometer was used to measure
the anatomic joint angle to calibrate the Kin-Com angle readings.
Gravity corrections to torque were calculated by the gravity correction
program in the Kin-Com software package (version 3.2) on the basis of
the weight of the arm in the horizontal position at 2.62 rad (150°)
and the leg at 2.97 rad (170°; 3.13 rad = straight leg). The force
threshold required for movement of the lever arm was set at 50 N, but
when necessary the force threshold was adjusted for arm strength
measurement to a minimum of 2 N. The joint arc of the elbow was limited
to 1.05 rad (60°), and the maximal elbow extension angle was set at
2.62 rad (150°). The joint arc of the knee was limited to 1.13 or
1.22 rad (65 or 70°), and the maximal knee extension angle was set
at 2.97 rad (170°). Accuracy of the force movement was determined
weekly by using the internal Kin-Com diagnostic check and force
calibration programs. For force calibrations the lever arm was
positioned parallel to the floor at 3.14 rad (180°) and known
weights of 45 and 110 N (10 and 25 pounds) were hung directly on the
load cell. The force reported by the Kin-Com was compared with the
actual weights, and force outputs were calibrated when necessary.
Reliability of strength testing with use of this Kin-Com dynamometer
and protocol was tested in 10 older men on two occasions with a 1-wk
interval between trials. Intraclass correlation coefficients were
between 0.96 and 0.99 for leg tests. Mean coefficient of variation for
leg tests was 5% (range 1.5-7.5%).
ABSTRACT
Top
Abstract
Introduction
References
0.01 and
P < 0.05 for Con and Ecc PT,
respectively). Moreover, the age-associated decrease in arm MQ was
steeper in men than in women whether Con or Ecc PT was used (both
P < 0.05). Arm MQ as determined by
Con PT showed a linear age-related decline in men and women (28 and
20%, respectively, P < 0.001),
whereas arm MQ as determined by Ecc PT showed a linear age-related
decline in men (25%, P < 0.001) but
not in women (not significant). In contrast, both genders exhibited an
age-related quadratic decline in leg MQ as determined by Con PT
(~40%) and Ecc PT (~25%; both P < 0.001), and the rate of decline was similar for men and women. Thus
MQ is affected by age and gender, but the magnitude of this effect
depends on the muscle group studied and the type of muscle action (Con
vs. Ecc) used to assess strength.
INTRODUCTION
Top
Abstract
Introduction
References
METHODS
5 min. Three submaximal practice repetitions preceded
three maximal efforts for each specific test. All maximal efforts were
separated by a 30-s rest period. PT was determined for each maximal
effort with use of the Kin-Com's Torque vs. Angle program (KC772.047).
The trial yielding the highest PT for each test was used in the
analysis. Arm PTCon was defined as
the sum of Con elbow flexor and extensor PT, arm
PTEcc as the sum of Ecc elbow
flexor and extensor PT, leg PTCon
as the sum of Con knee flexor and extensor PT, and leg
PTEcc as the sum of Ecc knee
flexor and extensor PT.
Arm and leg MQ.
Arm MQCon and arm
MQEcc
(N · m · kg
1)
were calculated by dividing arm
PTCon (N · m)
and arm PTEcc
(N · m), respectively, by arm MM (kg). Leg
MQCon and leg
MQEcc were calculated by dividing leg PTCon
(N · m) and leg
PTEcc (N · m),
respectively, by leg MM (kg).
Arm and leg difference. To determine whether the arm and leg showed similar changes with increasing age, the difference between arm and leg PT (Diff arm-leg PTCon and Diff arm-leg PTEcc) and the difference between arm and leg MQ (Diff arm-leg MQCon and Diff arm-leg MQEcc) were calculated.
Statistical analysis. One-way ANOVA was used to compare age decade and gender differences for the following physical characteristics and peak torques: height, body mass, percent body fat, arm MM, leg MM, arm PTCon, arm PTEcc, leg PTCon, and leg PTEcc (Tables 1 and 2). Significant main effects for age decade were followed up with Dunnett's multiple comparison technique. Dunnett's test was used to determine the specific age decades that were significantly different from the young (20- to 39-yr-old) adults.
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RESULTS |
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Physical characteristics. Physical characteristics of the men and women by age group are reported in Tables 1 and 2, respectively. Men were significantly taller and heavier and had lower percent body fat and greater arm and leg MM than women throughout the entire adult life span (all P < 0.01). An age-related reduction in height from the young adults became apparent for the men in their 70s and for the women in their 60s (P < 0.01). Body mass was significantly lower in the oldest decade than in the young adults among the men (P < 0.05); however, there were no differences in body mass in women across the adult life span. In men, percent body fat showed a significant increase beginning in their 50s, and in women it was significantly higher than in the young adults in their 40s, 50s, and 60s (P < 0.01). Men had significantly lower arm and leg MM in their 60s and older decades (P < 0.01). Arm MM was significantly lower in their 60s and older decades in women (P < 0.01); however, leg MM reductions began as early as the 40s (P < 0.05). There were no significant differences in age, height, weight, percent body fat, or PT measurements between the total population (n = 703) and the subgroup (n = 502) in which arm and leg MM were measured.
Arm and leg PT.
Age-associated declines were observed for arm
PTCon (Tables 1 and 2, Fig.
1A),
leg PTCon (Tables 1 and 2, Fig.
1B), arm PTEcc (Tables 1 and 2, Fig.
2A), and
leg PTEcc (Tables 1 and 2, Fig.
2B; all
P < 0.05). In 50-yr-old men, arm
PTCon and leg PTCon were significantly lower
than in younger men (P < 0.05). In
60-yr-old men, arm PTEcc and leg
PTEcc were significantly lower
than in younger men (P < 0.01). In
50-yr-old women, arm PTcon and
PTEcc were significantly lower,
whereas in 40-yr-old women leg
PTCon was significantly lower than
in younger women (all P < 0.05). In
addition, in 60-yr-old women, leg
PTEcc was significantly lower than
in younger women (all P < 0.05).
Changes in arm and leg PT were curvilinear with age, such that declines were modest or nonexistent until the 40s, and thereafter more robust
declines were present. Age-associated declines in PT were greater for
men than for women in all muscle locations (all age-by-gender interactions, P < 0.001).
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PT and appendicular MM. PT for Con and Ecc and appendicular MM were highly related in all body regions (P < 0.001). Arm MM accounted for 44 and 50% of the variance in arm PTCon and 38 and 46% in arm PTEcc for men and women, respectively. Leg MM accounted for 36 and 39% of the variance in leg PTCon and 32 and 39% in leg PTEcc for men and women, respectively.
Arm and leg MQ.
MQ as a function of age for men and women is presented in Figs.
3 and Fig. 4.
A linear age-associated decline was observed in arm
MQCon for men and women
(P < 0.001; Fig.
3A). Arm
MQEcc declined linearly with age
in men; however, no age-related decline was observed in women (Fig.
4A). A significant age-by-gender
interaction was observed for arm
MQCon and arm
MQEcc
(P < 0.05). For example, as
reflected in Fig. 3A, arm
MQCon was ~10
N · m · kg1
more in men than in women at 30 yr of age. However, at 90 yr of age the
gender difference in arm MQCon
narrowed to ~4
N · m · kg1.
Furthermore, the difference between men and women decreased with
advancing age in arm MQCon and arm
MQEcc.
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DISCUSSION |
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The major new findings from this study are as follows. 1) Age-associated differences in arm MQ declined more in men than in women; however, leg MQ declined with age at the same rate in both genders. 2) Arm MQ was higher than leg MQ across age for men and women. 3) Arm MQ declined at the same rate across age as leg MQ in men; however, the age-related decline was greater in leg MQ than in arm MQ for women. Finally, leg PT was higher than arm PT across age, but this difference decreased across the adult life span in both genders.
Conflicting results have been reported in previous studies regarding the relationship between MQ and age. Alway et al. (1) reported that isometric torque per unit muscle cross-sectional area (CSA), measured by magnetic resonance imaging (leg MQ), was not significantly different between young and older men. Overend et al. (24) reported no age-related difference when leg MQ was estimated by isometric strength per CSA as measured by computed tomography but lower MQ in the elderly than in the young men when MQ was expressed as Con isokinetic strength per CSA of the leg. Reed et al. (28) found a significant age-associated loss in cumulative MQ (combined strength of the arm and leg per kg of total body lean MM); however, they used a bioelectrical impedance analysis to estimate total body lean MM and concluded that more accurate measures of regional MM are needed in future studies. Frontera et al. (10) showed age-related declines in MQ of the arm and leg when using FFM estimated by hydrostatic weighing but no change in MQ when using MM estimated from urinary creatinine excretion. However, these results are difficult to interpret, because hydrostatic weighing was performed without the measurement of residual volume and PT was performed using the Cybex II with no gravity correction. Each of these factors can lead to significant errors (31, 32). Thus the various techniques used in previous studies to estimate MM may explain some of the inconsistent findings regarding the effects of age on MQ. This is the first study in which age-related MQ comparisons in the arm vs. leg were made using reliable techniques for assessing strength and limb MM (8, 11, 30).
In addition to differences in measurement techniques, some of the conflicting results from previous studies may be explained by differences in age, gender, or the muscle group tested. For example, previous studies have reported that although men were stronger than women, MQ was the same in men and women (23, 28, 33, 34). In contrast, the present study shows a higher MQ in men than in women in the arm and leg. In addition, Young et al. (33, 34) reported that MQ was lower in older than in younger men but was the same in older and younger women. In the present study, MQ was lower with advancing age in men and women in all muscle locations, except arm MQEcc in women. Furthermore, the age-associated rate of change differed between men and women for arm MQ. Arm MQ appears to decline more with age in men than in women, although it is important to note that because men begin with more MQ at a young age, they have more MQ to lose over the adult life span. In contrast to arm MQ, the age-associated rate of change in MQ of the leg was similar for men and women.
The finding of a significant age-related decline in leg MQEcc in women is in contrast to our previous report, which did not show a decline in women (18). There were almost four times as many women >65 yr of age in the current study as in the previous study. Thus the greater sample size for this variable increased the statistical power for detecting a significant age effect. Although our previous (18) study did not report arm MQ data, we have since examined the relationship between arm and leg MQ from the previous study's sample and found the same relationship reported in this study.
This is the first study to report a gender difference in the decline of arm and leg MQ with advanced age. As shown in Fig. 3, the difference between arm and leg MQ was unchanged with age in men but increased in women, indicating that leg MQ declined more with advancing age than arm MQ in women. This suggests that in women arm muscles may not experience as much age-related change in contractile properties, connective tissue, or architectural components, such as pennation angles, as leg muscles. Qualitative changes in contractile properties (17) and increases in connective tissue (25) have been associated with aging. In addition, increases in muscle fiber pennation angle in hypertrophied muscle (15) suggest that pennation angle is likely to decrease with aging. An additional novel finding from this study is that MQ of the arm was significantly higher than MQ of the leg across the entire adult life span in both genders. Thus more strength is produced per unit of MM in the arm than in the leg in men and women. In addition, the variance in arm PT accounted for by arm MM was greater than the variance in leg PT accounted for by leg MM. Therefore, MM may be more important in explaining arm strength loss than leg strength loss. Although other age-related factors to explain this difference have not been identified, possible mechanisms include neural activation, muscle fiber type distribution, and muscle pennation angle differences between the arm and leg.
In general, muscle strength has been reported to peak in the 20s and 30s, remain stable or decline slowly into the 40s, and decline ~12-14%/decade after 50 yr of age (2, 16, 22). Overall, our results support previous findings describing the age-associated loss of strength. Moreover, our findings appear to be in partial agreement with those of previous investigators who also report a greater age-related loss of Con than Ecc strength (12, 26). An age-related decline in Ecc strength was not observed in these studies; however, we observed a significant age-related decline in Con and Ecc strength in all muscle locations and in both genders. However, the variance accounted for by age was higher for Con than for Ecc measurements in both genders and in the arm and leg. In addition, results from this study confirm previous reports that showed a greater age-related loss of strength in the leg than in the arm (4, 28, 29). A possible explanation for the greater leg strength loss may be related to increased disuse in the legs, but no physiological or biochemical mechanisms have been identified.
There were several limitations of this study in addition to the cross-sectional design. For example, there was no measure of contractile or mechanical properties of the muscle groups studied to help explain our findings. In addition, future studies should investigate age-related differences in muscle architecture, such as fiber pennation angles, so that this information can be related to losses in strength and MM.
In conclusion, the results of this study indicate that there are age-related declines in arm and leg MQ in men and women, except for arm MQEcc, which remained stable across age in women. MQ was greater in the arm than in the leg as determined by Con and Ecc PT in men and women throughout the adult life span. Furthermore, there was a greater age-related decline in leg than in arm MQ in women; however, arm and leg MQ declined at the same rate with age in men. Finally, leg PT was higher and declined more with advancing age than arm PT in men and women.
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ACKNOWLEDGEMENTS |
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The authors thank Dorothy O'Donnell for technical assistance and the participants in the Baltimore Longitudinal Study of Aging.
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FOOTNOTES |
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This study was supported in part by a National Institutes of Health Intramural Research Training Award fellowship to N. A. Lynch and was conducted as part of the Baltimore Longitudinal Study of Aging, a component of the National Institute on Aging intramural research program.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address reprint requests to B. F. Hurley.
Received 16 June 1998; accepted in final form 27 August 1998.
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