| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Canadian Centre for Activity and Aging, Lawson Health Research Institute, and 2 School of Kinesiology, Faculty of Health Sciences, and 3 Departments of Anatomy and Cell Biology, and 4 Medical Biophysics, Faculty of Medicine and Dentistry, The University of Western Ontario, London, Ontario, Canada N6G 2M3
 |
ABSTRACT |
|---|
 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The purpose of this study was to determine whether the loss of muscle strength in the elderly could be explained entirely by a decline in the physiological cross-sectional area (PCSA) of muscle. Isometric force, muscle activation (twitch interpolation), and coactivation (surface electromyograph) were measured during maximal voluntary contractions (MVCs) of the elbow flexors (EFs) and extensors (EEs) in 20 young (23 ± 3 yr) and 13 older (81 ± 6 yr) healthy men. PCSA was determined using magnetic resonance imaging, and normalized force (NF) was calculated as the MVC/PCSA ratio. The PCSA was smaller in the old compared with the young men, more so in the EEs (28%) compared with the EFs (19%) (P < 0.001); however, the decline in MVC (~30%) with age was similar in the two muscle groups. Muscle activation was not different between the groups, but coactivation was greater (5%) (P < 0.001) in the old men for both muscles. NF was less (11%) in the EFs (P < 0.01) and tended to be unchanged in the EEs of the old compared with young subjects. The relative maintenance of NF in the EEs compared with the EFs may be related to age-associated changes in the architecture of the triceps brachii muscle. In conclusion, although the decline in PCSA explained the majority of strength loss in the old men, additional factors such as greater coactivation or reduced specific tension also may have contributed to the age-related loss of isometric strength.
elbow flexors; elbow extensors; specific tension; physiological cross-sectional area; sarcopenia
| |
INTRODUCTION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
A COMMON OBSERVATION IN OLDER people is the loss of muscle mass and strength (41). What is controversial, however, is whether the loss of strength (force) is entirely explained by the decrease in muscle size or whether other factors, such as muscle activation, coactivation, and specific tension, are also important (9, 11). The typical approach used to study this problem is to determine the normalized force (NF) in young and old subjects. The NF is the ratio of maximal voluntary force [maximal voluntary contraction (MVC)] to some measure of the size of the muscle(s) producing the force. A number of authors reported no age-related changes in NF (11, 26, 40), which implies that the decrease in muscle size explains virtually all of the force loss. In contrast, others have found up to a 40% decline in NF with age (8, 27, 32, 48), which indicates that other factors, in addition to a decrease in muscle size, may contribute to the loss of strength.
The explanation for the conflicting findings of NF and aging may relate, in part, to the methods used to measure muscle strength and muscle size. For example, a decline in NF with age seemed to be more prevalent during dynamic rather than isometric contractions, and the decrease may be greater in women compared with men (16, 32, 40). As well, muscle size may have been overestimated in older people because of the inability of indirect techniques to distinguish muscle from noncontractile tissue (8, 32). Moreover, the anatomic cross-sectional area (ACSA), which is the area of muscle measured from a single cross section, commonly measured in NF studies may underestimate the loss of muscle mass with age (2). A more accurate index of muscle size and force-generating capacity, particularly in muscles with a pennate fiber architecture such as the triceps brachii, may be the physiological cross-sectional area (PCSA) (12, 42). The PCSA, which is the total cross-sectional area of all the muscle fibers in a muscle, can be determined in vivo by combining the measurement of muscle volume from magnetic resonance imaging (MRI) with muscle fiber length estimated from cadavers. The PCSA of the upper and lower limb muscles has been measured in young subjects but not in the muscles of the elderly (12, 25).
Neural drive to the agonist and antagonist muscles can influence force-generating capacity. The level of muscle activation, as assessed by the twitch interpolation technique, was reported to be less in the elbow flexors (EFs) in old compared with young people (9, 49). As well, coactivation level of the knee flexors, as measured by surface electromyograph (EMG), was higher with old age during MVCs of the knee extensors (15, 22). A decrease in activation or an increase in coactivation, or both, could reduce NF in aged people. However, in many studies of NF, the level of activation was not measured (27, 32, 48), so it is uncertain whether the young and old recruited all motor units maximally during the MVC. In addition, no studies have reported coactivation measures in relation to old age in the EFs and elbow extensors (EEs) during maximal contractions.
In this study we measured PCSA, MVC, NF, activation, and coactivation in the EFs and EEs of young and old men. The main purpose was to determine whether the NF of the arm muscles changes with age and, if so, whether the EFs and EEs are affected similarly.
| |
METHODS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Subjects. Twenty young men, aged 20-29 yr (mean age 22.6 ± 2.7 yr), and thirteen old men, aged 76-95 yr (mean age 81 ± 6.5 yr), volunteered for the study. The young subjects were university students, and the old subjects were living independently in the community. A written questionnaire and interview determined their medical history and the extent of their participation in physical activity. Exclusion criteria for participation in this study included orthopedic or neurological pathologies of the upper or lower limbs, diabetes, previous myocardial infarction, uncontrolled hypertension, alcoholism, medications that affect muscle performance, and extreme physical activity. Most of the subjects were sedentary and had not participated in weight training or other formal exercise program. The purpose, methodology, and possible risks involved in the experiments were explained, and informed written consent was obtained from each subject. The ethics review committee of the University of Western Ontario approved all procedures.
MRI acquisition. Within 3 wk of recording the MVC, serial T1-weighted images in the axial plane were acquired with MRI using a 20-cm-diameter extremity coil in a 1.5-T whole body magnet and 64-MHz scanner (Siemens Vision System, Siemens Medical, Erlangen, Germany). Subjects were supine with the left elbow extended and adjacent to the trunk and the forearm in a neutral position. Foam padding was placed under the elbow and forearm, so the arm was parallel to the gantry, and the triceps brachii was not compressed. Rather than encircling the arm, the extremity coil was positioned over the dorsal, lateral, and ventral aspect of the arm or forearm and held in place with Velcro straps that crossed the trunk. By not encircling the arm, the origins of the biceps brachii and triceps brachii could be imaged. Reference markers were placed on the medial epicondyle and mid point of the arm.
The arm was imaged in four segments from the top of the humerus to the wrist by moving the extremity coil three times. Using the software, a grid of 20-24 (depending on arm length) slices was centered on a coronal scout image so the slices were perpendicular to the arm (or forearm). Images were acquired using the following parameters: repetition time, 1,000 ms; echo time, 14 ms; number of acquisitions, 1; matrix, 256 × 256; field of view, 200 mm (2 proximal segments, i.e., arm) and 160 mm (2 distal segments i.e., forearm); slice thickness, 7 mm; and interslice gap, 0 mm (imaging time, 4 min/segment). These parameters were selected to delineate muscle borders and differentiate muscle, fat, and connective tissue. To ensure that the four segments were contiguous, the distance between the marker and the most distal slice of a segment was measured (mm) on the scout image using the software. An ink mark, corresponding to this distance, was placed on the arm so that the extremity coil could be moved the appropriate distance.Muscles analyzed. The biceps brachii, brachialis, and brachioradialis muscles were traced in each image and together made up the EFs. The triceps brachii and anconeus were traced and together made up the EEs. The pronator teres and the extensor carpi radialis longus muscles, which together generate 15% of EF torque (38), were not included in the EF volume because they were not clearly visible in the images over their entire length. The brachioradialis, extensor carpi radialis longus, and brevis muscles were traced as a group. The brachioradialis volume was then estimated to be 39% of the combined volume of these three muscles (4). The length of the brachioradialis, however, could be determined because the origin and insertion regions were clearly evident in all images. The coracobrachialis muscle was traced as part of the biceps brachii because these two muscles could not be separated convincingly throughout their entire length. In both young and old cadavers, the coracobrachialis is 23% of the weight of the biceps brachii plus the coracobrachialis (47). To exclude the coracobrachialis from the EF volume, the biceps brachii volume was reduced by 23% in all subjects.
Morphological measures.
The same investigator analyzed the images with a software program
(Analyze 7.5, Mayo Clinic) and was not blinded to subject identity
because it was obvious that images with the smaller muscle size and
larger amount of fat were of older subjects. However, the data
corresponding to images of subjects previously analyzed were not
referred to during subsequent analysis and data were not compiled into
the young and old groups until all images were analyzed. The
cross-sectional area of muscle, bone, and noncontractile tissue were
determined in each image for the entire arm. The regions were either
manually traced and/or autotraced. During an autotrace, which is based
on different ranges of pixel intensity for different tissues, the
operator pointed to the region and then moved a bar to progressively
highlight the tissue to its border. The cross-sectional area of
noncontractile tissue was always determined with the autotrace feature.
The different muscles, bone, and noncontractile tissue that were traced
were automatically filled with color-coded maps that could be edited
and saved (Fig. 1).
|
Validity and reliability of image analysis. Axial images of a cylindrically shaped acrylic phantom (260-ml volume) filled with saline were acquired on each day to determine the validity of estimating tissue volume. A volumetric flask was used to determine the true volume of the phantom. Over the course of the study the volume of the phantom, as measured by the analysis software, was 252 ± 3 cm3 and did not vary significantly. Two investigators (CSK, CLR) analyzed the same four images (10th, 20th, 30th, and 40th) of the arm in each of four subjects (2 old subjects) to determine the intraobserver and interobserver reliability of the CSA measurements. The coefficient of variation (CV) for CSA of muscle and noncontractile tissue was 4 and 22% (intraobserver) and 6 and 25% (interobserver), respectively. The higher variability for noncontractile tissue, which is expected given its small area, has a negligible effect on the percentage of noncontractile tissue we obtained.
Experimental setup for force measurements.
Great care was taken to standardize the position of the subjects
for recording the MVC. The subjects were supine on a padded table and
the left arm (nondominant in all cases) was placed in a custom-designed
force dynamometer (Fig. 2). Compared with
a seated position, it was assumed that the supine position minimized the effect of body weight and extraneous movements on MVC production. The legs were supported on a wooden box, with the knee and hip joints
flexed to 90°, and the shoulders were secured by straps firmly
against a padded metal brace. The box and brace prevented the torso
from sliding during the MVCs. Two additional straps were used to
stabilize the upper limb during an MVC of the EEs. One was positioned
across the arm ~2 cm proximal to the elbow crease, and the other was
placed across the forearm ~5 cm distal to the elbow crease. Once the
subject was secured, the position of the box and the length of all
straps were recorded for positioning on subsequent visits.
|
MVC and NF. The subjects did not participate in any activity that required vigorous use of their arms for 48 h before the measurements. The MVCs were determined during each of three visits to the laboratory over 2-4 wk. Three to four MVCs, each held for 4 s with a 3-min rest, were recorded for each of the EFs and EEs during all visits. Strong encouragement was provided during the contractions and visual feedback was provided. The order in which MVCs of the EFs and EEs were recorded was balanced across the three visits and across groups. The force and EMG signals were analyzed off-line using a customized software package (Spike 2, Cambridge Electronic Design). The highest MVC of the three visits was used to calculate muscle activation, coactivation, and NF. The NF of the EFs or EEs was calculated as the MVC divided by the PCSA of the respective muscle groups.
Activation level.
A modified twitch interpolation technique was used to assess the level
of muscle activation during the MVC (1). The stimulating electrodes were made of aluminum foil, measured 3 × 4 cm to
7 × 4 cm, and were wrapped in gauze and soaked in saline and
conducting gel. The cathode was placed over the motor point of the
biceps brachii or triceps brachii and the anode over the distal third of the muscle. Using a constant-current stimulator (model DS7H, Digitimer), two doublets (2 pulses at 100 Hz, 50-µs pulse duration) were applied both during and after the MVC. The doublets were triggered
manually at the peak of the MVC. The stimulus current intensity for the
doublets was 50-60% of the level used to obtain the maximal
twitch force. Pilot studies and previous reports (6) found
that in the arm muscles, submaximal stimulation resulted in larger
interpolated twitches than maximal stimulation. Activation level was
calculated as: percent activation = [1 
(Ts/Tr)] × 100%, where Ts is the
force of the interpolated response of the doublet at peak force, and
Tr is the mean force of the two post-MVC doublets.
Coactivation level. Coactivation during the MVC was determined by recording the EMG activity over the antagonist muscle(s). After the skin was abraded with sandpaper and cleansed with ethyl alcohol, bipolar silver-silver chloride strip electrodes (1 × 3 cm, Marquette Electronics, Milwaukee, WI) were positioned 15 mm apart over the midbiceps brachii, midtriceps brachii, and proximal third of the brachioradialis. The raw EMG signals were amplified (×500) and filtered (between 10 Hz and 10 kHz) using a Neurolog NL284 (Digitimer) preamplifier, amplifier, and filter and sampled at 2.5 kHz. A 0.5-s period of the EMG was analyzed corresponding to the point of peak force, which usually occurred within the first 2 s of the MVC. The EMG signals were full-wave rectified and integrated (IEMG) over a 500-ms time constant. Coactivation level was expressed as a percentage of the muscle's maximal IEMG recorded during the MVC.
The extent of possible cross talk between the biceps brachii and triceps brachii was determined by examining whether M waves were recorded concurrently over both muscles during supramaximal stimulation of the musculocutaneous or radial nerve. A custom-designed bar electrode was used for stimulation and placed over the musculocutaneous nerve just medial to the anterior deltoid at the axilla. For stimulation of the radial nerve, the electrode was placed over medial head of the triceps brachii at the posterior axilla. Because the nerves were not easily accessible in the supine position, the M waves were recorded with the subject seated and the elbow joint flexed 100°. Bipolar electrodes for recording the voluntary EMG were used but were placed on the distal third of the biceps brachii and triceps brachii to record M waves that were uncontaminated by stimulus artifact.Statistical analysis. A two-by-two-factor of ANOVA was used to assess the influence of age (young and old) and muscle (EFs, EEs) on PCSA, ACSA, MVC, and NF. A two-by-three-factor ANOVA determined the effect of age and muscle (biceps brachii, brachioradialis, and triceps brachii) on coactivation level, and post hoc comparisons of the three muscles was done with the Tukey's test. Muscle activation level was assessed using the Mann-Whitney test because the data were not normally distributed. Pearson's product-moment correlation coefficients were applied to determine the relationships between MVC and PCSA and between NF, activation, and coactivation. The CV was calculated to determine the reliability of measurements. Analyses were performed using SPSS software (version 10 for Windows). Differences were considered significant when P < 0.05, and all data are presented as means ± SD.
| |
RESULTS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Anthropometric and morphological measures.
The subjects' weight, height, and length of the humerus were not
different (P > 0.05) between the young and old men
(Table 1). Muscle volume, excluding
noncontractile tissue, was less in the old compared with the young men
in the EFs (297 ± 56 vs. 375 ± 54 cm3) and EEs
(323 ± 62 vs. 444 ± 61 cm3) (P < 0.001). The results for morphological measures, MVC, NF, and
activation are presented in Table 2. The
PCSA was 19 and 28% smaller with age in the EFs and EEs respectively
(P < 0.001), and the decrease was significantly
greater in the EEs (age × muscle interaction, P = 0.001). The percent decrease in PCSA was the same among muscles that
constitute the EFs and EEs. Because age had no effect on muscle length
in the EFs or EEs, the lower PCSA in the old men was due to a smaller
CSA over the length of the muscle. The ACSA of the biceps brachii + brachialis and triceps brachii were also lower in the old compared
with the young men, and the decrease was less (2%) than the decline in
PCSA. The relatively larger age-related decrease in PCSA compared with
ACSA was significant in the triceps brachii (age × measurement
interaction, P = 0.01) but not in the biceps
brachii + brachialis (P = 0.43). The percentage of
muscle volume that was noncontractile tissue was greater
(P < 0.001) with age (Table 2). The PCSA and
noncontractile tissue were smaller (P < 0.001) in the
EFs compared with the EEs in the young and old. In both the young and
old groups, the brachialis, biceps brachii, and brachioradialis were
52, 36, and 12%, respectively, of EF PCSA, and the anconeus was 5% of
EE PCSA.
|
|
MVC.
The highest MVC on each of the three visits was highly reproducible;
the CV was 3 ± 2 and 6 ± 4% in the young and 3 ± 1 and 5 ± 3% in the old men for the EFs and EEs, respectively. The
MVC was less (P < 0.001) in the EFs (27%) and EEs
(33%) in the old compared with the young, but the magnitude of the
decrease was not different between the muscles (age × muscle
interaction, P = 0.84) (Table 2). The MVC of the EFs
were significantly (P < 0.001) greater than the EEs in
both the young and old. There was a significant correlation between
PCSA and MVC (r 
0.74) in the EFs and EEs in the young and
old men (Figs. 3 and
4). When data of both groups
were combined the correlation coefficients between PCSA and MVC were
r = 0.86 for the EFs and r = 0.87 for
the EEs (P < 0.01). These correlations were larger
than the correlations between ACSA and MVC in both the EFs
(r = 0.83) and EEs (r = 0.80) for the
groups combined.
|
|
Activation and coactivation level.
The level of activation during the MVCs was incomplete (<100%)
in the biceps brachii (range 92-100%) and triceps brachii
(94-100%) in both groups. The deficit in activation was similar
in both groups for the triceps brachii (P = 0.13) but
tended to be greater (P = 0.07) in the biceps brachii
of the old compared with the young (Table 2). The level of coactivation
in the antagonist muscles during MVCs of the EFs and EEs was ~5%
greater (P < 0.001) with age (Fig.
5). There was no evidence of cross talk
because M waves were not evident in the biceps brachii or triceps
brachii during supramaximal stimulation of the radial and
musculocutaneous nerves, respectively.
|
NF. The NF was less in the old compared with the young group (main effect for age, P = 0.001). The decrease in NF with age was more prevalent in the EFs (11%) compared with the EEs (7%), and the difference between the muscles approached significance (age × muscle interaction, P = 0.06) (Table 2, Figs. 3 and 4). The MVC/ACSA also was reduced more in the EFs compared with EEs with age. There were no significant (P > 0.05) correlations between activation or coactivation and NF in either group or when the data from both groups were combined. The NF of the EFs were greater (P < 0.001) than the EEs in both the young and old (Table 2).
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
In this study, we determined the age-related differences in PCSA,
NF, and muscle activation and coactivation in the arm muscles of young
and old men. The NF was significantly less in the EFs (11%), but not
the EEs, of the old men compared with the young men. In addition,
coactivation was ~5% higher with old age in both muscles. These
findings suggest that additional factors, besides the decrease in PCSA,
contribute to the loss of strength in the EFs, whereas the decline in
muscle size seems to explain much of the strength loss in the EEs of
the old men.
Morphological measures.
The PCSA was lower in the old compared with the young group, more
so in the EEs (28%) compared with the EFs (19%). Age-related changes in PCSA have not been reported previously, but the reduction in
ACSA found in this study was consistent with others (26, 27, 40,
43, 48). The greater percent decrease in the PCSA of the EEs
compared with the EFs may have been due to differences in activity
level between the muscles (i.e., amount and/or intensity of
contractions). In addition, the EEs may atrophy at a greater rate than
the EF because the triceps brachii, at least in young men, seems to
have a higher percentage (~10%) of type II fibers than the biceps
brachii (33, 34, 35). Type II fiber area is less, whereas
type I fiber area is minimally affected in the biceps brachii with age
(14). The effect of age on the triceps brachii fiber area
or the daily activity patterns of the EFs and EEs, however, has not
been determined. On the basis of our findings, it is apparent that the
extent of muscle loss with age differs even among the muscles in the
same limb.
MVC, activation, and coactivation.
The MVC was less (~30%) in the EFs and EEs in the old compared with
the young men. Others have reported similar (9, 10) or
smaller (20%) (36) losses of EF strength with age, but
no previous data on the isometric strength of the EEs are available. A
primary question of the present study was whether there is an age-related change in the neural drive to the agonist and antagonist muscles and, if so, what effect this would have on NF. Neural drive to
the agonists was estimated by measuring the activation level of the
biceps brachii and triceps brachii using the twitch interpolation
technique. Similar to previous work (9, 49), our results
indicate that activation was incomplete (<100%) and tended to be less
in the EFs with age, although this age difference was not significant.
A deficit in activation in the old men could imply that the neural
drive (i.e., motor unit recruitment and/or firing rate) is less during
strong contractions and this could contribute to the lower NF of the
EFs. However, there was no correlation between activation (range of
94-100%) and NF in either the young or old men. Although the
age-related difference in activation was small and not significant,
larger differences may occur during dynamic compared with isometric
contractions. For example, the IEMG of the vastus lateralis tended to
be reduced more with age during the standing long jump than during
isometric maneuvers (15). Although Herbert and Gandevia
(17) have questioned whether twitch interpolation is a
sensitive measure of motoneuron excitation, a larger impairment in
activation with age may become apparent if stimulation is applied
during dynamic movements.
NF. The NF was 11% lower in the EFs and tended to be less affected in the EEs with ageing. As mentioned previously, the lower NF in the EFs could stem from an increase in coactivation. Other factors, however, such as a decline in specific tension of the muscle fibers could also contribute to a decrease of NF (11). It is unclear why NF in the EEs is less affected than the EFs with old age. One possible explanation is a reduction in fiber pennation angle in the triceps brachii, secondary to muscle atrophy, compensates for any age-related changes in coactivation and specific tension, by transmitting relatively more tension to the tendon during a contraction (31, 39). In young athletic subjects, the pennation angle of the triceps brachii is positively correlated with muscle size (24) and negatively correlated with NF of the EEs (21). It is interesting that Frontera and co-workers (11) reported a decrease (30%) in specific tension of single fibers but no change in NF in the quadriceps with age. This paradoxical finding may be a reflection of age-related changes in muscle architecture and connective tissue (43) that sustains NF by enhancing force transmission in vivo (20).
In previous studies, investigators found either no change in NF with age (11, 26, 40) or a decrease of up to 40% (8, 23, 27, 32, 46, 48). Similar to our findings, Klittgaard et al. (27) reported a 14% decrease in isometric NF (MVC/ACSA) in the EFs of old (68 yr) compared with young men when computed tomography was used to measure ACSA. As well, in these same subjects, the age-related decrease (27%) in NF of the knee extensor muscles was larger than in the EFs (27). Young and co-workers (48) also reported a 27% decline in isometric NF of the knee extensors with age using ultrasound imaging. However, other investigators reported no change in isometric NF with age in the knee extensors using computed tomography (11, 40) or in the ankle dorsiflexors using MRI (26). An age-related decline in NF during dynamic (isokinetic) contractions also has been reported (23, 32, 40). For example, Overend et al. (40) found that isokinetic NF, but not isometric NF, of the knee extensors and flexors was 10-20% lower in men aged 70 yr compared with 20-yr-old men. Jubrias and co-workers (23) used MRI and reported a 21% decrease in NF of the knee extensors at contraction speeds of 120°/s and greater, but not at 60°/s, in 42 men and women between the ages of 65 and 80 yr. In a large sample of men aged 19-91 yr, Lynch and co-workers (32) reported a decrease in isokinetic (30-45°/s) NF of 28 and 40% in the arm (EFs plus EEs) and thigh (knee flexors plus knee extensors) muscles, respectively, using dual-energy X-ray absorptiometry (DXA). The prevalence of a decline in isokinetic NF with age evident in previous studies, particularly at faster contraction speeds, may be due to a number of factors, including a decrease in fast-twitch fiber area (30), a decline in muscle activation, and increased coactivation (15, 22). The extent of the age-related decline in NF demonstrated in previous work may be related to the method used to measure muscle size as well as the general health, motivation, and physical activity level of the subjects. In the present study the subjects were equally motivated to give their best effort during the MVCs. This conclusion is based on the small day-to-day variability of the MVC and activation level. As well, the subjects were healthy and not highly trained and the nondominant arm was measured in all cases. Thus the group differences in PCSA, strength, and NF are more likely related to the effects of aging per se rather than to differences in physical activity level, although we have no direct measures of activity level. More importantly, the large age-related deficits (27-40%) in NF reported in some studies (8, 32, 46) could be exaggerated because the techniques that were used may not have adequately distinguished muscle and noncontractile tissue. Because the noncontractile tissue is increased in the elderly (43), ultrasound (46), DXA (29, 32), and less direct techniques (8) may overestimate muscle size and thereby underestimate NF. For example, Lynch et al. (32) reported a 20% decrease in arm and thigh muscle mass between young and old (>80 yr) men with DXA. In the present study, we found a 20-28% decrease in EF and EE PCSA and Lexell et al. (30) reported a 45% decrease in the ACSA of the vastus lateralis muscle in cadavers across the same age range. A 45% decrease in ACSA would be enough to account for all of the strength loss commonly reported in the knee extensors (41). The age-related deficit (15-25%) in specific tension of whole animal muscle may also be exaggerated because noncontractile tissue was not accounted for in the ACSA measurements (7, 28). Ansved and Larsson (5), however, measured specific tension with (ACSA minus total fiber area) and without (muscle wet weight) correction for noncontractile tissue in young and old rats. Specific tension was reduced by 20% in the old rats when wet weight was used but was unaffected when noncontractile tissue was accounted for. Thus it may be that NF and whole muscle specific tension during isometric contractions are not greatly impaired when adequate techniques are used to measure muscle size. The EEs were ~10-20% weaker than the EFs in both groups despite having almost twice the PCSA. This resulted in a lower NF in the EEs compared with the EFs by almost 50%. Part of the difference in NF between the muscle groups is because the pronator teres and the extensor carpi radialis longus muscles, which can function as elbow flexors, were not included in the EF volume. Consequently, NF of the EFs was likely overestimated by ~15% in the present study (38). A more important factor contributing to the lower NF in the EEs compared with the EFs is the smaller moment arm length of the triceps brachii compared with the EFs (38). We have since confirmed using MRI that the moment arm length of the triceps brachii is approximately one-half that of the EFs in young and old men and that the specific tension of the two muscle groups is similar (25). In conclusion, isometric strength and PCSA of the EFs and EEs were reduced in old compared with young men. The percent loss in strength and PCSA with old age was similar in the EEs resulting in an unchanged NF for this muscle group. In contrast, since strength was reduced more than PCSA, the NF of the EFs was reduced in the old men compared with the young men. Possible mechanisms that may contribute to the lower NF of the EFs include an increase in coactivation, or a decline in specific tension of the muscle fibers.| |
ACKNOWLEDGEMENTS |
|---|
We acknowledge the assistance of Jean Theberge in the acquisition of the magnetic resonance images. We also thank Brian Allman and Dr. Jennifer Jakobi for assistance during pilot testing and reading an earlier draft of the manuscript. Finally, we are grateful to all the subjects who participated in this study.
| |
FOOTNOTES |
|---|
This work was supported by the National Sciences and Engineering Research Council of Canada, St. Joseph's Health Centre, and the Academic Development Fund of the University of Western Ontario. C. S. Klein was a recipient of an Ontario Graduate Scholarship in Science and Technology during the course of this study.
Address for correspondence: C. L. Rice, Canadian Centre for Activity and Aging, St. Joseph's Health Center Annex, 1490 Richmond St., London, ON, Canada N6G 2M3.
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. Section 1734 solely to indicate this fact.
Received 5 March 2001; accepted in final form 18 May 2001.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Allen, GM,
McKenzie DK,
and
Gandevia SC.
Twitch interpolation of the elbow flexor muscles at high forces.
Muscle Nerve
21:
318-328,
1998[ISI][Medline].
2.
Alway, SE,
Coggan AR,
Sproul MS,
Abduljalil AM,
and
Robitaille PM.
Muscle torque in young and older untrained and endurance-trained men.
J Gerontol A Biol Sci Med Sci
51:
195-201,
1996.
3.
Amis, AA,
Dowson D,
and
Wright V.
Muscle strengths and musculo-skeletal geometry of the upper limb.
Eng Med
8:
41-48,
1979.
4.
An, KN,
Hui FC,
Morrey BF,
Linscheid RL,
and
Chao EY.
Muscles across the elbow joint: a biomechanical analysis.
J Biomech
14:
659-669,
1981[ISI][Medline].
5.
Ansved, T,
and
Larsson L.
Effects of ageing on enzyme-histochemical, morphometrical and contractile properties of the soleus muscle in the rat.
J Neurol Sci
93:
105-124,
1989[ISI][Medline].
6.
Awiszus, F,
Wahl B,
and
Meinecke I.
Influence of stimulus cross talk on results of the twitch-interpolation technique at the biceps brachii muscle.
Muscle Nerve
20:
1187-1190,
1997[Medline].
7.
Brooks, SV,
and
Faulkner JA.
Contractile properties of skeletal muscles from young, adult and aged mice.
J Physiol (Lond)
404:
71-82,
1988
8.
Bruce, SA,
Newton D,
and
Woledge RC.
Effect of age on voluntary force and cross-sectional area of human adductor pollicis muscle.
Q J Exp Physiol
74:
359-362,
1989
9.
De Serres, SJ,
and
Enoka RM.
Older adults can maximally activate the biceps brachii muscle by voluntary command.
J Appl Physiol
84:
284-291,
1998
10.
Doherty, TJ,
Vandervoort AA,
Taylor AW,
and
Brown WF.
Effects of motor unit losses on strength in older men and women.
J Appl Physiol
74:
868-874,
1993
11.
Frontera, WR,
Suh D,
Krivickas LS,
Hughes VA,
Goldstein R,
and
Roubenoff R.
Skeletal muscle fiber quality in older men and women.
Am J Physiol Cell Physiol
279:
C611-C618,
2000
12.
Fukunaga, T,
Roy RR,
Shellock FG,
Hodgson JA,
and
Edgerton VR.
Specific tension of human plantar flexors and dorsiflexors.
J Appl Physiol
80:
158-165,
1996
13.
Graves, AE,
Kornatz KW,
and
Enoka RM.
Older adults use a unique strategy to lift inertial loads with the elbow flexor muscles.
J Neurophysiol
83:
2030-2039,
2000
14.
Grimby, G,
Danneskiold-Samsoe B,
Hvid K,
and
Saltin B.
Morphology and enzymatic capacity in arm and leg muscles in 78-81 year old men and women.
Acta Physiol Scand
115:
125-134,
1984.
15.
Hakkinen, K,
Alen M,
Kallinen M,
Izquierdo M,
Jokelainen K,
Lassila H,
Malkia E,
Kraemer WJ,
and
Newton RU.
Muscle CSA, force production, and activation of leg extensors during isometric and dynamic actions in middle-aged and elderly men and women.
J Aging Phys Act
6:
232-247,
1998[ISI].
16.
Hakkinen, K,
Kraemer WJ,
Kallinen M,
Linnamo V,
Pastinen UM,
and
Newton RU.
Bilateral and unilateral neuromuscular function and muscle cross-sectional area in middle-aged and elderly men and women.
J Gerontol A Biol Sci Med Sci
51:
B21-B29,
1996[Abstract].
17.
Herbert, RD,
and
Gandevia SC.
Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation.
J Neurophysiol
82:
2271-2283,
1999
18.
Hooper, AC.
Length, diameter and number of ageing skeletal muscle fibres.
Gerontology
27:
121-126,
1981[ISI][Medline].
19.
Hortobagyi, T,
and
DeVita P.
Muscle pre- and coactivity during downward stepping are associated with leg stiffness in aging.
J Electromyogr Kinesiol
10:
117-126,
2000[ISI][Medline].
20.
Huijing, PA.
Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb.
J Biomech
32:
329-345,
1999[ISI][Medline].
21.
Ichinose, Y,
Kanehisa H,
Ito M,
Kawakami Y,
and
Fukunga T.
Relationship between muscle fiber pennation and force generation capability in Olympic athletes.
Int J Sports Med
19:
541-546,
1998[Medline].
22.
Izquierdo, M,
Ibanez J,
Gorostiaga E,
Garrues M,
Zuniga A,
Anton A,
Larrion JL,
and
Hakkinen K.
Maximal strength and power characteristics in isometric and dynamic actions of the upper and lower extremities in middle-aged and older men.
Acta Physiol Scand
167:
57-68,
1999[ISI][Medline].
23.
Jubrias, SA,
Odderson IR,
Esselman PC,
and
Conley KE.
Decline in isokinetic force with age: muscle cross-sectional area and specific force.
Pflügers Arch
434:
246-253,
1997[ISI][Medline].
24.
Kawakami, Y,
Abe T,
and
Fukunaga T.
Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles.
J Appl Physiol
74:
2740-2744,
1993
25.
Kawakami, Y,
Nakazawa K,
Fujimoto T,
Nozaki D,
Miyashita M,
and
Fukunaga T.
Specific tension of elbow flexor and extensor muscles based on magnetic resonance imaging.
Eur J Appl Physiol
68:
139-147,
1994.
26.
Kent-Braun, JA,
and
Ng AV.
Specific strength and voluntary muscle activation in young and elderly women and men.
J Appl Physiol
87:
22-29,
1999
27.
Klitgaard, H,
Mantoni M,
Schiaffino S,
Ausoni S,
Gorza L,
Laurent-Winter C,
Schnohr P,
and
Saltin B.
Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds.
Acta Physiol Scand
140:
41-54,
1990[ISI][Medline].
28.
Klitgaard, H,
Marc R,
Brunet A,
Vandewalle H,
and
Monod H.
Contractile properties of old rat muscles: effect of increased use.
J Appl Physiol
67:
1401-1408,
1989
29.
Levine, JA,
Abboud L,
Barry M,
Reed JE,
Sheedy PF,
and
Jensen MD.
Measuring leg muscle and fat mass in humans: comparison of CT and dual-energy X-ray absorptiometry.
J Appl Physiol
88:
452-456,
2000
30.
Lexell, J,
Taylor CC,
and
Sjostrom M.
What is the cause of the ageing 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[ISI][Medline].
31.
Lieber, RL,
and
Friden J.
Functional and clinical significance of skeletal muscle architecture.
Muscle Nerve
23:
1647-1666,
2000[ISI][Medline].
32.
Lynch, NA,
Metter EJ,
Lindle RS,
Fozard JL,
Tobin JD,
Roy TA,
Fleg JL,
and
Hurley BF.
Muscle quality. I. Age-associated differences between arm and leg muscle groups.
J Appl Physiol
86:
188-194,
1999
33.
MacDougall, JD,
Elder GC,
Sale DG,
Moroz JR,
and
Sutton JR.
Effects of strength training and immobilization on human muscle fibres.
Eur J Appl Physiol
43:
25-34,
1980.
34.
MacDougall, JD,
Sale DG,
Alway SE,
and
Sutton JR.
Muscle fiber number in biceps brachii in bodybuilders and control subjects.
J Appl Physiol
57:
1399-1403,
1984
35.
McCall, GE,
Byrnes WC,
Dickinson A,
Pattany PM,
and
Fleck SJ.
Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training.
J Appl Physiol
81:
2004-2012,
1996
36.
McDonagh, MJ,
White MJ,
and
Davies CT.
Different effects of ageing on the mechanical properties of human arm and leg muscles.
Gerontology
30:
49-54,
1984[ISI][Medline].
37.
Mitsiopoulos, N,
Baumgartner RN,
Heymsfield SB,
Lyons W,
Gallagher D,
and
Ross R.
Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography.
J Appl Physiol
85:
115-122,
1998
38.
Murray, WM,
Buchanan TS,
and
Delp SL.
The isometric functional capacity of muscles that cross the elbow.
J Biomech
33:
943-952,
2000[ISI][Medline].
39.
Narici, MV,
Capodaglio P,
Minetti AE,
Ferrari-Bardile A,
Maini M,
and
Cerretelli P.
Changes in human skeletal muscle architecture induced by disuse-atrophy (Abstract).
J Physiol (Lond)
506P:
59P,
1998.
40.
Overend, TJ,
Cunningham DA,
Kramer JF,
Lefcoe MS,
and
Paterson DH.
Knee extensor and knee flexor strength: cross-sectional area ratios in young and elderly men.
J Gerontol A Biol Sci Med Sci
47:
M204-M210,
1992.
41.
Porter, MM,
Vandervoort AA,
and
Lexell J.
Aging of human muscle: structure, function and adaptability.
Scand J Med Sci Sports
5:
129-142,
1995[Medline].
42.
Powell, PL,
Roy RR,
Kanim P,
Bello MA,
and
Edgerton VR.
Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs.
J Appl Physiol
57:
1715-1721,
1984
43.
Rice, CL,
Cunningham DA,
Paterson DH,
and
Lefcoe MS.
Arm and leg composition determined by computed tomography in young and elderly men.
Clin Physiol
9:
207-220,
1989[ISI][Medline].
44.
Singh, M,
and
Kapovich PV.
Isotonic and isometric forces of the forearm flexors and extensors.
J Appl Physiol
21:
1435-1437,
1966
45.
Thomas, CK,
Tucker ME,
and
Bigland-Ritchie B.
Voluntary muscle weakness and co-activation after chronic cervical spinal cord injury.
J Neurotrauma
15:
149-161,
1998[ISI][Medline].
46.
Vandervoort, AA,
and
McComas AJ.
Contractile changes in opposing muscles of the human ankle joint.
J Appl Physiol
61:
361-367,
1986
47.
Veeger, HE,
Van der Helm FC,
Van der Woude LH,
Pronk GM,
and
Rozendal RH.
Inertia and muscle contraction parameters for musculoskeletal modelling of the shoulder mechanism.
J Biomech
24:
615-29,
1991[ISI][Medline].
48.
Young, A,
Stokes M,
and
Crowe M.
The size and strength of the quadriceps muscles of old and young men.
Clin Physiol
5:
145-154,
1985[ISI][Medline].
49.
Yue, GH,
Ranganathan VK,
Siemionow V,
Liu JZ,
and
Sahgal V.
Older adults exhibit a reduced ability to fully activate their biceps brachii muscle.
J Gerontol A Biol Sci Med Sci
54:
M249-M253,
1999[Abstract].
This article has been cited by other articles:
|
|
 |
|
  M. Klass, S. Baudry, and J. Duchateau Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions J Appl Physiol, March 1, 2008; 104(3): 739 - 746. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. I. Morse, K. Tolfrey, J. M. Thom, V. Vassilopoulos, C. N. Maganaris, and M. V. Narici Gastrocnemius muscle specific force in boys and men J Appl Physiol, February 1, 2008; 104(2): 469 - 474. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. H. Chung, D. M. Callahan, and J. A. Kent-Braun Age-related resistance to skeletal muscle fatigue is preserved during ischemia J Appl Physiol, November 1, 2007; 103(5): 1628 - 1635. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. J. McNeil, A. A. Vandervoort, and C. L. Rice Peripheral impairments cause a progressive age-related loss of strength and velocity-dependent power in the dorsiflexors J Appl Physiol, May 1, 2007; 102(5): 1962 - 1968. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Suetta, P. Aagaard, S. P. Magnusson, L. L. Andersen, S. Sipila, A. Rosted, A. K. Jakobsen, B. Duus, and M. Kjaer Muscle size, neuromuscular activation, and rapid force characteristics in elderly men and women: effects of unilateral long-term disuse due to hip-osteoarthritis J Appl Physiol, March 1, 2007; 102(3): 942 - 948. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. D. Reeves, M. V. Narici, and C. N. Maganaris Myotendinous plasticity to ageing and resistance exercise in humans Exp Physiol, May 1, 2006; 91(3): 483 - 498. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. I. Morse, J. M. Thom, N. D. Reeves, K. M. Birch, and M. V. Narici In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men J Appl Physiol, September 1, 2005; 99(3): 1050 - 1055. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Klass, S. Baudry, and J. Duchateau Aging does not affect voluntary activation of the ankle dorsiflexors during isometric, concentric, and eccentric contractions J Appl Physiol, July 1, 2005; 99(1): 31 - 38. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Simoneau, A. Martin, and J. Van Hoecke Muscular Performances at the Ankle Joint in Young and Elderly Men J. Gerontol. A Biol. Sci. Med. Sci., April 1, 2005; 60(4): 439 - 447. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. G. Candow and P. D. Chilibeck Differences in Size, Strength, and Power of Upper and Lower Body Muscle Groups in Young and Older Men J. Gerontol. A Biol. Sci. Med. Sci., February 1, 2005; 60(2): 148 - 156. [Abstract] [Full Text] [PDF]
|
|
|
|
P < 0.05 compared with the biceps
brachii and brachioradialis in both the young and old.