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J Appl Physiol 95:2229-2234, 2003. First published Jul 3, 2003; doi:10.1152/japplphysiol.00433.2003

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Effect of aging on human muscle architecture
M. V. Narici,1 C. N. Maganaris,1 N. D. Reeves,1 and P. Capodaglio2
1
Centre for Biophysical and Clinical Research into Human Movement (CRM), Manchester Metropolitan
University, Alsager Campus, Alsager, ST7 2HL, Cheshire, United Kingdom; and 2Centro Studi Attività
Motorie, Fondazione Salvatore Maugeri, via Ferrata 8, 2100 Pavia, Italy
Submitted 30 April 2003; accepted in final form 26 June 2003
Narici, M. V., C. N. Maganaris, N. D. Reeves, and P.
Capodaglio. Effect of aging on human muscle architecture.
J Appl Physiol 95: 2229–2234, 2003. First published July 3,
2003; 10.1152/japplphysiol.00433.2003.—The effect of aging
on human gastrocnemius medialis (GM) muscle architecture
was evaluated by comparing morphometric measurements
on 14 young (aged 27–42 yr) and on 16 older (aged 70–81 yr)
physically active men, matched for height, body mass, and
physical activity. GM muscle anatomic cross-sectional area
(ACSA) and volume (Vol) were measured by computerized
tomography, and GM fascicle length (Lf) and pennation angle
(␪) were assessed by ultrasonography. GM physiological
cross-sectional area (PCSA) was calculated as the ratio of
Vol/Lf. In the elderly, ACSA and Vol were, respectively,
19.1% (P ⬍ 0.005) and 25.4% (P ⬍ 0.001) smaller than in the
young adults. Also, Lf and ␪ were found to be smaller in the
elderly group by 10.2% (P ⬍ 0.01) and 13.2% (P ⬍ 0.01),
respectively. When the data for the young and elderly adults
were pooled together, ␪ significantly correlated with ACSA
(P ⬍ 0.05). Because of the reduced Vol and Lf in the elderly
group, the resulting PCSA was found to be 15.2% (P ⬍ 0.05)
smaller. In conclusion, this study demonstrates that aging
significantly affects human skeletal muscle architecture.
These structural alterations are expected to have implica-
tions for muscle function in old age.
skeletal muscle; muscle fiber; sarcopenia; muscle strength
AGING IS KNOWN TO BE ASSOCIATED with a reduction in
muscle mass (sarcopenia). Cross-sectional studies sug-
gest that this phenomenon starts toward the end of the
fifth decade of life (19), which also corresponds with the
onset of force decline (34). This loss of muscle mass is
greater for the muscles of the lower limbs than for the
upper limbs, and from 20 to 70⫹ yr of age, lower limb
muscle mass decreases by ⬃25% (19). When the cross-
sectional area (CSA) rather than muscle mass (or vol-
ume) of essential muscles of locomotion is considered, a
25–33% difference in quadriceps CSA is found between
young (20–29 yr) and elderly (70–81 yr) adults (27, 46).
However, several investigators (20, 23, 29, 40, 46), but
not some others (9), have observed a greater reduction
in strength than of muscle CSA so that force, or torque,
expressed per unit of muscle CSA, has been found to be
reduced in older individuals.
Original submission in response to a call for papers on
“Physiology of Aging.”
Address for reprint requests and other correspondence: M. V.
Narici, Centre for Biophysical and Clinical Research into Human
Movement (CRM), Manchester Metropolitan Univ., Alsager Campus,
Alsager, ST7 2HL, Cheshire, UK (E-mail: m.narici@mmu.ac.uk).
http://www.jap.org 8750-7587/03 $5.00 Copyright © 2003 the American Physiological Society
J Appl Physiol 95: 2229–2234, 2003.
First published July 3, 2003; 10.1152/japplphysiol.00433.2003.
These studies suggest that sarcopenia alone cannot
fully account for the observed loss of muscle strength
and that additional factors, such as a reduction in
motor unit activation capacity (12, 45), an increase in
the coactivation of antagonist muscles (22, 29), and a
decrease in single fiber-specific tension (26) also play a
role. However, the contribution of changes in muscle
architecture has seldom been considered. As a matter
of fact, most investigators comparing differences in
Downloaded from jap.physiology.org on November 14, 2008
strength and muscle size of young and elderly individ-
uals have related force (or torque) to the anatomic CSA
(ACSA) of the muscle, which is at right angles to the
muscle belly. However, in pennate muscles (as is the
case for most locomotor muscles) in which muscle fi-
bers run at an angle to the axis of traction of the
muscle, the ACSA does not represent the cross section
perpendicular to all fibers in the muscle, i.e., the phys-
iological CSA (PCSA) (28, 35, 42). In fact, the maxi-
mum force of a muscle depends on its PCSA rather
than its ACSA (1, 10, 13, 28, 35). Nevertheless, little is
known on how aging affects muscle architecture, de-
spite the fact that changes in muscle architecture could
potentially modify not only the maximum force-gener-
ating potential, dependent on the maximum number of
sarcomeres placed in parallel, but also the maximum
shortening velocity, which depends on the number of
sarcomeres placed in series. The present study aims to
demonstrate that sarcopenia not only involves a de-
crease in muscle mass but also entails changes in
muscle architecture. The study also addresses the
functional significance of these changes. Preliminary
data of this work have been presented elsewhere (37).
MATERIALS AND METHODS
Subjects. The investigation was conducted on 16 elderly
men aged 70–81 yr (height, 1.72 ⫾ 0.03 m; body mass, 74.5 ⫾
8.3 kg) and, for comparison, on 14 younger men aged 27–42
yr (height, 1.73 ⫾ 0.09 m; body mass, 73.2 ⫾ 10.4 kg). The
investigation was approved by the Ethics Committee of the
Salvatore Maugeri Foundation, and each individual gave
written, informed consent to the investigation after being
advised about the nature and purpose of the study. Most of
the elderly participants were members of the University of
the Third Age of the town of Pavia, whereas the younger
participants were recruited from among friends and col-
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.
2229
2230 AGING AND HUMAN MUSCLE ARCHITECTURE
leagues. Exclusion criteria for subject participation in the
study included known muscular, neurological, metabolic, and
inflammatory disease; uncontrolled hypertension; or angina.
Particular care was taken in recruiting young and elderly
individuals with similar activity levels and body stature. The
individuals selected for this investigation (both young and
elderly) were recreationally active, some belonging to walk-
ing clubs, some to aerobic and flexibility classes, some prac-
ticing ballroom dancing or using bicycle for transport, but
none was engaged in sporting activities at competitive level.
The number of hours spent in recreational activities was
assessed by use of the Saint-Etienne Physical Activity Ques-
tionnaire (3) validated in young and elderly individuals (5).
The participation in recreational activities expressed as
number of hours per week was similar in the two groups,
8.6 ⫾ 2.6 (range 5.3–12.8) in the young adults and 7.9 ⫾ 3.1
(range 3.7–14.0) in the older individuals, with no significant
differences between the two groups (P ⬎ 0.05, Mann-Whitney
rank-sum test).
Muscle ACSA and volume measurements. GM ACSA was
measured by computerized tomography. The subjects were
positioned supine in a General Electric scanner (ProSpeed Sx
power) operating at 120 kV peak, with the legs relaxed. The
ACSAs of 40 contiguous 10-mm slices (50-cm field of view,
matrix 512 ⫻ 512 pixels), with 0-mm interslice gap, were
obtained starting from the knee space (slice 1). For each axial
slice, ACSA computation (mean of three consecutive morpho-
metric measurements on the same MRI slice) was carried out
on the GM muscle. Calculation of muscle ACSA was per-
formed by digitizing throughout the muscle contour by use of
an image-analysis program (NIH Image version 1.61/ppc,
National Institutes of Health, Bethesda, MD). The maximum
ACSA of the GM, normally corresponding to the fifth or sixth
axial scan distal to the knee space, was selected for data
analysis. The error in this technique, evaluated by digitizing
shapes of known areas, was estimated to be 2.1%, whereas
the coefficient of variation for three ACSA measurements,
repeated on the same subject on 6 different days, was 2.6%.
For GM muscle volume (Vol) calculation, all slices were
fitted with a spline algorithm to interpolate for missing slices
between the minimum measurable CSA at the proximal and
distal ends of the muscle and the theoretical slice where the
proximal and distal CSAs of the GM would be equal to zero.
The total Vol was then calculated by adding the individual
ACSA of each image and multiplying the sum by the slice
thickness (10 mm) (36).
Muscle architecture. The participants were asked to rest
prone on an examination table with legs relaxed and both
feet hanging outside the table. A plastic cast shaped to the
sole of the foot and calcaneus and extending 10 cm above the
malleolus was taped to the dominant foot to standardize
measurements at the same resting ankle joint angle. The
tibiotalar joint angle chosen for this investigation was 115°
(90° being the angle when the foot is perpendicular to the
tibia). In both young and older participants, the above angle
corresponded to the spontaneous resting angle of the tibiota-
lar joint; hence the positioning of the foot in the cast did not
require any active force by the operator. Resting fascicle
length (Lf) and pennation angle (␪) were measured by real-
time ultrasound (HDI-3000, ATL, Bothell). Images were ob-
tained at midbelly of the dominant GM muscle by using a
7.5-MHz linear-array probe, 38 mm long. The probe was
positioned perpendicular to the dermal surface of the GM
muscle and oriented along the median longitudinal plane of
the muscle. Midbelly was defined as the point along the
median longitudinal axis of the muscle at 50% of the distance
between the proximal and distal apexes of the myotendinous
J Appl Physiol • VOL 95 • DECEMBER 2003 •
junctions. The center of the probe was aligned to this posi-
tion. The probe was coated with a water-soluble transmission
gel to provide acoustic contact without depressing the dermal
surface. Three images at rest were obtained within the same
experimental session in each individual. The ␪ was measured
as the angle of insertion of muscle fiber fascicles into the deep
aponeurosis, and Lf was defined as the length of the fascicu-
lar path between the insertions of the fascicle into the supe-
rior and deep aponeuroses. In cases in which the fascicle
extended off the acquired ultrasound image, the length of the
missing portion of the fascicle was estimated by extrapolat-
ing linearly both the fascicular path, visible in the image, and
the aponeurosis. The error introduced by this technique de-
pends primarily on the degree of curvature of the fascicle. We
recently showed in the tibialis anterior muscle that, during
contraction, when the curvature of the fascicles is greater
than at rest, our linear extrapolation approach results in an
error of only 2.4% (41). The error made in the present study
would be even smaller because resting fascicles present neg-
ligible curvature (32, 33). PCSA (cm2) was calculated as the
ratio between Vol (cm3) and Lf (cm) (1, 8, 16, 31, 42).
The accuracy of the ultrasound method in measuring the
Downloaded from jap.physiology.org on November 14, 2008
architectural features of the human GM muscle has been
previously tested against direct anatomic measurement on a
cadaver and found to be in good agreement (36): in the
central region of the muscle, Lf and ␪ differed by an average
of 1.2 mm and 1.5°, respectively, between the two techniques.
Images were captured with a video-capture card (Capsure,
iREZ Research) interfaced with a Macintosh Powerbook G3
computer. They were then frozen and saved on the hard disk
of the computer. Data analysis was performed with the same
digitizing software used for the ACSA determination, men-
tioned above. The mean of three consecutive morphometric
analyses of each image was used for data analysis. The
architectural measurements were performed by an investi-
gator blinded to subject identity.
Statistics. Data are presented as means ⫾ SD. Age-related
differences for all measurements were analyzed with the
independent-samples Student’s t-test. In those cases (hours
spent in recreational activities) in which the data did not
meet the criteria of normality (Shapiro-Wilks W test, P ⬍
0.05), a nonparametric Mann-Whitney rank-sum test was
applied. Linear regression analysis (Pearson’s product-mo-
ment correlation) was used to compare the degree of associ-
ation between variables. The critical level for statistical sig-
nificance was set at 5%.
RESULTS
GM muscle’s maximum ACSA (ACSAmax), Vol, Lf, ␪,
and PCSA of the elderly and young adult populations
are presented in Table 1. All the investigated muscle
architectural parameters were reduced in the elderly
compared with the younger adults.
The differences between the elderly and younger
groups were 19.1% (P ⬍ 0.005) for ACSAmax, 25.3%
(P ⬍ 0.001) for Vol, 10.2% (P ⬍ 0.01) for Lf, 13.2% (P ⬍
0.01) for ␪, and 15.2% (P ⬍ 0.05) for PCSA. When ␪ was
plotted against ACSA (Fig. 1), and the experimental
data points were fitted with a linear function, a signif-
icant correlation (r ⫽ 0.432, P ⬍ 0.05) was found
between the two variables, indicating that ␪ scales
with ACSAmax. Also, it is noteworthy that in most
elderly individuals values of both ACSAmax and ␪ were
smaller than in the younger adults.
www.jap.org
 AGING AND HUMAN MUSCLE ARCHITECTURE
Table 1. Summary of gastrocnemius medialis architectural data in young and elderly individuals
ACSAmax, cm2 Vol, cm3
Elderly 14.0 ⫾ 3.6 208.7 ⫾ 48.5
Young 17.4 ⫾ 2.8 279.3 ⫾ 59.3
Difference 19.1% 25.3%
P values (t-test) 0.005 0.001
Values are means ⫾ SD; n ⫽ 14 for the young (27–42 yr) group and n ⫽ 16 for the elderly (70–81 yr) group. ACSAmax, maximum anatomic
cross-sectional area; Vol, muscle volume; Lf, fascicle length; ␪, pennation angle; PCSA, physiological cross-sectional area.
Although the difference in ACSAmax seemed greater
than that of PCSA (Table 1), no significant difference
was found between the ratios of ACSAmax to PCSA of
the young (0.30 ⫾ 0.04) and those of the elderly sub-
jects (0.29 ⫾ 0.06, not significant). When the values of
ACSAsmax and PCSAs of the young and elderly sub-
jects were pooled together, a significant correlation
(r ⫽ 0.759, P ⬍ 0.01) was found between ACSAmax and
PCSA (see Fig. 2).
DISCUSSION
The present study demonstrates for the first time
that human GM muscle architecture is significantly
altered in old age. Because the elderly individuals
specifically selected for this study were physically ac-
tive and had daily energy expenditures similar to those
of the younger adult group, the possibility that these
alterations in muscle architecture were due to disuse
seems quite unlikely. Hence, we trust that these
changes are mostly attributable to the effect of aging
per se rather than to disuse. Furthermore, in this
study, particular care was taken in recruiting elderly
and young individuals matched for height to avoid
differences in muscle architecture due to a simple scal-
Fig. 1. Individual data of maximum anatomic cross-sectional area
(ACSA) plotted against pennation angle for the young adults (F) and
elderly individuals (E). Data are fitted with a linear regression
function after the values for the young and elderly subjects were
pooled together.
J Appl Physiol • VOL
2231
Lf, cm ␪,° PCSA (Vol/Lf), cm2
4.29 ⫾ 0.67 23.6 ⫾ 3.0 50.1 ⫾ 12.6
4.78 ⫾ 0.55 27.2 ⫾ 4.3 59.1 ⫾ 14.4
10.2% 13.2% 15.2%
0.01 0.01 0.05
ing phenomenon. A different approach was, instead,
followed by Kubo et al. (24, 25), who recently investi-
gated muscle architecture in sedentary young and el-
derly men and women not matched for height and
physical activity status. Interestingly, after normaliza-
tion of the measurement to limb segment length, Kubo
et al. (24) found differences in Lf and ␪ between young
and elderly subjects for the vastus lateralis muscle but
not for the GM and triceps brachii muscles. The lack of
physical activity matching between subjects makes it
Downloaded from jap.physiology.org on November 14, 2008
difficult to ascertain whether the above differences
were due to aging per se or the combined effect of aging
and disuse. The absence of architectural changes in the
GM was attributed by Kubo et al. (24) to a greater use
of the plantarflexors compared with the knee extensors
in locomotor activities or to a different plasticity of
these two muscles in response to aging. However, our
results demonstrate that, when the influence of disuse
is controlled for by matching individuals for physical
activity level, significant alterations in the architec-
ture of the GM muscle are observed; that is to say,
changes in plantarflexor muscle architecture do occur
in old age, even in active elderly individuals. Besides,
the approach followed by Kubo et al. (24) to scale Lf to
limb length does not fully eliminate the effect of differ-
ent body dimension on muscle architecture. This is
because taller individuals will have a greater body
mass that would place a greater mechanical load on
weight-bearing muscles such as the vastus lateralis
and GM. This mechanical stimulus is likely to affect ␪
and Lf, a factor that is accounted for by the approach
we employed to match the subjects for body height and
mass.
In the present study, muscle Vol, ACSAmax, Lf, and ␪
were all found to be significantly reduced in the older
individuals compared with the younger adults. As a
result of the decrease in muscle Vol (⫺25.3%) and in
fiber Lf (⫺10.2%), a reduction in PCSA was also found
(⫺15.2%). This decrease in PCSA was affected more by
the reduction in muscle Vol than by that in fiber
fascicle length. Nevertheless, the fact that both of these
decrease strongly suggests that sarcopenia involves a
loss of sarcomeres not only in parallel but also in
series. Hence, the decrease in PCSA is likely to be a
primary factor for the well-documented decrease in
contractile force-generating potential in old age (20, 23,
29, 40, 46). This major role of the reduction in PCSA in
the loss of muscle strength in old age was also shown in
the arm muscles by Klein et al. (22). However, in this
case, PCSA was estimated by dividing muscle Vol,
95 • DECEMBER 2003 • www.jap.org
2232 AGING AND HUMAN MUSCLE ARCHITECTURE
Fig. 2. Typical sonographs of the gas-
trocnemius medialis muscle of an el-
derly man (A) and of a young man (B).
determined by MRI, by Lf estimated from the ratio of
fiber length to muscle length published in the litera-
ture, thereby assuming that the ratio of fiber length to
muscle length does not change with age. A secondary
factor could be the decreased tensile stiffness of the
in-series tendon in old age (30, 39), which would result
in a leftward shift of the length-tension relation (48).
However, it could be argued that this secondary dete-
riorating effect might be partly cancelled out by the
decrease in the total number of serial sarcomeres, as
indicated by the present results, which theoretically
would shift rightward the length-tension relation of
the muscle. Other factors accounting for the reduced
force-generating potential in old age would be a de-
crease in single fiber-specific tension (26), an increased
antagonist muscle coactivation (11, 17, 29), and in
some cases a reduced muscle activation capacity (4, 12,
47), not always found (6, 7, 18, 22, 43).
Assuming a linear relationship between in-series
sarcomere number and Lf (14), it follows from previous
reports on human cadaver GM architecture measure-
ments (16) that the number of sarcomeres in series
would be ⬃14,540 in the elderly (for a Lf of 4.29 cm)
and ⬃16,200 in the younger adults (for a Lf of 4.78 cm).
This difference in sarcomere number predicts that, in
these elderly individuals, the maximum shortening
velocity of the GM fascicles should be at least 10%
lower than in the younger adults. Nevertheless, the
actual reduction in maximum shortening velocity in
the elderly is likely to be greater given that 1) the
intrinsic maximum speed of shortening of (the most
abundant) type I myosin heavy chain isoform is signif-
icantly lower in old age (15), 2) antagonist muscle
coactivation is greater in old age (22, 29), and 3) tendon
stiffness decreases in old age (30, 39). Because of the
reduction in PCSA (and thus of maximum isometric
force) and in fiber Lf (and thus of maximum shortening
velocity), the maximum muscle power is also expected
to be reduced in the elderly. However, considering that
in elderly subjects PCSA and Lf were, respectively, 85
and 90% of those found in the young adults, the data
predict a greater reduction in isometric force than in
maximum shortening velocity. As a result, the opti-
mum velocity for peak power generation is also ex-
J Appl Physiol • VOL
pected to be lower in the elderly than in the young
adults.
At present, without the use of labeling with radioac-
Downloaded from jap.physiology.org on November 14, 2008
tive markers such as [3H]adenosine injected into the
muscle, it is difficult to speculate on the mechanisms
leading to this decrease in Lf in aged muscle. However,
it seems plausible that the removal of sarcomeres in
series occurs at the distal and proximal ends of the
fascicles, through mechanisms similar to those medi-
ating the loss of sarcomeres in series in disuse due to
immobilization (44).
In the elderly, fascicles were found to be not only
shorter but also less pennate than in the younger
adults. This effect is likely due to the decrease in
contractile tissue packed along the tendon aponeuroses
and is similar to that observed in disuse atrophy (38).
For both sarcopenia and disuse atrophy, this phenom-
enon is probably due to the decrease in fiber size;
however, in sarcopenia an additional decrease in ␪
should be expected owing to the reduction in fiber
number (27). It seems that both sarcopenia and disuse
atrophy involve changes in ␪ that are diametrically
opposite to those found in hypertrophy, which is char-
acterized by an increase in ␪ (21). A decrease in ␪ with
muscle atrophy was predicted as early as in 1952 by
Benninghoff and Rollhäuser (2) and was thought to
give fibers a slight mechanical advantage due to a more
effective force transmission to the tendon during con-
traction (10). Given that the resting ␪ is one of the
factors determining the ␪ during contraction, quantify-
ing architectural differences between subjects in the
resting state is important to identify the origin of the
respective differences in architectural changes on con-
traction.
Although in this study a significant correlation was
found between ACSA and PCSA, the coefficient of de-
termination (R2) was 0.576, indicating that ⬍60% of
the variance in ACSA is explained by the variance in
PCSA. This suggests that ACSA and PCSA should not
be used interchangeably, particularly when normaliz-
ing force per CSA for estimating specific force, known
to strictly depend on PCSA.
In conclusion, this study demonstrates that human
GM architecture is significantly altered by aging. The
95 • DECEMBER 2003 • www.jap.org
 AGING AND HUMAN MUSCLE ARCHITECTURE
findings suggest that sarcopenia not only involves a
loss of sarcomeres in parallel but also in series. These
architectural changes are believed to play a significant
role in the loss of muscle function in old age because
they are likely to affect the length-tension as well as
the force-velocity and power-velocity relations of this
muscle on which common daily functions such as walk-
ing and stair negotiation depend.
The authors appreciate the collaboration of Dr. Edda Capodaglio
in the screening of subjects for physical activity. We are also indebted
to the participants of this study, particularly the senior volunteers,
for the commitment and time given to this project.
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