M. V. Narici, C. N. Maganaris, N. D. Reeves and P.

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

You might find this additional information useful...

This article cites 43 articles, 19 of which you can access free at:
http://jap.physiology.org/cgi/content/full/95/6/2229#BIBL

This article has been cited by 11 other HighWire hosted articles, the first 5 are:
Resistance training induces qualitative changes in muscle morphology, muscle
architecture, and muscle function in elderly postoperative patients
C. Suetta, J. L. Andersen, U. Dalgas, J. Berget, S. Koskinen, P. Aagaard, S. P. Magnusson and
M. Kjaer
J Appl Physiol, July 1, 2008; 105 (1): 180-186.
[Abstract] [Full Text] [PDF]

Influence of concentric and eccentric resistance training on architectural adaptation in

human quadriceps muscles
A. J. Blazevich, D. Cannavan, D. R. Coleman and S. Horne
J Appl Physiol, November 1, 2007; 103 (5): 1565-1575.
[Abstract] [Full Text] [PDF]

Downloaded from jap.physiology.org on November 14, 2008

Age-related neuromuscular function during drop jumps
M. Hoffren, M. Ishikawa and P. V. Komi
J Appl Physiol, October 1, 2007; 103 (4): 1276-1283.
[Abstract] [Full Text] [PDF]

Peripheral impairments cause a progressive age-related loss of strength and

velocity-dependent power in the dorsiflexors
C. J. McNeil, A. A. Vandervoort and C. L. Rice
J Appl Physiol, May 1, 2007; 102 (5): 1962-1968.
[Abstract] [Full Text] [PDF]

Myotendinous plasticity to ageing and resistance exercise in humans

N. D. Reeves, M. V. Narici and C. N. Maganaris
Exp Physiol, May 1, 2006; 91 (3): 483-498.
[Abstract] [Full Text] [PDF]

Updated information and services including high-resolution figures, can be found at:
http://jap.physiology.org/cgi/content/full/95/6/2229

Additional material and information about Journal of Applied Physiology can be found at:
http://www.the-aps.org/publications/jappl

This information is current as of November 14, 2008 .

Journal of Applied Physiology publishes original papers that deal with diverse areas of research in applied physiology, especially
those papers emphasizing adaptive and integrative mechanisms. It is published 12 times a year (monthly) by the American
Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2005 by the American Physiological Society.
ISSN: 8750-7587, ESSN: 1522-1601. Visit our website at http://www.the-aps.org/.
 J Appl Physiol 95: 2229–2234, 2003.
First published July 3, 2003; 10.1152/japplphysiol.00433.2003.

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. These studies suggest that sarcopenia alone cannot
Capodaglio. Effect of aging on human muscle architecture. fully account for the observed loss of muscle strength
J Appl Physiol 95: 2229–2234, 2003. First published July 3, and that additional factors, such as a reduction in
2003; 10.1152/japplphysiol.00433.2003.—The effect of aging motor unit activation capacity (12, 45), an increase in
on human gastrocnemius medialis (GM) muscle architecture
the coactivation of antagonist muscles (22, 29), and a
was evaluated by comparing morphometric measurements
on 14 young (aged 27–42 yr) and on 16 older (aged 70–81 yr) decrease in single fiber-specific tension (26) also play a
physically active men, matched for height, body mass, and role. However, the contribution of changes in muscle
physical activity. GM muscle anatomic cross-sectional area architecture has seldom been considered. As a matter
(ACSA) and volume (Vol) were measured by computerized of fact, most investigators comparing differences in

Downloaded from jap.physiology.org on November 14, 2008

tomography, and GM fascicle length (Lf) and pennation angle strength and muscle size of young and elderly individ-
(␪) were assessed by ultrasonography. GM physiological uals have related force (or torque) to the anatomic CSA
cross-sectional area (PCSA) was calculated as the ratio of (ACSA) of the muscle, which is at right angles to the
Vol/Lf. In the elderly, ACSA and Vol were, respectively, muscle belly. However, in pennate muscles (as is the
19.1% (P ⬍ 0.005) and 25.4% (P ⬍ 0.001) smaller than in the case for most locomotor muscles) in which muscle fi-
young adults. Also, Lf and ␪ were found to be smaller in the bers run at an angle to the axis of traction of 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
muscle, the ACSA does not represent the cross section
were pooled together, ␪ significantly correlated with ACSA perpendicular to all fibers in the muscle, i.e., the phys-
(P ⬍ 0.05). Because of the reduced Vol and Lf in the elderly iological CSA (PCSA) (28, 35, 42). In fact, the maxi-
group, the resulting PCSA was found to be 15.2% (P ⬍ 0.05) mum force of a muscle depends on its PCSA rather
smaller. In conclusion, this study demonstrates that aging than its ACSA (1, 10, 13, 28, 35). Nevertheless, little is
significantly affects human skeletal muscle architecture. known on how aging affects muscle architecture, de-
These structural alterations are expected to have implica- spite the fact that changes in muscle architecture could
tions for muscle function in old age. potentially modify not only the maximum force-gener-
skeletal muscle; muscle fiber; sarcopenia; muscle strength ating potential, dependent on the maximum number of
sarcomeres placed in parallel, but also the maximum
shortening velocity, which depends on the number of
AGING IS KNOWN TO BE ASSOCIATED with a reduction in sarcomeres placed in series. The present study aims to
muscle mass (sarcopenia). Cross-sectional studies sug- demonstrate that sarcopenia not only involves a de-
gest that this phenomenon starts toward the end of the crease in muscle mass but also entails changes in
fifth decade of life (19), which also corresponds with the muscle architecture. The study also addresses the
onset of force decline (34). This loss of muscle mass is functional significance of these changes. Preliminary
greater for the muscles of the lower limbs than for the data of this work have been presented elsewhere (37).
upper limbs, and from 20 to 70⫹ yr of age, lower limb
MATERIALS AND METHODS
muscle mass decreases by ⬃25% (19). When the cross-
sectional area (CSA) rather than muscle mass (or vol- Subjects. The investigation was conducted on 16 elderly
ume) of essential muscles of locomotion is considered, a men aged 70–81 yr (height, 1.72 ⫾ 0.03 m; body mass, 74.5 ⫾
25–33% difference in quadriceps CSA is found between 8.3 kg) and, for comparison, on 14 younger men aged 27–42
young (20–29 yr) and elderly (70–81 yr) adults (27, 46). yr (height, 1.73 ⫾ 0.09 m; body mass, 73.2 ⫾ 10.4 kg). The
However, several investigators (20, 23, 29, 40, 46), but investigation was approved by the Ethics Committee of the
not some others (9), have observed a greater reduction Salvatore Maugeri Foundation, and each individual gave
written, informed consent to the investigation after being
in strength than of muscle CSA so that force, or torque, advised about the nature and purpose of the study. Most of
expressed per unit of muscle CSA, has been found to be the elderly participants were members of the University of
reduced in older individuals. the Third Age of the town of Pavia, whereas the younger
participants were recruited from among friends and col-
Original submission in response to a call for papers on
“Physiology of Aging.”
Address for reprint requests and other correspondence: M. V. The costs of publication of this article were defrayed in part by the
Narici, Centre for Biophysical and Clinical Research into Human payment of page charges. The article must therefore be hereby
Movement (CRM), Manchester Metropolitan Univ., Alsager Campus, marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
Alsager, ST7 2HL, Cheshire, UK (E-mail: [email protected]). solely to indicate this fact.

http://www.jap.org 8750-7587/03 $5.00 Copyright © 2003 the American Physiological Society 2229
2230 AGING AND HUMAN MUSCLE ARCHITECTURE

leagues. Exclusion criteria for subject participation in the junctions. The center of the probe was aligned to this posi-
study included known muscular, neurological, metabolic, and tion. The probe was coated with a water-soluble transmission
inflammatory disease; uncontrolled hypertension; or angina. gel to provide acoustic contact without depressing the dermal
Particular care was taken in recruiting young and elderly surface. Three images at rest were obtained within the same
individuals with similar activity levels and body stature. The experimental session in each individual. The ␪ was measured
individuals selected for this investigation (both young and as the angle of insertion of muscle fiber fascicles into the deep
elderly) were recreationally active, some belonging to walk- aponeurosis, and Lf was defined as the length of the fascicu-
ing clubs, some to aerobic and flexibility classes, some prac- lar path between the insertions of the fascicle into the supe-
ticing ballroom dancing or using bicycle for transport, but rior and deep aponeuroses. In cases in which the fascicle
none was engaged in sporting activities at competitive level. extended off the acquired ultrasound image, the length of the
The number of hours spent in recreational activities was missing portion of the fascicle was estimated by extrapolat-
assessed by use of the Saint-Etienne Physical Activity Ques- ing linearly both the fascicular path, visible in the image, and
tionnaire (3) validated in young and elderly individuals (5). the aponeurosis. The error introduced by this technique de-
The participation in recreational activities expressed as pends primarily on the degree of curvature of the fascicle. We
number of hours per week was similar in the two groups, recently showed in the tibialis anterior muscle that, during
8.6 ⫾ 2.6 (range 5.3–12.8) in the young adults and 7.9 ⫾ 3.1 contraction, when the curvature of the fascicles is greater
(range 3.7–14.0) in the older individuals, with no significant than at rest, our linear extrapolation approach results in an
differences between the two groups (P ⬎ 0.05, Mann-Whitney error of only 2.4% (41). The error made in the present study
rank-sum test). would be even smaller because resting fascicles present neg-
Muscle ACSA and volume measurements. GM ACSA was ligible curvature (32, 33). PCSA (cm2) was calculated as the
measured by computerized tomography. The subjects were ratio between Vol (cm3) and Lf (cm) (1, 8, 16, 31, 42).
positioned supine in a General Electric scanner (ProSpeed Sx The accuracy of the ultrasound method in measuring the

Downloaded from jap.physiology.org on November 14, 2008

power) operating at 120 kV peak, with the legs relaxed. The architectural features of the human GM muscle has been
ACSAs of 40 contiguous 10-mm slices (50-cm field of view, previously tested against direct anatomic measurement on a
matrix 512 ⫻ 512 pixels), with 0-mm interslice gap, were cadaver and found to be in good agreement (36): in the
obtained starting from the knee space (slice 1). For each axial central region of the muscle, Lf and ␪ differed by an average
slice, ACSA computation (mean of three consecutive morpho- of 1.2 mm and 1.5°, respectively, between the two techniques.
metric measurements on the same MRI slice) was carried out Images were captured with a video-capture card (Capsure,
on the GM muscle. Calculation of muscle ACSA was per- iREZ Research) interfaced with a Macintosh Powerbook G3
formed by digitizing throughout the muscle contour by use of computer. They were then frozen and saved on the hard disk
an image-analysis program (NIH Image version 1.61/ppc, of the computer. Data analysis was performed with the same
National Institutes of Health, Bethesda, MD). The maximum digitizing software used for the ACSA determination, men-
ACSA of the GM, normally corresponding to the fifth or sixth tioned above. The mean of three consecutive morphometric
axial scan distal to the knee space, was selected for data analyses of each image was used for data analysis. The
analysis. The error in this technique, evaluated by digitizing architectural measurements were performed by an investi-
shapes of known areas, was estimated to be 2.1%, whereas gator blinded to subject identity.
the coefficient of variation for three ACSA measurements, Statistics. Data are presented as means ⫾ SD. Age-related
repeated on the same subject on 6 different days, was 2.6%. differences for all measurements were analyzed with the
For GM muscle volume (Vol) calculation, all slices were independent-samples Student’s t-test. In those cases (hours
fitted with a spline algorithm to interpolate for missing slices spent in recreational activities) in which the data did not
between the minimum measurable CSA at the proximal and meet the criteria of normality (Shapiro-Wilks W test, P ⬍
distal ends of the muscle and the theoretical slice where the 0.05), a nonparametric Mann-Whitney rank-sum test was
proximal and distal CSAs of the GM would be equal to zero. applied. Linear regression analysis (Pearson’s product-mo-
The total Vol was then calculated by adding the individual ment correlation) was used to compare the degree of associ-
ACSA of each image and multiplying the sum by the slice ation between variables. The critical level for statistical sig-
thickness (10 mm) (36). nificance was set at 5%.
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 RESULTS
sole of the foot and calcaneus and extending 10 cm above the GM muscle’s maximum ACSA (ACSAmax), Vol, Lf, ␪,
malleolus was taped to the dominant foot to standardize
measurements at the same resting ankle joint angle. The
and PCSA of the elderly and young adult populations
tibiotalar joint angle chosen for this investigation was 115° are presented in Table 1. All the investigated muscle
(90° being the angle when the foot is perpendicular to the architectural parameters were reduced in the elderly
tibia). In both young and older participants, the above angle compared with the younger adults.
corresponded to the spontaneous resting angle of the tibiota- The differences between the elderly and younger
lar joint; hence the positioning of the foot in the cast did not groups were 19.1% (P ⬍ 0.005) for ACSAmax, 25.3%
require any active force by the operator. Resting fascicle (P ⬍ 0.001) for Vol, 10.2% (P ⬍ 0.01) for Lf, 13.2% (P ⬍
length (Lf) and pennation angle (␪) were measured by real- 0.01) for ␪, and 15.2% (P ⬍ 0.05) for PCSA. When ␪ was
time ultrasound (HDI-3000, ATL, Bothell). Images were ob- plotted against ACSA (Fig. 1), and the experimental
tained at midbelly of the dominant GM muscle by using a
data points were fitted with a linear function, a signif-
7.5-MHz linear-array probe, 38 mm long. The probe was
positioned perpendicular to the dermal surface of the GM icant correlation (r ⫽ 0.432, P ⬍ 0.05) was found
muscle and oriented along the median longitudinal plane of between the two variables, indicating that ␪ scales
the muscle. Midbelly was defined as the point along the with ACSAmax. Also, it is noteworthy that in most
median longitudinal axis of the muscle at 50% of the distance elderly individuals values of both ACSAmax and ␪ were
between the proximal and distal apexes of the myotendinous smaller than in the younger adults.
J Appl Physiol • VOL 95 • DECEMBER 2003 • www.jap.org
 AGING AND HUMAN MUSCLE ARCHITECTURE 2231

Table 1. Summary of gastrocnemius medialis architectural data in young and elderly individuals
ACSAmax, cm2 Vol, cm3 Lf, cm ␪,° PCSA (Vol/Lf), cm2

Elderly 14.0 ⫾ 3.6 208.7 ⫾ 48.5 4.29 ⫾ 0.67 23.6 ⫾ 3.0 50.1 ⫾ 12.6
Young 17.4 ⫾ 2.8 279.3 ⫾ 59.3 4.78 ⫾ 0.55 27.2 ⫾ 4.3 59.1 ⫾ 14.4
Difference 19.1% 25.3% 10.2% 13.2% 15.2%
P values (t-test) 0.005 0.001 0.01 0.01 0.05
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 ing phenomenon. A different approach was, instead,
than that of PCSA (Table 1), no significant difference followed by Kubo et al. (24, 25), who recently investi-
was found between the ratios of ACSAmax to PCSA of gated muscle architecture in sedentary young and el-
the young (0.30 ⫾ 0.04) and those of the elderly sub- derly men and women not matched for height and
jects (0.29 ⫾ 0.06, not significant). When the values of physical activity status. Interestingly, after normaliza-
ACSAsmax and PCSAs of the young and elderly sub- tion of the measurement to limb segment length, Kubo
jects were pooled together, a significant correlation et al. (24) found differences in Lf and ␪ between young
(r ⫽ 0.759, P ⬍ 0.01) was found between ACSAmax and and elderly subjects for the vastus lateralis muscle but
PCSA (see Fig. 2). 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

DISCUSSION
difficult to ascertain whether the above differences
The present study demonstrates for the first time were due to aging per se or the combined effect of aging
that human GM muscle architecture is significantly and disuse. The absence of architectural changes in the
altered in old age. Because the elderly individuals GM was attributed by Kubo et al. (24) to a greater use
specifically selected for this study were physically ac- of the plantarflexors compared with the knee extensors
tive and had daily energy expenditures similar to those in locomotor activities or to a different plasticity of
of the younger adult group, the possibility that these these two muscles in response to aging. However, our
alterations in muscle architecture were due to disuse results demonstrate that, when the influence of disuse
seems quite unlikely. Hence, we trust that these is controlled for by matching individuals for physical
changes are mostly attributable to the effect of aging activity level, significant alterations in the architec-
per se rather than to disuse. Furthermore, in this ture of the GM muscle are observed; that is to say,
study, particular care was taken in recruiting elderly changes in plantarflexor muscle architecture do occur
and young individuals matched for height to avoid in old age, even in active elderly individuals. Besides,
differences in muscle architecture due to a simple scal- 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,
Fig. 1. Individual data of maximum anatomic cross-sectional area 29, 40, 46). This major role of the reduction in PCSA in
(ACSA) plotted against pennation angle for the young adults (F) and
elderly individuals (E). Data are fitted with a linear regression
the loss of muscle strength in old age was also shown in
function after the values for the young and elderly subjects were the arm muscles by Klein et al. (22). However, in this
pooled together. case, PCSA was estimated by dividing muscle Vol,
J Appl Physiol • 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 pected to be lower in the elderly than in the young
fiber length to muscle length published in the litera- adults.
ture, thereby assuming that the ratio of fiber length to At present, without the use of labeling with radioac-

Downloaded from jap.physiology.org on November 14, 2008

muscle length does not change with age. A secondary tive markers such as [3H]adenosine injected into the
factor could be the decreased tensile stiffness of the muscle, it is difficult to speculate on the mechanisms
in-series tendon in old age (30, 39), which would result leading to this decrease in Lf in aged muscle. However,
in a leftward shift of the length-tension relation (48). it seems plausible that the removal of sarcomeres in
However, it could be argued that this secondary dete- series occurs at the distal and proximal ends of the
riorating effect might be partly cancelled out by the fascicles, through mechanisms similar to those medi-
decrease in the total number of serial sarcomeres, as ating the loss of sarcomeres in series in disuse due to
indicated by the present results, which theoretically immobilization (44).
would shift rightward the length-tension relation of In the elderly, fascicles were found to be not only
the muscle. Other factors accounting for the reduced shorter but also less pennate than in the younger
force-generating potential in old age would be a de- adults. This effect is likely due to the decrease in
crease in single fiber-specific tension (26), an increased contractile tissue packed along the tendon aponeuroses
antagonist muscle coactivation (11, 17, 29), and in and is similar to that observed in disuse atrophy (38).
some cases a reduced muscle activation capacity (4, 12, For both sarcopenia and disuse atrophy, this phenom-
47), not always found (6, 7, 18, 22, 43). enon is probably due to the decrease in fiber size;
Assuming a linear relationship between in-series however, in sarcopenia an additional decrease in ␪
sarcomere number and Lf (14), it follows from previous should be expected owing to the reduction in fiber
reports on human cadaver GM architecture measure- number (27). It seems that both sarcopenia and disuse
ments (16) that the number of sarcomeres in series atrophy involve changes in ␪ that are diametrically
would be ⬃14,540 in the elderly (for a Lf of 4.29 cm) opposite to those found in hypertrophy, which is char-
and ⬃16,200 in the younger adults (for a Lf of 4.78 cm). acterized by an increase in ␪ (21). A decrease in ␪ with
This difference in sarcomere number predicts that, in muscle atrophy was predicted as early as in 1952 by
these elderly individuals, the maximum shortening Benninghoff and Rollhäuser (2) and was thought to
velocity of the GM fascicles should be at least 10% give fibers a slight mechanical advantage due to a more
lower than in the younger adults. Nevertheless, the effective force transmission to the tendon during con-
actual reduction in maximum shortening velocity in traction (10). Given that the resting ␪ is one of the
the elderly is likely to be greater given that 1) the factors determining the ␪ during contraction, quantify-
intrinsic maximum speed of shortening of (the most ing architectural differences between subjects in the
abundant) type I myosin heavy chain isoform is signif- resting state is important to identify the origin of the
icantly lower in old age (15), 2) antagonist muscle respective differences in architectural changes on con-
coactivation is greater in old age (22, 29), and 3) tendon traction.
stiffness decreases in old age (30, 39). Because of the Although in this study a significant correlation was
reduction in PCSA (and thus of maximum isometric found between ACSA and PCSA, the coefficient of de-
force) and in fiber Lf (and thus of maximum shortening termination (R2) was 0.576, indicating that ⬍60% of
velocity), the maximum muscle power is also expected the variance in ACSA is explained by the variance in
to be reduced in the elderly. However, considering that PCSA. This suggests that ACSA and PCSA should not
in elderly subjects PCSA and Lf were, respectively, 85 be used interchangeably, particularly when normaliz-
and 90% of those found in the young adults, the data ing force per CSA for estimating specific force, known
predict a greater reduction in isometric force than in to strictly depend on PCSA.
maximum shortening velocity. As a result, the opti- In conclusion, this study demonstrates that human
mum velocity for peak power generation is also ex- GM architecture is significantly altered by aging. The
J Appl Physiol • VOL 95 • DECEMBER 2003 • www.jap.org
 AGING AND HUMAN MUSCLE ARCHITECTURE 2233

findings suggest that sarcopenia not only involves a 19. Janssen I, Heymsfield SB, Wang ZM, and Ross R. Skeletal
loss of sarcomeres in parallel but also in series. These muscle mass and distribution in 468 men and women aged
18–88 yr. J Appl Physiol 89: 81–88, 2000.
architectural changes are believed to play a significant 20. Jubrias SA, Odderson IR, Esselman PC, and Conley KE.
role in the loss of muscle function in old age because Decline in isokinetic force with age: muscle cross-sectional area
they are likely to affect the length-tension as well as and specific force. Pflügers Arch 434: 246–253, 1997.
the force-velocity and power-velocity relations of this 21. Kawakami Y, Abe T, and Fukunaga T. Muscle-fiber penna-
muscle on which common daily functions such as walk- tion angles are greater in hypertrophied than in normal muscles.
J Appl Physiol 74: 2740–2744, 1993.
ing and stair negotiation depend. 22. Klein CS, Rice CL, and Marsh GD. Normalized force, activa-
tion, and coactivation in the arm muscles of young and old men.
The authors appreciate the collaboration of Dr. Edda Capodaglio
J Appl Physiol 91: 1341–1349, 2001.
in the screening of subjects for physical activity. We are also indebted
23. Klitgaard H, Mantoni M, Schiaffino S, Ausoni S, Gorza L,
to the participants of this study, particularly the senior volunteers,
Laurent-Winter C, Schnohr P, and Saltin B. Function, mor-
for the commitment and time given to this project.
phology and protein expression of ageing skeletal muscle: a
cross-sectional study of elderly men with different training back-
REFERENCES
grounds. Acta Physiol Scand 140: 41–54, 1990.
1. Alexander RM and Vernon A. The dimensions of the knee and 24. Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY, Okada
ankle muscles and the forces they exert. J Mov Stud 1: 115–123, M, and Fukunaga T. Muscle architectural characteristics in
1975. young and elderly men and women. Int J Sports Med 24: 125–
2. Benninghoff A and Rollhäuser H. Zur inneren Mechanik des 130, 2003.
fiederten Muskels. Pflügers Arch 254: 527–548, 1952. 25. Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY, Okada
3. Berthouze SE, Minaire PM, Chatard JC, Boutet C, Castells M, and Fukunaga T. Muscle architectural characteristics in
J, and Lacour JR. A new tool for evaluating energy expendi- women aged 20–79 years. Med Sci Sports Exerc 35: 39–44, 2003.

Downloaded from jap.physiology.org on November 14, 2008

ture: the “QAPSE” development and validation. Med Sci Sports 26. Larsson L, Li X, and Frontera WR. Effects of aging on short-
Exerc 25: 1405–1414, 1993. ening velocity and myosin isoform composition in single human
4. Bilodeau M, Erb MD, Nichols JM, Joiner KL, and Weeks skeletal muscle cells. Am J Physiol Cell Physiol 272: C638–
JB. Fatigue of elbow flexor muscles in younger and older adults. C649, 1997.
Muscle Nerve 24: 98–106, 2001. 27. Lexell J, Taylor CC, and Sjostrom M. What is the cause of the
5. Bonnefoy M, Kostka T, Berthouze SE, and Lacour JR. ageing atrophy? Total number, size and proportion of different
Validation of a physical activity questionnaire in the elderly. Eur fiber types studied in whole vastus lateralis muscle from 15- to
J Appl Physiol 74: 528–533, 1996. 83-year-old men. J Neurol Sci 84: 275–294, 1988.
6. Connelly DM, Rice CL, Roos MR, and Vandervoort AA. 28. Lieber RL and Friden J. Functional and clinical significance
Motor unit firing rates and contractile properties in tibialis of skeletal muscle architecture. Muscle Nerve 23: 1647–1666,
anterior of young and old men. J Appl Physiol 87: 843–852, 1999. 2000.
7. De Serres SJ and Enoka RM. Older adults can maximally 29. Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMil-
activate the biceps brachii muscle by voluntary command. J Appl lan NC, and De Vito G. Contractile muscle volume and agonist-
Physiol 84: 284–291, 1998. antagonist coactivation account for differences in torque be-
8. Friederich JA and Brand RA. Muscle fiber architecture in the tween young and older women. Muscle Nerve 25: 858–863, 2002.
human lower limb. J Biomech 23: 91–95, 1990. 30. Maganaris CN. In vivo tendon mechanical properties in young
9. Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein adults and healthy elderly. Active Life Span Research Sympo-
R, and Roubenoff R. Skeletal muscle fiber quality in older men sium. The Plasticity of the Motor System: Adaptations to In-
and women. Am J Physiol Cell Physiol 279: C611–C618, 2000. creased Use, Disuse and Ageing, Manchester Metropolitan Uni-
10. Gans C and Bock WJ. The functional significance of muscle versity, United Kingdom, 2001, p. 13–14. [online] http://www.
architecture—a theoretical analysis. Ergeb Anat Entwicklungs- mmu.ac.uk/c-a/exspsci/research/invivo.htm.
gesch 38: 115–142, 1965.
31. Maganaris CN, Baltzopoulos V, Ball D, and Sargeant AJ.
11. Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K,
In vivo specific tension of human skeletal muscle. J Appl Physiol
Lassila H, Malkia E, Kraemer WJ, Newton RU, and Alen
90: 865–872, 2001.
M. Changes in agonist-antagonist EMG, muscle CSA, and force
32. Maganaris CN, Baltzopoulos V, and Sargeant AJ. In vivo
during strength training in middle-aged and older people. J Appl
measurements of the triceps surae complex architecture in man:
Physiol 84: 1341–1349, 1998.
implications for muscle function. J Physiol 512: 603–614, 1998.
12. Harridge SD, Kryger A, and Stensgaard A. Knee extensor
strength, activation, and size in very elderly people following 33. Muramatsu T, Muraoka T, Kawakami Y, Shibayama A,
strength training. Muscle Nerve 22: 831–839, 1999. and Fukunaga T. In vivo determination of fascicle curvature in
13. Haxton HA. Absolute muscle force in the ankle flexors of man. contracting human skeletal muscles. J Appl Physiol 92: 129–
J Physiol 103: 267–273, 1944. 134, 2002.
14. Herzog W, Abrahamse SK, and ter Keurs HE. Theoretical 34. Narici MV, Bordini M, and Cerretelli P. Effect of aging on
determination of force-length relations of intact human skeletal human adductor pollicis muscle function. J Appl Physiol 71:
muscles using the cross-bridge model. Pflügers Arch 416: 113– 1277–1281, 1991.
119, 1990. 35. Narici MV, Landoni L, and Minetti AE. Assessment of hu-
15. Höök P, Sriramoju V, and Larsson L. Effects of aging on man knee extensor muscles stress from in vivo physiological
actin sliding speed on myosin from single skeletal muscle cells of cross-sectional area and strength measurements. Eur J Appl
mice, rats, and humans. Am J Physiol Cell Physiol 280: C782– Physiol 65: 438–444, 1992.
C788, 2001. 36. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, and
16. Huijing PA. Architecture of the human gastrocnemius muscle Cerretelli P. In vivo human gastrocnemius architecture with
and some functional consequences. Acta Anat (Basel) 123: 101– changing joint angle at rest and during graded isometric con-
107, 1985. traction. J Physiol 496: 287–297, 1996.
17. Izquierdo M, Ibanez J, Gorostiaga E, Garrues M, Zuniga 37. Narici MV, Susta D, Ciuffreda L, Ferri A, Scaglioni G, and
A, Anton A, Larrion JL, and Hakkinen K. Maximal strength Capodaglio P. Changes in human gastrocnemius muscle archi-
and power characteristics in isometric and dynamic actions of tecture with ageing (Abstract). J Physiol 518P: 87P, 1999.
the upper and lower extremities in middle-aged and older men. 38. Narici MV and Capodaglio P. Changes in muscle size and
Acta Physiol Scand 167: 57–68, 1999. architecture in disuse-atrophy. In: Muscle Atrophy: Disuse and
18. Jakobi JM and Rice CL. Voluntary muscle activation varies Disease, edited by Capodaglio P and Narici MV. Pavia, Italy:
with age and muscle group. J Appl Physiol 93: 457–462, 2002. PI-ME Press, 1998, p. 55–63.

J Appl Physiol • VOL 95 • DECEMBER 2003 • www.jap.org

2234 AGING AND HUMAN MUSCLE ARCHITECTURE

39. Noyes FR and Grood ES. The strength of the anterior cruciate 44. Williams PE and Goldspink G. The effect of immobilization on
ligament in humans and Rhesus monkeys. J Bone Joint Surg Am the longitudinal growth of striated muscle fibres. J Anat 116:
58: 1074–1082, 1976. 45–55, 1973.
40. Phillips SK, Bruce SA, Newton D, and Woledge RC. The 45. Winegard KJ, Hicks AL, Sale DG, and Vandervoort AA. A
weakness of old age is not due to failure of muscle activation. J 12-year follow-up study of ankle muscle function in older adults.
Gerontol 47: M45–M49, 1992. J Gerontol A Biol Sci Med Sci 51: B202–B207, 1996.
41. Reeves ND and Narici MV. Behavior of human muscle fasci- 46. Young A, Stokes M, and Crowe M. Size and strength of the
cles during shortening and lengthening contractions in vivo. quadriceps muscles of old and young women. Eur J Clin Invest
J Appl Physiol 95: 1090–1096, 2003. 14: 282–287, 1984.
42. Roy RR and Edgerton VR. Skeletal muscle architecture and 47. Yue GH, Ranganathan VK, Siemionow V, Liu JZ, and
performance. In: Strength and Power in Sports, edited by Komi Sahgal V. Older adults exhibit a reduced ability to fully activate
PV. Oxford, UK: Blackwell, 1990, p. 249–265. their biceps brachii muscle. J Gerontol A Biol Sci Med Sci 54:
43. Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, M249–M253, 1999.
Capodaglio P, Sartorio A, and Narici MV. Plantar flexor 48. Zajac FE. Muscle and tendon: properties, models, scaling, and
activation capacity and H reflex in older adults: adaptations to application to biomechanics and motor control. Crit Rev Biomed
strength training. J Appl Physiol 92: 2292–2302, 2002. Eng 17: 359–411, 1989.

Downloaded from jap.physiology.org on November 14, 2008

J Appl Physiol • VOL 95 • DECEMBER 2003 • www.jap.org