J Appl Physiol 95: 22292234, 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
Centre for Biophysical and Clinical Research into Human Movement (CRM), Manchester Metropolitan University, Alsager Campus, Alsager, ST7 2HL, Cheshire, United Kingdom; and 2Centro Studi Attivita ` Motorie, Fondazione Salvatore Maugeri, via Ferrata 8, 2100 Pavia, Italy
Submitted 30 April 2003; accepted in nal form 26 June 2003
1

Narici, M. V., C. N. Maganaris, N. D. Reeves, and P. Capodaglio. Effect of aging on human muscle architecture. J Appl Physiol 95: 22292234, 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 2742 yr) and on 16 older (aged 7081 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, signicantly 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 signicantly affects human skeletal muscle architecture. These structural alterations are expected to have implications for muscle function in old age. skeletal muscle; muscle ber; sarcopenia; muscle strength

AGING IS KNOWN TO BE ASSOCIATED

with a reduction in muscle mass (sarcopenia). Cross-sectional studies suggest that this phenomenon starts toward the end of the fth 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 crosssectional area (CSA) rather than muscle mass (or volume) of essential muscles of locomotion is considered, a 2533% difference in quadriceps CSA is found between young (2029 yr) and elderly (7081 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.

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 ber-specic 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 strength and muscle size of young and elderly individuals 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 bers run at an angle to the axis of traction of the muscle, the ACSA does not represent the cross section perpendicular to all bers in the muscle, i.e., the physiological CSA (PCSA) (28, 35, 42). In fact, the maximum 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, despite the fact that changes in muscle architecture could potentially modify not only the maximum force-generating 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 decrease in muscle mass but also entails changes in muscle architecture. The study also addresses the functional signicance 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 7081 yr (height, 1.72 0.03 m; body mass, 74.5 8.3 kg) and, for comparison, on 14 younger men aged 2742 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-

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

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

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leagues. Exclusion criteria for subject participation in the study included known muscular, neurological, metabolic, and inammatory 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 walking clubs, some to aerobic and exibility classes, some practicing 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 Questionnaire (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 signicant 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 eld 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 morphometric measurements on the same MRI slice) was carried out on the GM muscle. Calculation of muscle ACSA was performed 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 fth 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 coefcient 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 tted 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 tibiotalar 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 realtime ultrasound (HDI-3000, ATL, Bothell). Images were obtained 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 dened 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
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junctions. The center of the probe was aligned to this position. 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 ber fascicles into the deep aponeurosis, and Lf was dened as the length of the fascicular path between the insertions of the fascicle into the superior 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 extrapolating linearly both the fascicular path, visible in the image, and the aponeurosis. The error introduced by this technique depends 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 negligible 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 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, mentioned above. The mean of three consecutive morphometric analyses of each image was used for data analysis. The architectural measurements were performed by an investigator blinded to subject identity. Statistics. Data are presented as means SD. Age-related differences for all measurements were analyzed with the independent-samples Students 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 (Pearsons product-moment correlation) was used to compare the degree of association between variables. The critical level for statistical signicance was set at 5%.
RESULTS

GM muscles 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 tted with a linear function, a significant 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.
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Table 1. Summary of gastrocnemius medialis architectural data in young and elderly individuals
ACSAmax, cm2 Vol, cm3 Lf, cm , PCSA (Vol/Lf), cm2

Elderly Young Difference P values (t-test)

14.0 3.6 17.4 2.8 19.1% 0.005

208.7 48.5 279.3 59.3 25.3% 0.001

4.29 0.67 4.78 0.55 10.2% 0.01

23.6 3.0 27.2 4.3 13.2% 0.01

50.1 12.6 59.1 14.4 15.2% 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 than that of PCSA (Table 1), no signicant difference was found between the ratios of ACSAmax to PCSA of the young (0.30 0.04) and those of the elderly subjects (0.29 0.06, not signicant). When the values of ACSAsmax and PCSAs of the young and elderly subjects were pooled together, a signicant correlation (r 0.759, P 0.01) was found between ACSAmax and PCSA (see Fig. 2).
DISCUSSION

The present study demonstrates for the rst time that human GM muscle architecture is signicantly altered in old age. Because the elderly individuals specically selected for this study were physically active 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 tted with a linear regression function after the values for the young and elderly subjects were pooled together. J Appl Physiol VOL

ing phenomenon. A different approach was, instead, followed by Kubo et al. (24, 25), who recently investigated muscle architecture in sedentary young and elderly men and women not matched for height and physical activity status. Interestingly, after normalization 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 difcult 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 plantarexors 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 inuence of disuse is controlled for by matching individuals for physical activity level, signicant alterations in the architecture of the GM muscle are observed; that is to say, changes in plantarexor 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 different 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 signicantly reduced in the older individuals compared with the younger adults. As a result of the decrease in muscle Vol (25.3%) and in ber 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 ber 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,
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Fig. 2. Typical sonographs of the gastrocnemius medialis muscle of an elderly man (A) and of a young man (B).

determined by MRI, by Lf estimated from the ratio of ber length to muscle length published in the literature, thereby assuming that the ratio of ber 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 deteriorating 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 decrease in single ber-specic 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 measurements (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 significantly 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 ber 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 optimum velocity for peak power generation is also exJ Appl Physiol VOL

pected to be lower in the elderly than in the young adults. At present, without the use of labeling with radioactive markers such as [3H]adenosine injected into the muscle, it is difcult 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 mediating 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 phenomenon is probably due to the decrease in ber size; however, in sarcopenia an additional decrease in should be expected owing to the reduction in ber number (27). It seems that both sarcopenia and disuse atrophy involve changes in that are diametrically opposite to those found in hypertrophy, which is characterized by an increase in (21). A decrease in with muscle atrophy was predicted as early as in 1952 by Benninghoff and Rollha user (2) and was thought to give bers a slight mechanical advantage due to a more effective force transmission to the tendon during contraction (10). Given that the resting is one of the factors determining the during contraction, quantifying architectural differences between subjects in the resting state is important to identify the origin of the respective differences in architectural changes on contraction. Although in this study a signicant correlation was found between ACSA and PCSA, the coefcient of determination (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 normalizing force per CSA for estimating specic force, known to strictly depend on PCSA. In conclusion, this study demonstrates that human GM architecture is signicantly altered by aging. The
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ndings suggest that sarcopenia not only involves a loss of sarcomeres in parallel but also in series. These architectural changes are believed to play a signicant 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 walking 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. REFERENCES 1. Alexander RM and Vernon A. The dimensions of the knee and ankle muscles and the forces they exert. J Mov Stud 1: 115 123, 1975. 2. Benninghoff A and Rollha user H. Zur inneren Mechanik des ederten Muskels. Pu gers Arch 254: 527 548, 1952. 3. Berthouze SE, Minaire PM, Chatard JC, Boutet C, Castells J, and Lacour JR. A new tool for evaluating energy expenditure: the QAPSE development and validation. Med Sci Sports Exerc 25: 1405 1414, 1993. 4. Bilodeau M, Erb MD, Nichols JM, Joiner KL, and Weeks JB. Fatigue of elbow exor muscles in younger and older adults. Muscle Nerve 24: 98 106, 2001. 5. Bonnefoy M, Kostka T, Berthouze SE, and Lacour JR. Validation of a physical activity questionnaire in the elderly. Eur J Appl Physiol 74: 528 533, 1996. 6. Connelly DM, Rice CL, Roos MR, and Vandervoort AA. Motor unit ring rates and contractile properties in tibialis anterior of young and old men. J Appl Physiol 87: 843 852, 1999. 7. 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. 8. Friederich JA and Brand RA. Muscle ber architecture in the human lower limb. J Biomech 23: 91 95, 1990. 9. Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein R, and Roubenoff R. Skeletal muscle ber quality in older men and women. Am J Physiol Cell Physiol 279: C611 C618, 2000. 10. Gans C and Bock WJ. The functional signicance of muscle architecturea theoretical analysis. Ergeb Anat Entwicklungsgesch 38: 115 142, 1965. 11. Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, Kraemer WJ, Newton RU, and Alen M. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 84: 1341 1349, 1998. 12. Harridge SD, Kryger A, and Stensgaard A. Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22: 831 839, 1999. 13. Haxton HA. Absolute muscle force in the ankle exors of man. J Physiol 103: 267 273, 1944. 14. Herzog W, Abrahamse SK, and ter Keurs HE. Theoretical determination of force-length relations of intact human skeletal muscles using the cross-bridge model. Pu gers Arch 416: 113 119, 1990. 15. Ho o k P, Sriramoju V, and Larsson L. Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am J Physiol Cell Physiol 280: C782 C788, 2001. 16. Huijing PA. Architecture of the human gastrocnemius muscle and some functional consequences. Acta Anat (Basel) 123: 101 107, 1985. 17. 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. 18. Jakobi JM and Rice CL. Voluntary muscle activation varies with age and muscle group. J Appl Physiol 93: 457 462, 2002. J Appl Physiol VOL

19. Janssen I, Heymseld SB, Wang ZM, and Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18 88 yr. J Appl Physiol 89: 81 88, 2000. 20. Jubrias SA, Odderson IR, Esselman PC, and Conley KE. Decline in isokinetic force with age: muscle cross-sectional area and specic force. Pu gers Arch 434: 246 253, 1997. 21. Kawakami Y, Abe T, and Fukunaga T. Muscle-ber pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol 74: 2740 2744, 1993. 22. Klein CS, Rice CL, and Marsh GD. Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol 91: 1341 1349, 2001. 23. Klitgaard H, Mantoni M, Schiafno 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. 24. Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY, Okada M, and Fukunaga T. Muscle architectural characteristics in young and elderly men and women. Int J Sports Med 24: 125 130, 2003. 25. Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY, Okada M, and Fukunaga T. Muscle architectural characteristics in women aged 20 79 years. Med Sci Sports Exerc 35: 39 44, 2003. 26. Larsson L, Li X, and Frontera WR. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol Cell Physiol 272: C638 C649, 1997. 27. Lexell J, Taylor CC, and Sjostrom M. What is the cause of the ageing atrophy? Total number, size and proportion of different ber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84: 275 294, 1988. 28. Lieber RL and Friden J. Functional and clinical signicance of skeletal muscle architecture. Muscle Nerve 23: 1647 1666, 2000. 29. Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, and De Vito G. Contractile muscle volume and agonistantagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25: 858 863, 2002. 30. Maganaris CN. In vivo tendon mechanical properties in young adults and healthy elderly. Active Life Span Research Symposium. The Plasticity of the Motor System: Adaptations to Increased Use, Disuse and Ageing, Manchester Metropolitan University, United Kingdom, 2001, p. 13 14. [online] http://www. mmu.ac.uk/c-a/exspsci/research/invivo.htm. 31. Maganaris CN, Baltzopoulos V, Ball D, and Sargeant AJ. In vivo specic tension of human skeletal muscle. J Appl Physiol 90: 865 872, 2001. 32. Maganaris CN, Baltzopoulos V, and Sargeant AJ. In vivo measurements of the triceps surae complex architecture in man: implications for muscle function. J Physiol 512: 603 614, 1998. 33. Muramatsu T, Muraoka T, Kawakami Y, Shibayama A, and Fukunaga T. In vivo determination of fascicle curvature in contracting human skeletal muscles. J Appl Physiol 92: 129 134, 2002. 34. Narici MV, Bordini M, and Cerretelli P. Effect of aging on human adductor pollicis muscle function. J Appl Physiol 71: 1277 1281, 1991. 35. Narici MV, Landoni L, and Minetti AE. Assessment of human knee extensor muscles stress from in vivo physiological cross-sectional area and strength measurements. Eur J Appl Physiol 65: 438 444, 1992. 36. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, and Cerretelli P. In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol 496: 287 297, 1996. 37. Narici MV, Susta D, Ciuffreda L, Ferri A, Scaglioni G, and Capodaglio P. Changes in human gastrocnemius muscle architecture with ageing (Abstract). J Physiol 518P: 87P, 1999. 38. Narici MV and Capodaglio P. Changes in muscle size and architecture in disuse-atrophy. In: Muscle Atrophy: Disuse and Disease, edited by Capodaglio P and Narici MV. Pavia, Italy: PI-ME Press, 1998, p. 55 63. www.jap.org

95 DECEMBER 2003

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AGING AND HUMAN MUSCLE ARCHITECTURE 44. Williams PE and Goldspink G. The effect of immobilization on the longitudinal growth of striated muscle bres. J Anat 116: 45 55, 1973. 45. Winegard KJ, Hicks AL, Sale DG, and Vandervoort AA. A 12-year follow-up study of ankle muscle function in older adults. J Gerontol A Biol Sci Med Sci 51: B202 B207, 1996. 46. Young A, Stokes M, and Crowe M. Size and strength of the quadriceps muscles of old and young women. Eur J Clin Invest 14: 282 287, 1984. 47. 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. 48. Zajac FE. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng 17: 359 411, 1989.

39. Noyes FR and Grood ES. The strength of the anterior cruciate ligament in humans and Rhesus monkeys. J Bone Joint Surg Am 58: 1074 1082, 1976. 40. Phillips SK, Bruce SA, Newton D, and Woledge RC. The weakness of old age is not due to failure of muscle activation. J Gerontol 47: M45 M49, 1992. 41. Reeves ND and Narici MV. Behavior of human muscle fascicles during shortening and lengthening contractions in vivo. J Appl Physiol 95: 1090 1096, 2003. 42. Roy RR and Edgerton VR. Skeletal muscle architecture and performance. In: Strength and Power in Sports, edited by Komi PV. Oxford, UK: Blackwell, 1990, p. 249 265. 43. Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, Capodaglio P, Sartorio A, and Narici MV. Plantar exor activation capacity and H reex in older adults: adaptations to strength training. J Appl Physiol 92: 2292 2302, 2002.

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