Effects of age on mechanical properties of dorsiflexor and plantarflexor muscles

Annals of Biomedical Engineering

Volumn 40, Issue 5, 2012, Pages 1088-1101

  Hasson, Christopher J ^a,b   Caldwell, Graham E ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Aging; Gastrocnemius; Hill muscle model; Musculoskeletal modeling; Optimization; Soleus; Subject specific; Tibialis anterior; Triceps surae

Indexed keywords

GASTROCNEMIUS; MUSCLE MODELS; MUSCULOSKELETAL MODELING; SOLEUS; SUBJECT-SPECIFIC; TIBIALIS ANTERIOR; TRICEPS SURAE;

AGING OF MATERIALS; COMPUTER SIMULATION; ELASTICITY; FORECASTING; MAGNETIC RESONANCE; OPTIMIZATION; ULTRASONIC IMAGING;

MUSCLE;

ADULT; AGED; AGING; ARTICLE; BIOLOGICAL MODEL; CLINICAL TRIAL; ECHOGRAPHY; FEMALE; HUMAN; MALE; METHODOLOGY; MUSCLE ISOMETRIC CONTRACTION; MUSCLE STRENGTH; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; RADIOGRAPHY; SKELETAL MUSCLE;

ADULT; AGED; AGING; FEMALE; HUMANS; ISOMETRIC CONTRACTION; MAGNETIC RESONANCE IMAGING; MALE; MODELS, BIOLOGICAL; MUSCLE STRENGTH; MUSCLE, SKELETAL;

EID: 84862012239     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-011-0481-4     Document Type: Article

References (65)

1. Agur, A. M., V. Ng Thow Hing, K. A. Ball, E. Fiume, and N. H. McKee. Documentation and three dimensional modelling of human soleus muscle architecture. Clin. Anat. 16:285-293, 2003. (Pubitemid 36753669)
2. Arnold, E. M., S. R. Ward, R. L. Lieber, and S. L. Delp. A model of the lower limb for analysis of human movement. Ann. Biomed. Eng. 38:269-279, 2010.
3. Bahler, A. S. Series elastic component of mammalian skeletal muscle. Am. J. Physiol. 213:1560-1564, 1967.
4. Bahler, A. S. Modeling of mammalian skeletal muscle. IEEE Trans. Biomed. Eng. 15:249-257, 1968.
5. Baumgartner, R. N., D. L. Waters, D. Gallagher, J. E. Morley, and P. J. Garry. Predictors of skeletal muscle mass in elderly men and women. Mech. Ageing Dev. 107:123-136, 1999. (Pubitemid 29138849)
6. Blanpied, P., and G. L. Smidt. The difference in stiffness of the active plantarflexors between young and elderly human females. J. Gerontol. 48:M58-M63, 1993. (Pubitemid 23084179)
7. Bobbert, M. F., and G. J. van Ingen Schenau. Isokinetic plantar flexion: experimental results and model calculations. J. Biomech. 23:105-119, 1990. (Pubitemid 20104610)
8. Bojsen-Moller, J., P. Hansen, P. Aagaard, U. Svantesson, M. Kjaer, and S. P. Magnusson. Differential displacement of the human soleus and medial gastrocnemius aponeuro- ses during isometric plantar flexor contractions in vivo. J. Appl. Physiol. 97:1908-1914, 2004. (Pubitemid 39426010)
9. Brand, R. A., D. R. Pedersen, and J. A. Friederich. The sensitivity of muscle force predictions to changes in physiologic cross-sectional area. J. Biomech. 19:589-596, 1986.
10. Buchanan, T. S., D. G. Lloyd, K. Manal, and T. F. Besier. Estimation of muscle forces and joint moments using a forward-inverse dynamics model. Med. Sci. Sports Exerc. 37:1911-1916, 2005. (Pubitemid 41691834)
11. Caldwell, G. E., and A. E. Chapman. The general distribution problem: a physiological solution which includes antagonism. Hum. Mov. Sci. 10:355-392, 1991.
12. Chino, K., T. Oda, T. Kurihara, T. Nagayoshi, K. Yoshikawa, H. Kanehisa, T. Fukunaga, S. Fukashiro, and Y. Kawakami. In vivo fascicle behavior of synergistic muscles in concentric and eccentric plantar flexions in humans. J. Electromyogr. Kinesiol. 18:79-88, 2008.
13. Close, R. Dynamic properties of fast and slow skeletal muscles of the rat after nerve cross-union. J. Physiol. 204:331-346, 1969.
14. Close, R. I. Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52:129-197, 1972.
15. Cook, C., and M. McDonagh. Force responses to controlled stretches of electrically stimulated human muscle- tendon complex. Exp. Physiol. 80:477-490, 1995.
16. Delp, S. L., J. P. Loan, M. G. Hoy, F. E. Zajac, E. L. Topp, and J. M. Rosen. An interactive graphicsbased model of the lower extremity to study orthopaedic surgical procedures. IEEE Trans. Biomed. Eng. 37:757-767, 1990. (Pubitemid 20324141)
17. Diffee, G. M., V. J. Caiozzo, R. E. Herrick, and K. M. Baldwin. Contractile and biochemical properties of rat soleus and plantaris after hindlimb suspension. Am. J. Physiol. Cell Physiol. 260:C528-C534, 1991.
18. Edman, K. A., C. Caputo, and F. Lou. Depression of tetanic force induced by loaded shortening of frog muscle fibres. J. Physiol. 466:535-552, 1993. (Pubitemid 23225242)
19. Edman, K. A., G. Elzinga, and M. I. Noble. Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J. Physiol. 281:139-155, 1978. (Pubitemid 9015877)
20. Enoka, R. M. Eccentric contractions require unique activation strategies by the nervous system. J. Appl. Physiol. 81:2339-2346, 1996. (Pubitemid 27043342)
21. Epstein, M., and W. Herzog. Theoretical Models of Skeletal Muscle. New York: Wiley, 1998.
22. Fitz Hugh, R. A model of optimal voluntary muscular control. J. Math. Biol. 4:203-236, 1977. (Pubitemid 8139220)
23. Frontera, W. R., D. Suh, L. S. Krivickas, V. A. Hughes, R. Goldstein, and R. Roubenoff. Skeletal muscle fiber quality in older men and women. Am. J. Physiol. Cell Physiol. 279:C611-C618, 2000.
24. Fukashiro, S., M. Rob, Y. Ichinose, Y. Kawakami, and T. Fukunaga. Ultrasonography gives directly but noninvasively elastic characteristic of human tendon in vivo. Eur. J. Appl. Physiol. Occup. Physiol. 71:555-557, 1995. (Pubitemid 26002271)
25. Fukunaga, T., K. Kubo, Y. Kawakami, S. Fukashiro, H. Kanehisa, and C. N. Maganaris. In vivo behaviour of human muscle tendon during walking. Proc. R. Soc. B 268:229, 2001.
26. Garner, B. A., and M. G. Pandy. Estimation of musculotendon properties in the human upper limb. Ann. Biomed. Eng. 31:207-220, 2003.
27. Gordon, A. M., A. F. Huxley, and F. J. Julian. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184:170-192, 1966.
28. Harman, S. M., E. J. Metter, J. D. Tobin, J. Pearson, and M. R. Blackman. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. J. Clin. Endocrinol. Metab. 86:724-731, 2001. (Pubitemid 32207487)
29. Hasson, C. J., J. A. Kent-Braun, and G. E. Caldwell. Contractile and non-contractile tissue volume and distribution in ankle muscles of young and older adults. J. Biomech. 44:2299-2306, 2011.
30. Hasson, C. J., R. H. Miller, and G. E. Caldwell. Contractile and elastic ankle joint muscular properties in young and older adults. PLoS One 6:e15953, 2011.
31. Henriksson-Larsén, K. B., J. Lexell, and M. Sjöström. Distribution of different fibre types in human skeletal muscles. I. Method for the preparation and analysis of cross-sections of whole tibialis anterior. Histochem. J. 15:167-178, 1983.
32. Hill, A. V. The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. B 126B:136-195, 1938.
33. Hill, A. V. First and Last Experiments in Muscle Mechanics. London: Cambridge Press, 1970.
34. Hof, A. L. Muscle mechanics and neuromuscular control. J. Biomech. 36:1031-1038, 2003. (Pubitemid 36566642)
35. Hoy, M. G., F. E. Zajac, and M. E. Gordon. A musculoskeletal model of the human lower extremity: the effect of muscle, tendon, and moment arm on the moment-angle relationship of musculotendon actuators at the hip, knee, and ankle. J. Biomech. 23:157-169, 1990. (Pubitemid 20104614)
36. Huijing, P. A. Important experimental factors for skeletal muscle modelling: non-linear changes of muscle length force characteristics as a function of degree of activity. Eur. J. Morphol. 34:47-54, 1996. (Pubitemid 26126062)
37. Jakobsson, F., K. Borg, L. Edström, and L. Grimby. Use of motor units in relation to muscle fiber type and size in man. Muscle Nerve 11:1211-1218, 1988. (Pubitemid 19000568)
38. Johnson, M. A., J. Polgar, D. Weightman, and D. Appleton. Data on the distribution of fibre types in thirty-six human muscles: an autopsy study. J. Neurol. Sci. 18:111-129, 1973.
39. Kannus, P., M. Paavola, and L. Józsa. Aging and degeneration of tendons. In: Tendon Injuries: Basic Science and Clinical Medicine, edited by N. Maffulli, P. Renström, and W. B. Leadbetter. London: Springer, 2005, pp. 25-31.
40. Kent-Braun, J. A., and A. V. Ng. Specific strength and voluntary muscle activation in young and elderly women and men. J. Appl. Physiol. 87:22-29, 1999. (Pubitemid 29330660)
41. Klass, M., S. Baudry, and J. Duchateau. Aging does not affect voluntary activation of the ankle dorsiflexors during isometric, concentric, and eccentric contractions. J. Appl. Physiol. 99:31-38, 2005. (Pubitemid 40934460)
42. Lanza, I. R., T. F. Towse, G. E. Caldwell, D. M. Wigmore, and J. A. Kent-Braun. Effects of age on human muscle torque, velocity, and power in two muscle groups. J. Appl. Physiol. 95:2361-2369, 2003. (Pubitemid 37444980)
43. Larsson, L., X. Li, and W. R. Frontera. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am. J. Physiol. 272:C638-C649, 1997.
44. Loram, I. D., C. N. Maganaris, and M. Lakie. Paradoxical muscle movement in human standing. J. Physiol. 556:683-689, 2004. (Pubitemid 38660307)
45. Lundberg, A., O. Svensson, G. Nemeth, and G. Selvik. The axis of rotation of the ankle joint. J. Bone Joint Surg. Br. 71:94-99, 1989. (Pubitemid 19049591)
46. Maganaris, C. N., V. Baltzopoulos, and A. J. Sargeant. In vivo measurements of the triceps surae complex architecture in man: implications for muscle function. J. Physiol. 512(Pt 2):603-614, 1998. (Pubitemid 28486904)
47. Maganaris, C. N., V. Baltzopoulos, and A. J. Sargeant. Changes in the tibialis anterior tendon moment arm from rest to maximum isometric dorsiflexion: in vivo observations in man. Clin. Biomech. 14:661-666, 1999. (Pubitemid 29410483)
48. Morgan, D. New insights into the behavior of muscle during active lengthening. Biophys. J. 57:209-221, 1990. (Pubitemid 20058256)
49. 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. (Pubitemid 37444961)
50. Ochala, J., W. R. Frontera, D. J. Dorer, J. Van Hoecke, and L. S. Krivickas. Single skeletal muscle fiber elastic and contractile characteristics in young and older men. J. Gerontol. A Biol. Sci. Med. Sci. 62:375-381, 2007. (Pubitemid 47065704)
51. Ochala, J., D. Lambertz, M. Pousson, F. Goubel, and J. V. Hoecke. Changes in mechanical properties of human plantar flexor muscles in ageing. Exp. Gerontol. 39:349-358, 2004. (Pubitemid 38264365)
52. Out, L., T. G. Vrijkotte, A. J. van Soest, and M. F. Bobbert. Influence of the parameters of a human triceps surae muscle model on the isometric torque-angle relationship. J. Biomech. Eng. 118:17-25, 1996. (Pubitemid 26087278)
53. Rugg, S. G., R. J. Gregor, B. R. Mandelbaum, and L. Chiu. In vivo moment arm calculations at the ankle using magnetic resonance imaging (MRI). J. Biomech. 23:495-501, 1990. (Pubitemid 20197724)
54. Scovil, C. Y., and J. L. Ronsky. Sensitivity of a Hill-based muscle model to perturbations in model parameters. J. Biomech. 39:2055-2063, 2006. (Pubitemid 44038723)
55. Shao, Q., D. N. Bassett, K. Manal, and T. S. Buchanan. An EMG-driven model to estimate muscle forces and joint moments in stroke patients. Comput. Biol. Med. 39:1083-1088, 2009.
56. Simoneau, E., A. Martin, and J. Van Hoecke. Effects of joint angle and age on ankle dorsi- and plantar-flexor strength. J. Electromyogr. Kinesiol. 17:307-316, 2007. (Pubitemid 46529491)
57. Spoor, C. W., J. L. van Leeuwen, W. J. van der Meulen, and A. Huson. Active force-length relationship of human lower-leg muscles estimated from morphological data: a comparison of geometric muscle models. Eur. J. Morphol. 29:137-160, 1991.
58. Storn, R., and K. Price. Differential evolution-a simple and efficient adaptive scheme for global optimization over continuous spaces. Technical Report TR-95-012, International Computer Science Institute, 1995.
59. Thelen, D. G. Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults. J. Biomech. Eng. 125:70-77, 2003. (Pubitemid 36297228)
60. Toursel, T., L. Stevens, and Y. Mounier. Evolution of contractile and elastic properties of rat soleus muscle fibres under unloading conditions. Exp. Physiol. 84:93-107, 1999. (Pubitemid 29054291)
61. Wickiewicz, T. L., R. R. Roy, P. L. Powell, and V. R. Edgerton. Muscle architecture of the human lower limb. Clin. Orthop. Relat. Res. 179:275-283, 1983. (Pubitemid 13017338)
62. Wilkie, D. R. The relation between force and velocity in human muscle. J. Physiol. 110:249-280, 1950.
63. Winters, J. M. Hill-based muscle models: a systems engineering perspective. In: Multiple Muscle Systems: Biomechanics and Movement Organization, edited by J. M. Winters, and S. L.-Y. Woo. New York: Springer, 1990, pp. 69-93.
64. Woittiez, R. D., P. A. Huijing, and R. H. Rozendal. Influence of muscle architecture on the length-force diagram. A model and its verification. Pflugers Arch. 397:73-74, 1983. (Pubitemid 13110913)
65. Zajac, F. E. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17:359-411, 1989.