Tendon material properties vary and are interdependent among turkey hindlimb muscles

Journal of Experimental Biology

Volumn 215, Issue 20, 2012, Pages 3552-3558

  Matson, Andrew ^a   Konow, Nicolai ^a   Miller, Samuel ^a   Konow, Pernille P ^a   Roberts, Thomas J ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Elasticity; Tendon; Tensile strength; Tissue material properties

Indexed keywords

ANIMAL; ARTICLE; ELASTICITY; HINDLIMB; MECHANICAL STRESS; MUSCLE CONTRACTION; MUSCLE STRENGTH; PHYSIOLOGY; SKELETAL MUSCLE; TENDON; TENSILE STRENGTH; TURKEY (BIRD); YOUNG MODULUS;

ANIMALS; ELASTIC MODULUS; ELASTICITY; HINDLIMB; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SKELETAL; STRESS, MECHANICAL; TENDONS; TENSILE STRENGTH; TURKEYS;

MELEAGRIS GALLOPAVO;

EID: 84866850746     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.072728     Document Type: Article

References (56)

1. Alexander, R. M. (1991). Energy-saving mechanisms in walking and running. J. Exp. Biol. 160, 55-69.
2. Alexander, R. M. (2003). Principles of Animal Locomotion. Princeton, NJ: Princeton University Press.
3. Arruda, E. M., Calve, S., Dennis, R. G., Mundy, K. and Baar, K. (2006). Regional variation of tibialis anterior tendon mechanics is lost following denervation. J. Appl. Physiol. 101, 1113-1117.
4. Azizi, E., Halenda, G. M. and Roberts, T. J. (2009). Mechanical properties of the gastrocnemius aponeurosis in wild turkeys. Integr. Comp. Biol. 49, 51-58.
5. Benjamin, M. and Ralphs, J. R. (1998). Fibrocartilage in tendons and ligaments -an adaptation to compressive load. J. Anat. 193, 481-94.
6. Bennett, M. B. (1985). Interrelationships of crural muscles and tendons in a range of birds. J. Zool. 235, 33-42.
7. Bennett, M. B. and Stafford, J. A. (1988). Tensile properties of calcified and uncalcified avian tendons. J. Zool. 214, 343-351.
8. Bennett, M. B., Ker, R. F., Dimery, N. J. and Alexander, R. M. (1986). Mechanical-properties of various mammalian tendons. J. Zool. 209, 537-548.
9. Bojsen-Moller, J., Kalliokoski, K., Seppanen, M., Kjaer, M. and Magnusson, S. P. (2006). Low-intensity tensile loading increases intratendinous glucose uptake in the Achilles tendon. J. Appl. Phys. 101, 196-201.
10. Buchanan, C. I. and Marsh, R. L. (2001). Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. J. Appl. Physiol. 90, 164-171.
11. Cavagna, G. A., Heglund, N. C. and Taylor, C. R. (1977). Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. Am. J. Physiol. 233, R243-R261.
12. Chen, L. X., Wu, Y. P., Yu, J. K., Jiao, Z. D., Ao, Y. F., Yu, C. L., Wang, J. Q. and Cui, G. Q. (2011). Effect of repeated freezing-thawing on the Achilles tendon of rabbits. Knee Surg. Sports Traum. Arthr. 19, 1028-1034.
13. Cui, L., Maas, H., Perreault, E. J. and Sandercock, T. G. (2009). In situ estimation of tendon material properties: Differences between muscles of the feline hindlimb. J. Biomech. 42, 679-685.
14. Grant, C. A., Brockwell, D. J., Radford, S. E. and Thomson, N. H. (2009). Tuning the elastic modulus of hydrated collagen fibrils. Biophys. J. 97, 2985-2992.
15. Harvey, E. B., Kaiser, H. E. and Rosenberg, L. E. (1968). An atlas of the domestic turkey (Meleagris gallopavo); myology and osteology. Washington, DC: US Atomic Energy Commission.
16. Hedrick, T. L. (2008). Software techniques for two-and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir. Biomim. 3, 034001.
17. Heglund, N. C., Fedak, M. A., Taylor, C. R. and Cavagna, G. A. (1982). Energetics and mechanics of terrestrial locomotion. IV. Total mechanical energy changes as a function of speed and body size in birds and mammals. J. Exp. Biol. 97, 57-66.
18. Kalliokoski, K. K., Langberg, H., Ryberg, A. K., Scheede-Bergdahl, C., Doessing, S., Kjaer, A., Boushel, R. and Kjaer, M. (2005). The effect of dynamic knee-extension exercise on patellar tendon and quadriceps femoris muscle glucose uptake in humans studied by positron emission tomography. J. Phys. 99, 1189-1192.
19. Ker, R. F. (1981). Dynamic tensile properties of the plantaris tendon of sheep (Ovis aris). J. Exp. Biol. 93, 283-302.
20. Ker, R. F. (2007). Mechanics of tendon, from an engineering perspective. Int. J. Fatigue 29, 1001-1009.
21. Ker, R. F., Alexander, R. M. and Bennett, M. B. (1988). Why are mammalian tendons so thick? J. Zool. 216, 309-324.
22. Kjaer, M. (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Phys. Rev. 84, 649-698.
23. Konow, N., Azizi, E. and Roberts, T. J. (2011). Muscle power attenuation by tendon during energy dissipation. Proc. Biol. Sci. 279, 1108-1113.
24. Kubo, K., Kawakami, Y., Kanehisa, H. and Fukunaga, T. (2002). Measurement of viscoelastic properties of tendon structures in vivo. Scand. J. Med. Sci. Sports 12, 3-8.
25. Langberg, H., Skovgaard, D., Petersen, L. J., Bulow, J. and Kjaer, M. (1999). Type I collagen synthesis and degradation in peritendinous tissue after exercise determined by microdialysis in humans. J. Phys. 521, 299-306.
26. Langberg, H., Rosendal, L. and Kjaer, M. (2001). Training-induced changes in peritendinous type I collagen turnover determined by microdialysis in humans. J. Phys. 534, 297-302.
27. Legerlotz, K., Riley, G. P. and Screen, H. R. C. (2010). Specimen dimensions influence the measurement of material properties in tendon fascicles. J. Biomech. 43, 2274-2280.
28. Lichtwark, G. A. and Wilson, A. M. (2006). Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion. J. Exp. Biol. 209, 4379-4388.
29. Lieber, R. L., Leonard, M. E., Brown, C. G. and Trestik, C. L. (1991). Frog semitendinosis tendon load-strain and stress-strain properties during passive loading. Am. J. Phys. 261, C86-C92.
30. Maganaris, C. N. (2002). Tensile properties of in vivo human tendinous tissue. J. Biomech. 35, 1019-1027.
31. Maganaris, C. N. and Paul, J. P. (2000). Hysteresis measurements in intact human tendon. J. Biomech. 33, 1723-1727.
32. Maganaris, C. N. and Paul, J. P. (2002). Tensile properties of the in vivo human gastrocnemius tendon. J. Biomech. 35, 1639-1646.
33. Maganaris, C. N., Narici, M. V. and Reeves, N. D. (2004). In vivo human tendon mechanical properties: effect of resistance training in old age. J. Musculoskelet. Neuronal Interact. 4, 204-208.
34. Magnusson, S. P., Narici, M. V., Maganaris, C. N. and Kjaer, M. (2008). Human tendon behaviour and adaptation, in vivo. J. Phys. 586, 71-81.
35. Matsumoto, F., Trudel, G., Uhthoff, H. K. and Backman, D. S. (2003). Mechanical effects of immobilization on the Achilles tendon. Arch. Phys. Med. Rehabil. 84, 662-667.
36. Mendez, J. and Keys, A. (1960). Density and composition of mammalian muscle. Metabolism 9, 184-188.
37. Miller, B. F., Olesen, J. L., Hansen, M., Døssing, S., Crameri, R. M., Welling, R. J., Langberg, H., Flyvbjerg, A., Kjaer, M., Babraj, J. A. et al. (2005). Co-ordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J. Phys. 567, 1021-1033.
38. Nakagawa, Y., Hayashi, K., Yamamoto, N. and Nagashima, K. (1996). Age-related changes in biomechanical properties of the Achilles tendon in rabbits. Eur. J. Appl. Physiol. Occup. Physiol. 73, 7-10.
39. Narici, M. V., Maffulli, N. and Maganaris, C. N. (2008). Ageing of human muscles and tendons. Disabil. Rehabil. 30, 1548-1554.
40. Pollock, C. M. and Shadwick, R. E. (1994). Relationship between body mass and biomechanical properties of limb tendons in adult mammals. Am. J. Physiol. 266, R1016-R1021.
41. Reeves, N. D., Maganaris, C. N. and Narici, M. V. (2003). Effect of strength training on human patella tendon mechanical properties of older individuals. J. Physiol. 548, 971-981.
42. Roberts, T. J. (2002). The integrated function of muscles and tendons during locomotion. Comp. Biochem. Physiol. 133A, 1087-1099.
43. Roberts, T. J. and Azizi, E. (2011). Flexible mechanisms: the diverse roles of biological springs in vertebrate movement. J. Exp. Biol. 214, 353-361.
44. Roberts, T. J., Marsh, R. L., Weyand, P. G. and Taylor, C. R. (1997). Muscular force in running turkeys: the economy of minimizing work. Science 275, 1113-1115.
45. Roberts, T. J., Chen, M. and Taylor, C. (1998). Energetics of bipedal running. II. Limb design and running mechanics. J. Exp. Biol. 201, 2753-2762.
46. Robinson, P. S., Huang, T.-F., Kazam, E., Iozzo, R. V., Birk, D. E. and Soslowsky, L. J. (2005). Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. J. Biomech. Eng. 127, 181-185.
47. Sawicki, G. S., Lewis, C. L. and Ferris, D. P. (2009). It pays to have a spring in your step. Exerc. Sport. Sci. Rev. 37, 130-138.
48. Schatzmann, L., Brunner, P. and Stäubli, H. U. (1998). Effect of cyclic preconditioning on the tensile properties of human quadriceps tendons and patellar ligaments. Knee Surg. Sports Traum. Arthr. 6, S56-S61.
49. Shadwick, R. E. (1990). Elastic energy storage in tendons: mechanical differences related to function and age. J. Appl. Physiol. 68, 1033-1040.
50. Svendsen, K. H. and Thomson, G. (1984). A new clamping and stretching procedure for determination of collagen fiber stiffness and strength relations upon maturation. J. Biomech. 17, 225-229.
51. Vanden Bergen, J. S. and Zweers, G. A. (1993). Myologia. In Handbook of Avian Anatomy (ed. J. J. Baumel), pp. 189-251. Cambridge, MA: Nuttall Ornithological Club.
52. Woo, S. L. (1982). Mechanical properties of tendons and ligaments. I. Quasi-static and non-linear viscoelastic properties. Biorheology 19, 385-396.
53. Woo, S. L., Ritter, M. A., Amiel, D., Sanders, T. M., Gomez, M. A., Kuei, S. C., Garfin, S. R. and Akeson, W. H. (1980). The biomechanical and biochemical properties of swine tendons-long term effects of exercise on the digital extensors. Connect Tissue Res. 7, 177-183.
54. Wood, L. K., Arruda, E. M. and Brooks, S. V. (2011). Regional stiffening with aging in tibialis anterior tendons of mice occurs independent of changes in collagen fibril morphology. J. Appl. Phys. 111, 999-1006.
55. Wood, T. O., Cooke, P. H. and Goodship, A. E. (1988). The effect of exercise and anabolic steroids on the mechanical properties and crimp morphology of the rat tendon. Am. J. Sports Med. 16, 153-158.
56. Zajac, F. E. (1989). Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17, 359-411.