Changes of calf muscle-tendon biomechanical properties induced by passive-stretching and active-movement training in children with cerebral palsy

Journal of Applied Physiology

Volumn 111, Issue 2, 2011, Pages 435-442

  Zhao, Heng ^a,b   Wu, Yi Ning ^a,b   Hwang, Miriam ^a,c   Ren, Yupeng ^a,b   Gao, Fan ^d   Gaebler Spira, Deborah ^a,b   Zhang, Li Qun ^a,b  

^a REHABILITATION INSTITUTE OF CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c Korea University College of Medicine   (South Korea)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Achilles tendon; Muscle fascicles; Pennation; Stiffness; Ultrasonography

Indexed keywords

ACHILLES TENDON; ADOLESCENT; ANKLE; ARTICLE; BIOMECHANICS; CEREBRAL PALSY; CHILD; COMPARATIVE STUDY; ECHOGRAPHY; FEMALE; HUMAN; KINESIOTHERAPY; LEG; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; SKELETAL MUSCLE; STRETCHING EXERCISE; YOUNG MODULUS;

ACHILLES TENDON; ADOLESCENT; ANKLE; BIOMECHANICS; CEREBRAL PALSY; CHILD; CHILD, PRESCHOOL; ELASTIC MODULUS; EXERCISE MOVEMENT TECHNIQUES; FEMALE; HUMANS; LEG; MALE; MUSCLE STRETCHING EXERCISES; MUSCLE, SKELETAL;

EID: 80051767590     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01361.2010     Document Type: Article

References (47)

1. Barrett RS, Lichtwark GA. Gross muscle morphology and structure in spastic cerebral palsy: a systematic review. Dev Med Child Neurol 52: 794-804, 2010.
2. Benard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT. Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve 39: 652-665, 2009.
3. Buschbacher RM, Porter CD. Deconditioning, conditioning, and the benefits of exercise. In: Physical Medicine and Rehabilitation (2nd ed.), edited by Braddom RL. Philadelphia, PA: W. B. Sauders, 2000, p. 702-726.
4. de Almeida F, Tomiosso T, Nakagaki W, Gomes L, Matiello-Rosa S, Pimentel E. Effects of passive stretching on the biochemical and biomechanical properties of calcaneal tendon of rats. Connect Tissue Res 50: 279-284, 2009.
5. Engsberg JR, Ross SA, Olree KS, Park TS. Ankle spasticity and strength in children with spastic diplegic cerebral palsy. Dev Med Child Neurol 42: 42-47, 2000. (Pubitemid 30009140)
6. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Day MK, Lee PL, Wong-Fu H, Edgerton VR. Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. J Orthop Res 10: 926-934, 1992.
7. Gajdosik CG, Cicirello N. Secondary conditions of the musculoskeletal system in adolescents and adults with cerebral palsy. Phys Occup Ther Pediatr 21: 49-68, 2001. (Pubitemid 34522345)
8. Gao F, Zhao H, Gaebler-Spira D, Zhang L-Q. In vivo evaluations of morphological changes of gastrocnemius muscle fascicles and Achilles tendon in children with cerebral palsy. Am J Phys Med Rehab 90: 364-371, 2011.
9. Gao F, Grant TH, Roth EJ, Zhang LQ. Changes in passive mechanical properties of the gastrocnemius muscle at the muscle fascicle and joint levels in stroke survivors. Arch Phys Med Rehabil 90: 819-826, 2009.
10. Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral palsy in Sweden. IV. Epidemiological trends 1959-78. Acta Paediatr Scand 73: 433-440, 1984. (Pubitemid 14084684)
11. Hanna SE, Rosenbaum PL, Bartlett DJ, Palisano RJ, Walter SD, Avery L, Russell DJ. Stability and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21 years. Dev Med Child Neurol 51: 295-302, 2009.
12. Kawakami Y, Ichinose Y, Fukunaga T. Architectural and functional features of human triceps surae muscles during contraction. J Appl Physiol 85: 398-404, 1998. (Pubitemid 28365802)
13. Kemp TJ, Sadusky TJ, Saltisi F, Carey N, Moss J, Yang SY, Sassoon DA, Goldspink G, Coulton GR. Identification of Ankrd2, a novel skeletal muscle gene coding for a stretch-responsive ankyrin-repeat protein. Genomics 66: 229-241, 2000. (Pubitemid 30481769)
14. Kemp TJ, Sadusky TJ, Simon M, Brown R, Eastwood M, Sassoon DA, Coulton GR. Identification of a novel stretch-responsive skeletal muscle gene (Smpx). Genomics 72: 260-271, 2001. (Pubitemid 32281527)
15. Kjaer M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm L, Doessing S, Kongsgaard M, Krogsgaard MR, Magnusson SP. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports 19: 500-510, 2009.
16. Kubo K, Kanehisa H, Fukunaga T. Effect of stretching training on the viscoelastic properties of human tendon structures in vivo. J Appl Physiol 92: 595-601, 2002. (Pubitemid 34671025)
17. Kubo K, Kanehisa H, Fukunaga T. Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo. J Physiol 538: 219-226, 2002. (Pubitemid 35190051)
18. Lichtwark GA, Wilson AM. In vivo mechanical properties of the human Achilles tendon during one-legged hopping. J Exp Biol 208: 4715-4725, 2005. (Pubitemid 43120017)
19. Maganaris CN. Tensile properties of in vivo human tendinous tissue. J Biomech 35: 1019-1027, 2002. (Pubitemid 34765671)
20. Maganaris CN, Paul JP. In vivo human tendon mechanical properties. J Physiol 521: 307-313, 1999.
21. Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M. Load-displacement properties of the human triceps surae aponeurosis in vivo. J Physiol 531: 277-288, 2001. (Pubitemid 32178044)
22. Magnusson SP, Hansen P, Aagaard P, Brond J, Dyhre-Poulsen P, Bojsen-Moller J, Kjaer M. Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. Acta Physiol Scand 177: 185-195, 2003. (Pubitemid 36197509)
23. Malaiya R, McNee AE, Fry NR, Eve LC, Gough M, Shortland AP. The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. J Electromyogr Kinesiol 17: 657-663, 2007. (Pubitemid 47615465)
24. McNair PJ, Dombroski EW, Hewson DJ, Stanley SN. Stretching at the ankle joint: viscoelastic responses to holds and continuous passive motion. Med Sci Sports Exerc 33: 354-358, 2001. (Pubitemid 32215280)
25. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzopoulos V, Maganaris CN. Differences in gastrocnemius muscle architecture between the paretic and non-paretic legs in children with hemiplegic cerebral palsy. Clin Biomech (Bristol, Avon) 22: 718-724, 2007. (Pubitemid 46818630)
26. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzopoulos V, Maganaris CN. In vivo gastrocnemius muscle fascicle length in children with and without diplegic cerebral palsy. Dev Med Child Neurol 50: 44-50, 2008.
27. Morse CI, Degens H, Seynnes OR, Maganaris CN, Jones DA. The acute effect of stretching on the passive stiffness of the human gastrocnemius muscle tendon unit. J Physiol 586: 97-106, 2008.
28. Muraoka T, Chino K, Muramatsu T, Fukunaga T, Kanehisa H. In vivo passive mechanical properties of the human gastrocnemius muscle belly. J Biomech 38: 1213-1219, 2005. (Pubitemid 40603596)
29. Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H. Geometric and elastic properties of in vivo human Achilles tendon in young adults. Cells Tissues Organs 178: 197-203, 2004. (Pubitemid 41201464)
30. Nakagawa Y, Hayashi K, Yamamoto N, Nagashima K. Age-related changes in biomechanical properties of the Achilles tendon in rabbits. Eur J Appl Physiol Occup Physiol 73: 7-10, 1996. (Pubitemid 26113705)
31. Pin T, Dyke P, Chan M. The effectiveness of passive stretching in children with cerebral palsy. Dev Med Child Neurol 48: 855-862, 2006. (Pubitemid 44425695)
32. Reeves ND. Adaptation of the tendon to mechanical usage. J Musculoskelet Neuronal Interact 6: 174-180, 2006. (Pubitemid 44193218)
33. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, Dan B, Jacobsson B. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol 109: 8-14, 2007.
34. Sanger TD, Delgado MR, Gaebler-Spira D, Hallett M, Mink JW. Classification and definition of disorders causing hypertonia in childhood. Pediatrics 111: e89-e97, 2003.
35. Selles RW, Li X, Lin F, Chung SG, Roth EJ, Zhang LQ. Feedback-controlled and programmed stretching of the ankle plantarflexors and dorsiflexors in stroke: effects of a 4-week intervention program. Arch Phys Med Rehabil 86: 2330-2336, 2005. (Pubitemid 41774609)
36. Shadwick RE. Elastic energy storage in tendons: mechanical differences related to function and age. J Appl Physiol 68: 1033-1040, 1990. (Pubitemid 20136429)
37. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Dev Med Child Neurol 43: 796-801, 2001. (Pubitemid 33138223)
38. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Dev Med Child Neurol 44: 158-163, 2002. (Pubitemid 34232372)
39. Smith C, Young I, Kearney J. Mechanical properties of tendons: changes with sterilization and preservation. J Biomech Eng 118: 56-61, 1996. (Pubitemid 26087283)
40. Staron RS, Kraemer WJ, Hikida RS, Fry AC, Murray JD, Campos GER. Fiber type composition of four hindlimb muscles of adult Fisher 344 rats. Histochem Cell Biol 111: 117-123, 1999. (Pubitemid 29148251)
41. Weng L, Tirumalai AP, Lowery CM, Nock LF, Gustafson DE, Von Behren PL, Kim JH. US extended-field-of-view imaging technology. Radiology 203: 877-880, 1997. (Pubitemid 27227446)
42. Wren TA, Beaupre GS, Carter DR. Tendon and ligament adaptation to exercise, immobilization, and remobilization. J Rehabil Res Dev 37: 217-224, 2000. (Pubitemid 30641250)
43. Wren TA, Cheatwood AP, Rethlefsen SA, Hara R, Perez FJ, Kay RM. Achilles tendon length and medial gastrocnemius architecture in children with cerebral palsy and equinus gait. J Pediatr Orthop 30: 479-484, 2010.
44. Wren TA, Yerby SA, Beaupre GS, Carter DR. Mechanical properties of the human Achilles tendon. Clin Biomech (Bristol, Avon) 16: 245-251, 2001. (Pubitemid 32178312)
45. Wu YN, Hwang M, Ren Y, Gaebler-Spira DJ, Zhang LQ. Combined passive stretching and active movement rehabilitation of lower-limb impairments in children with cerebral palsy using a portable robot. Neurorehabil Neural Repair 25: 378-385, 2011.
46. Zhang LQ, Chung SG, Bai Z, Xu D, van Rey EM, Rogers MW, Johnson ME, Roth EJ. Intelligent stretching of ankle joints with contracture/ spasticity. IEEE Trans Neural Syst Rehabil Eng 10: 149-157, 2002. (Pubitemid 35462927)
47. Zhao H, Ren Y, Wu YN, Liu SQ, Zhang LQ. Ultrasonic evaluations of Achilles tendon mechanical properties post stroke. J Appl Physiol 106: 843-849, 2009.