Skip to main content
Top
Published in: Clinical Orthopaedics and Related Research® 11/2013

01-11-2013 | Basic Research

Amount of Torque and Duration of Stretching Affects Correction of Knee Contracture in a Rat Model of Spinal Cord Injury

Authors: Hideki Moriyama, PhD, Yoshiko Tobimatsu, PhD, Junya Ozawa, PhD, Nobuhiro Kito, PhD, Ryo Tanaka, PhD

Published in: Clinical Orthopaedics and Related Research® | Issue 11/2013

Login to get access

Abstract

Background

Joint contractures are a common complication of many neurologic conditions, and stretching often is advocated to prevent and treat these contractures. However, the magnitude and duration of the stretching done in practice usually are guided by subjective clinical impressions.

Questions/purposes

Using an established T8 spinal cord injury rat model of knee contracture, we sought to determine what combination of static or intermittent stretching, varied by magnitude (high or low) and duration (long or short), leads to the best (1) improvement in the limitation in ROM; (2) restoration of the muscular and articular factors leading to contractures; and (3) prevention and treatment of contracture-associated histologic alterations of joint capsule and articular cartilage.

Methods

Using a rat animal model, the spinal cord was transected completely at the level of T8. The rats were randomly assigned to seven treatment groups (n = 4 per group), which were composed of static or intermittent stretching in combination with different amounts of applied torque magnitude and duration. We assessed the effect of stretching by measuring the ROM and evaluating the histologic alteration of the capsule and cartilage.

Results

Contractures improved in all treated groups except for the low-torque and short-duration static stretching conditions. High-torque stretching was effective against shortening of the synovial membrane and adhesions in the posterosuperior regions. Collagen Type II and VEGF in the cartilage were increased by stretching.

Conclusions

High-torque and long-duration static stretching led to greater restoration of ROM than the other torque and duration treatment groups. Stretching was more effective in improving articular components of contractures compared with the muscular components. Stretching in this rat model prevented shortening and adhesion of the joint capsule, and affected biochemical composition, but did not change morphologic features of the cartilage.

Clinical Relevance

This animal study tends to support the ideas that static stretching can influence joint ROM and histologic qualities of joint tissues, and that the way stretching is performed influences its efficacy. However, further studies are warranted to determine if our findings are clinically applicable.
Literature
1.
go back to reference Ben M, Harvey L, Denis S, Glinsky J, Goehl G, Chee S, Herbert RD. Does 12 weeks of regular standing prevent loss of ankle mobility and bone mineral density in people with recent spinal cord injuries? Aust J Physiother. 2005;51:251–256.PubMedCrossRef Ben M, Harvey L, Denis S, Glinsky J, Goehl G, Chee S, Herbert RD. Does 12 weeks of regular standing prevent loss of ankle mobility and bone mineral density in people with recent spinal cord injuries? Aust J Physiother. 2005;51:251–256.PubMedCrossRef
2.
go back to reference Bramono DS, Richmond JC, Weitzel PP, Kaplan DL, Altman GH. Matrix metalloproteinases and their clinical applications in orthopaedics. Clin Orthop Relat Res. 2004;428:272–285.PubMedCrossRef Bramono DS, Richmond JC, Weitzel PP, Kaplan DL, Altman GH. Matrix metalloproteinases and their clinical applications in orthopaedics. Clin Orthop Relat Res. 2004;428:272–285.PubMedCrossRef
3.
go back to reference Coutinho EL, DeLuca C, Salvini TF, Vidal BC. Bouts of passive stretching after immobilization of the rat soleus muscle increase collagen macromolecular organization and muscle fiber area. Connect Tissue Res. 2006;47:278–286.PubMedCrossRef Coutinho EL, DeLuca C, Salvini TF, Vidal BC. Bouts of passive stretching after immobilization of the rat soleus muscle increase collagen macromolecular organization and muscle fiber area. Connect Tissue Res. 2006;47:278–286.PubMedCrossRef
4.
go back to reference Dalyan M, Sherman A, Cardenas DD. Factors associated with contractures in acute spinal cord injury. Spinal Cord. 1998;36:405–408.PubMedCrossRef Dalyan M, Sherman A, Cardenas DD. Factors associated with contractures in acute spinal cord injury. Spinal Cord. 1998;36:405–408.PubMedCrossRef
5.
go back to reference Enneking WF, Horowitz M. The intra-articular effects of immobilization on the human knee. J Bone Joint Surg Am. 1972;54:973–985.PubMed Enneking WF, Horowitz M. The intra-articular effects of immobilization on the human knee. J Bone Joint Surg Am. 1972;54:973–985.PubMed
6.
go back to reference Farmer SE, James M. Contractures in orthopaedic and neurological conditions: a review of causes and treatment. Disabil Rehabil. 2001;23:549–558.PubMedCrossRef Farmer SE, James M. Contractures in orthopaedic and neurological conditions: a review of causes and treatment. Disabil Rehabil. 2001;23:549–558.PubMedCrossRef
7.
go back to reference Fergusson D, Hutton B, Drodge A. The epidemiology of major joint contractures: a systematic review of the literature. Clin Orthop Relat Res. 2007;456:22–29.PubMedCrossRef Fergusson D, Hutton B, Drodge A. The epidemiology of major joint contractures: a systematic review of the literature. Clin Orthop Relat Res. 2007;456:22–29.PubMedCrossRef
8.
go back to reference Gomes AR, Cornachione A, Salvini TF, Mattiello-Sverzut AC. Morphological effects of two protocols of passive stretch over the immobilized rat soleus muscle. J Anat. 2007;210:328–335.PubMedCrossRef Gomes AR, Cornachione A, Salvini TF, Mattiello-Sverzut AC. Morphological effects of two protocols of passive stretch over the immobilized rat soleus muscle. J Anat. 2007;210:328–335.PubMedCrossRef
9.
go back to reference Harvey L, Herbert R, Crosbie J. Does stretching induce lasting increases in joint ROM? A systematic review. Physiother Res Int. 2002;7:1–13.PubMedCrossRef Harvey L, Herbert R, Crosbie J. Does stretching induce lasting increases in joint ROM? A systematic review. Physiother Res Int. 2002;7:1–13.PubMedCrossRef
10.
go back to reference Harvey LA, Batty J, Crosbie J, Poulter S, Herbert RD. A randomized trial assessing the effects of 4 weeks of daily stretching on ankle mobility in patients with spinal cord injuries. Arch Phys Med Rehabil. 2000;81:1340–1347.PubMedCrossRef Harvey LA, Batty J, Crosbie J, Poulter S, Herbert RD. A randomized trial assessing the effects of 4 weeks of daily stretching on ankle mobility in patients with spinal cord injuries. Arch Phys Med Rehabil. 2000;81:1340–1347.PubMedCrossRef
11.
go back to reference Harvey LA, Byak AJ, Ostrovskaya M, Glinsky J, Katte L, Herbert RD. Randomised trial of the effects of four weeks of daily stretch on extensibility of hamstring muscles in people with spinal cord injuries. Aust J Physiother. 2003;49:176–181.PubMed Harvey LA, Byak AJ, Ostrovskaya M, Glinsky J, Katte L, Herbert RD. Randomised trial of the effects of four weeks of daily stretch on extensibility of hamstring muscles in people with spinal cord injuries. Aust J Physiother. 2003;49:176–181.PubMed
12.
go back to reference Harvey LA, Herbert RD. Muscle stretching for treatment and prevention of contracture in people with spinal cord injury. Spinal Cord. 2002;40:1–9.PubMedCrossRef Harvey LA, Herbert RD. Muscle stretching for treatment and prevention of contracture in people with spinal cord injury. Spinal Cord. 2002;40:1–9.PubMedCrossRef
13.
go back to reference Harvey LA, Herbert RD, Glinsky J, Moseley AM, Bowden J. Effects of 6 months of regular passive movements on ankle joint mobility in people with spinal cord injury: a randomized controlled trial. Spinal Cord. 2009;47:62–66.PubMedCrossRef Harvey LA, Herbert RD, Glinsky J, Moseley AM, Bowden J. Effects of 6 months of regular passive movements on ankle joint mobility in people with spinal cord injury: a randomized controlled trial. Spinal Cord. 2009;47:62–66.PubMedCrossRef
14.
go back to reference Haywood L, McWilliams DF, Pearson CI, Gill SE, Ganesan A, Wilson D, Walsh DA. Inflammation and angiogenesis in osteoarthritis. Arthritis Rheum. 2003;48:2173–2177.PubMedCrossRef Haywood L, McWilliams DF, Pearson CI, Gill SE, Ganesan A, Wilson D, Walsh DA. Inflammation and angiogenesis in osteoarthritis. Arthritis Rheum. 2003;48:2173–2177.PubMedCrossRef
15.
go back to reference Katalinic OM, Harvey LA, Herbert RD. Effectiveness of stretch for the treatment and prevention of contractures in people with neurological conditions: a systematic review. Phys Ther. 2011;91:11–24.PubMedCrossRef Katalinic OM, Harvey LA, Herbert RD. Effectiveness of stretch for the treatment and prevention of contractures in people with neurological conditions: a systematic review. Phys Ther. 2011;91:11–24.PubMedCrossRef
16.
go back to reference Katalinic OM, Harvey LA, Herbert RD, Moseley AM, Lannin NA, Schurr K. Stretch for the treatment and prevention of contractures. Cochrane Database Syst Rev. 2010;9:CD007455. Katalinic OM, Harvey LA, Herbert RD, Moseley AM, Lannin NA, Schurr K. Stretch for the treatment and prevention of contractures. Cochrane Database Syst Rev. 2010;9:CD007455.
17.
go back to reference Kawamoto T. Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch Histol Cytol. 2003;66:123–143.PubMedCrossRef Kawamoto T. Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch Histol Cytol. 2003;66:123–143.PubMedCrossRef
18.
go back to reference Lee S, Sakurai T, Ohsako M, Saura R, Hatta H, Atomi Y. Tissue stiffness induced by prolonged immobilization of the rat knee joint and relevance of AGEs (pentosidine). Connect Tissue Res. 2010;51:467–477.PubMedCrossRef Lee S, Sakurai T, Ohsako M, Saura R, Hatta H, Atomi Y. Tissue stiffness induced by prolonged immobilization of the rat knee joint and relevance of AGEs (pentosidine). Connect Tissue Res. 2010;51:467–477.PubMedCrossRef
19.
go back to reference Lieber RL, Steinman S, Barash IA, Chambers H. Structural and functional changes in spastic skeletal muscle. Muscle Nerve. 2004;29:615–627.PubMedCrossRef Lieber RL, Steinman S, Barash IA, Chambers H. Structural and functional changes in spastic skeletal muscle. Muscle Nerve. 2004;29:615–627.PubMedCrossRef
20.
go back to reference Lowenthal M, Tobis JS. Contractures in chronic neurologic diseases. Arch Phys Med Rehabil. 1957;38:640–645.PubMed Lowenthal M, Tobis JS. Contractures in chronic neurologic diseases. Arch Phys Med Rehabil. 1957;38:640–645.PubMed
21.
go back to reference Moriyama H, Kanemura N, Brouns I, Pintelon I, Adriaensen D, Timmermans JP, Ozawa J, Kito N, Gomi T, Deie M. Effects of aging and exercise training on the histological and mechanical properties of articular structures in knee joints of male rat. Biogerontology. 2012;13:369–381.PubMedCrossRef Moriyama H, Kanemura N, Brouns I, Pintelon I, Adriaensen D, Timmermans JP, Ozawa J, Kito N, Gomi T, Deie M. Effects of aging and exercise training on the histological and mechanical properties of articular structures in knee joints of male rat. Biogerontology. 2012;13:369–381.PubMedCrossRef
22.
go back to reference Moriyama H, Nishihara K, Hosoda M, Saka Y, Kanemura N, Takayanagi K, Yoshimura O, Tobimatsu Y. Contrasting alteration patterns of different cartilage plates in knee articular cartilage after spinal cord injury in rats. Spinal Cord. 2009;47:218–224.PubMedCrossRef Moriyama H, Nishihara K, Hosoda M, Saka Y, Kanemura N, Takayanagi K, Yoshimura O, Tobimatsu Y. Contrasting alteration patterns of different cartilage plates in knee articular cartilage after spinal cord injury in rats. Spinal Cord. 2009;47:218–224.PubMedCrossRef
23.
go back to reference Moriyama H, Yoshimura O, Kawamata S, Takayanagi K, Kurose T, Kubota A, Hosoda M, Tobimatsu Y. Alteration in articular cartilage of rat knee joints after spinal cord injury. Osteoarthritis Cartilage. 2008;16:392–398.PubMedCrossRef Moriyama H, Yoshimura O, Kawamata S, Takayanagi K, Kurose T, Kubota A, Hosoda M, Tobimatsu Y. Alteration in articular cartilage of rat knee joints after spinal cord injury. Osteoarthritis Cartilage. 2008;16:392–398.PubMedCrossRef
24.
go back to reference Moriyama H, Yoshimura O, Kawamata S, Takemoto H, Saka Y, Tobimatsu Y. Alteration of knee joint connective tissues during contracture formation in spastic rats after an experimentally induced spinal cord injury. Connect Tissue Res. 2007;48:180–187.PubMedCrossRef Moriyama H, Yoshimura O, Kawamata S, Takemoto H, Saka Y, Tobimatsu Y. Alteration of knee joint connective tissues during contracture formation in spastic rats after an experimentally induced spinal cord injury. Connect Tissue Res. 2007;48:180–187.PubMedCrossRef
25.
go back to reference Moriyama H, Yoshimura O, Sunahori H, Nitta H, Imakita H, Saka Y, Maejima H, Tobimatsu Y. Progression and direction of contractures of knee joints following spinal cord injury in the rat. Tohoku J Exp Med. 2004;204:37–44.PubMedCrossRef Moriyama H, Yoshimura O, Sunahori H, Nitta H, Imakita H, Saka Y, Maejima H, Tobimatsu Y. Progression and direction of contractures of knee joints following spinal cord injury in the rat. Tohoku J Exp Med. 2004;204:37–44.PubMedCrossRef
26.
go back to reference Moriyama H, Yoshimura O, Sunahori H, Tobimatsu Y. Comparison of muscular and articular factors in the progression of contractures after spinal cord injury in rats. Spinal Cord. 2006;44:174–181.PubMedCrossRef Moriyama H, Yoshimura O, Sunahori H, Tobimatsu Y. Comparison of muscular and articular factors in the progression of contractures after spinal cord injury in rats. Spinal Cord. 2006;44:174–181.PubMedCrossRef
27.
go back to reference Poole AR. An introduction to the pathophysiology of osteoarthritis. Front Biosci. 1999;4:D662–670.PubMedCrossRef Poole AR. An introduction to the pathophysiology of osteoarthritis. Front Biosci. 1999;4:D662–670.PubMedCrossRef
28.
go back to reference Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA. The biosynthesis of collagen and its disorders (first of two parts). N Engl J Med. 1979;301:13–23.PubMedCrossRef Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA. The biosynthesis of collagen and its disorders (first of two parts). N Engl J Med. 1979;301:13–23.PubMedCrossRef
29.
go back to reference Pufe T, Lemke A, Kurz B, Petersen W, Tillmann B, Grodzinsky AJ, Mentlein R. Mechanical overload induces VEGF in cartilage discs via hypoxia-inducible factor. Am J Pathol. 2004;164:185–192.PubMedCrossRef Pufe T, Lemke A, Kurz B, Petersen W, Tillmann B, Grodzinsky AJ, Mentlein R. Mechanical overload induces VEGF in cartilage discs via hypoxia-inducible factor. Am J Pathol. 2004;164:185–192.PubMedCrossRef
30.
go back to reference Renner AF, Carvalho E, Soares E, Mattiello-Rosa S. The effect of a passive muscle stretching protocol on the articular cartilage. Osteoarthritis Cartilage. 2006;14:196–202.PubMedCrossRef Renner AF, Carvalho E, Soares E, Mattiello-Rosa S. The effect of a passive muscle stretching protocol on the articular cartilage. Osteoarthritis Cartilage. 2006;14:196–202.PubMedCrossRef
31.
go back to reference Sakamoto J, Origuchi T, Okita M, Nakano J, Kato K, Yoshimura T, Izumi S, Komori T, Nakamura H, Ida H, Kawakami A, Eguchi K. Immobilization-induced cartilage degeneration mediated through expression of hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and chondromodulin-I. Connect Tissue Res. 2009;50:37–45.PubMedCrossRef Sakamoto J, Origuchi T, Okita M, Nakano J, Kato K, Yoshimura T, Izumi S, Komori T, Nakamura H, Ida H, Kawakami A, Eguchi K. Immobilization-induced cartilage degeneration mediated through expression of hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and chondromodulin-I. Connect Tissue Res. 2009;50:37–45.PubMedCrossRef
32.
go back to reference Tabary JC, Tabary C, Tardieu C, Tardieu G, Goldspink G. Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. J Physiol. 1972;224:231–244.PubMed Tabary JC, Tabary C, Tardieu C, Tardieu G, Goldspink G. Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. J Physiol. 1972;224:231–244.PubMed
33.
go back to reference Trudel G, Jabi M, Uhthoff HK. Intraarticular tissue proliferation after immobility: methods of assessment and preliminary results in rat knee joints. J Rheumatol. 1998;25:945–950.PubMed Trudel G, Jabi M, Uhthoff HK. Intraarticular tissue proliferation after immobility: methods of assessment and preliminary results in rat knee joints. J Rheumatol. 1998;25:945–950.PubMed
34.
go back to reference Trudel G, Jabi M, Uhthoff HK. Localized and adaptive synoviocyte proliferation characteristics in rat knee joint contractures secondary to immobility. Arch Phys Med Rehabil. 2003;84:1350–1356.PubMedCrossRef Trudel G, Jabi M, Uhthoff HK. Localized and adaptive synoviocyte proliferation characteristics in rat knee joint contractures secondary to immobility. Arch Phys Med Rehabil. 2003;84:1350–1356.PubMedCrossRef
35.
go back to reference Trudel G, O’Neill PA, Goudreau LA. A mechanical arthrometer to measure knee joint contracture in rats. IEEE Trans Rehabil Eng. 2000;8:149–155.PubMedCrossRef Trudel G, O’Neill PA, Goudreau LA. A mechanical arthrometer to measure knee joint contracture in rats. IEEE Trans Rehabil Eng. 2000;8:149–155.PubMedCrossRef
36.
go back to reference Trudel G, Seki M, Uhthoff HK. Synovial adhesions are more important than pannus proliferation in the pathogenesis of knee joint contracture after immobilization: an experimental investigation in the rat. J Rheumatol. 2000;27:351–357.PubMed Trudel G, Seki M, Uhthoff HK. Synovial adhesions are more important than pannus proliferation in the pathogenesis of knee joint contracture after immobilization: an experimental investigation in the rat. J Rheumatol. 2000;27:351–357.PubMed
37.
go back to reference Trudel G, Uhthoff HK. Contractures secondary to immobility: is the restriction articular or muscular? An experimental longitudinal study in the rat knee. Arch Phys Med Rehabil. 2000;81:6–13.PubMed Trudel G, Uhthoff HK. Contractures secondary to immobility: is the restriction articular or muscular? An experimental longitudinal study in the rat knee. Arch Phys Med Rehabil. 2000;81:6–13.PubMed
38.
go back to reference Trudel G, Uhthoff HK, Brown M. Extent and direction of joint motion limitation after prolonged immobility: an experimental study in the rat. Arch Phys Med Rehabil. 1999;80:1542–1547.PubMedCrossRef Trudel G, Uhthoff HK, Brown M. Extent and direction of joint motion limitation after prolonged immobility: an experimental study in the rat. Arch Phys Med Rehabil. 1999;80:1542–1547.PubMedCrossRef
39.
go back to reference Usuba M, Akai M, Shirasaki Y, Miyakawa S. Experimental joint contracture correction with low torque—long duration repeated stretching. Clin Orthop Relat Res. 2007;456:70–78.PubMedCrossRef Usuba M, Akai M, Shirasaki Y, Miyakawa S. Experimental joint contracture correction with low torque—long duration repeated stretching. Clin Orthop Relat Res. 2007;456:70–78.PubMedCrossRef
40.
go back to reference Vasilceac FA, Renner AF, Teodoro WR, Mattiello-Rosa SM. The remodeling of collagen fibers in rats ankles submitted to immobilization and muscle stretch protocol. Rheumatol Int. 2011;31:737–742.PubMedCrossRef Vasilceac FA, Renner AF, Teodoro WR, Mattiello-Rosa SM. The remodeling of collagen fibers in rats ankles submitted to immobilization and muscle stretch protocol. Rheumatol Int. 2011;31:737–742.PubMedCrossRef
41.
go back to reference Walsh DA, Bonnet CS, Turner EL, Wilson D, Situ M, McWilliams DF. Angiogenesis in the synovium and at the osteochondral junction in osteoarthritis. Osteoarthritis Cartilage. 2007;15:743–751.PubMedCrossRef Walsh DA, Bonnet CS, Turner EL, Wilson D, Situ M, McWilliams DF. Angiogenesis in the synovium and at the osteochondral junction in osteoarthritis. Osteoarthritis Cartilage. 2007;15:743–751.PubMedCrossRef
42.
go back to reference Yarkony GM, Bass LM, Keenan V 3rd, Meyer PR Jr. Contractures complicating spinal cord injury: incidence and comparison between spinal cord centre and general hospital acute care. Paraplegia. 1985;23:265–271.PubMedCrossRef Yarkony GM, Bass LM, Keenan V 3rd, Meyer PR Jr. Contractures complicating spinal cord injury: incidence and comparison between spinal cord centre and general hospital acute care. Paraplegia. 1985;23:265–271.PubMedCrossRef
Metadata
Title
Amount of Torque and Duration of Stretching Affects Correction of Knee Contracture in a Rat Model of Spinal Cord Injury
Authors
Hideki Moriyama, PhD
Yoshiko Tobimatsu, PhD
Junya Ozawa, PhD
Nobuhiro Kito, PhD
Ryo Tanaka, PhD
Publication date
01-11-2013
Publisher
Springer US
Published in
Clinical Orthopaedics and Related Research® / Issue 11/2013
Print ISSN: 0009-921X
Electronic ISSN: 1528-1132
DOI
https://doi.org/10.1007/s11999-013-3196-z

Other articles of this Issue 11/2013

Clinical Orthopaedics and Related Research® 11/2013 Go to the issue

Symposium: ABJS Carl T. Brighton Workshop on Outcome Measures

Measuring Expectations in Orthopaedic Surgery: A Systematic Review