Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2014

Open Access 01-12-2014 | Research article

Contributions of biarticular myogenic components to the limitation of the range of motion after immobilization of rat knee joint

Authors: Momoko Nagai, Tomoki Aoyama, Akira Ito, Hirotaka Iijima, Shoki Yamaguchi, Junichi Tajino, Xiangkai Zhang, Haruhiko Akiyama, Hiroshi Kuroki

Published in: BMC Musculoskeletal Disorders | Issue 1/2014

Login to get access

Abstract

Background

Muscle atrophy caused by immobilization in the shortened position is characterized by a decrease in the size or cross-sectional area (CSA) of myofibers and decreased muscle length. Few studies have addressed the relationship between limitation of the range of motion (ROM) and the changes in CSA specifically in biarticular muscles after atrophy because of immobilization. We aimed to determine the contribution of 2 distinct muscle groups, the biarticular muscles of the post thigh (PT) and those of the post leg (PL), to the limitation of ROM as well as changes in the myofiber CSAs after joint immobilization surgery.

Methods

Male Wistar rats (n = 40) were randomly divided into experimental and control groups. In the experimental group, the left knee was surgically immobilized by external fixation for 1, 2, 4, 8, or 16 weeks (n = 5 each) and sham surgery was performed on the right knee. The rats in the control groups (n = 3 per time point) did not undergo surgery. After the indicated immobilization periods, myotomy of the PT or PL biarticular muscles was performed and the ROM was measured. The hamstrings and gastrocnemius muscles from the animals operated for 1 or 16 weeks were subjected to morphological analysis.

Results

In immobilized knees, the relative contribution of the PT biarticular myogenic components to the total restriction reached 80% throughout the first 4 weeks and decreased thereafter. The relative contribution of the PL biarticular myogenic components remained <20% throughout the immobilization period. The ratio of the myofiber CSA of the immobilized to that of the sham-operated knees was significantly lower at 16 weeks after surgery than at 1 week after surgery only in the hamstrings.

Conclusions

The relative contribution of the PT and PL components to myogenic contracture did not significantly change during the experimental period. However, the ratio of hamstrings CSAs to the sham side was larger than the ratio of medial gastrocnemius CSAs to the sham side after complete atrophy because of immobilization.
Appendix
Available only for authorised users
Literature
1.
go back to reference Hildebrand KA, Sutherland C, Zhang M: Rabbit knee model of post-traumatic joint contractures: the long-term natural history of motion loss and myofibroblasts. J Orthop Res. 2004, 31: 313-320.CrossRef Hildebrand KA, Sutherland C, Zhang M: Rabbit knee model of post-traumatic joint contractures: the long-term natural history of motion loss and myofibroblasts. J Orthop Res. 2004, 31: 313-320.CrossRef
2.
go back to reference van Bosse HJ, Feldman DS, Anavian J, Sala DA: Treatment of knee flexion contractures in patients with arthrogryposis. J Pediatr Orthop. 2007, 27: 930-937.CrossRefPubMed van Bosse HJ, Feldman DS, Anavian J, Sala DA: Treatment of knee flexion contractures in patients with arthrogryposis. J Pediatr Orthop. 2007, 27: 930-937.CrossRefPubMed
3.
go back to reference Frank C, Akeson WH, Woo SL, Amiel D, Coutts RD: Physiology and therapeutic value of passive joint motion. Clin Orthop Relat Res. 1984, 185: 113-125.PubMed Frank C, Akeson WH, Woo SL, Amiel D, Coutts RD: Physiology and therapeutic value of passive joint motion. Clin Orthop Relat Res. 1984, 185: 113-125.PubMed
4.
go back to reference Oates BR, Glover EI, West DW, Fry JL, Tarnopolsky MA, Phillips SM: Low-volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve. 2010, 42: 539-546.CrossRefPubMed Oates BR, Glover EI, West DW, Fry JL, Tarnopolsky MA, Phillips SM: Low-volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle Nerve. 2010, 42: 539-546.CrossRefPubMed
5.
go back to reference Gajdok RL: Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech. 2001, 16: 87-101.CrossRef Gajdok RL: Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech. 2001, 16: 87-101.CrossRef
6.
go back to reference Mai MT, Lieber RL: A model of semitendinosus muscle sarcomere length, knee and hip joint interaction in the frog hind limb. J Biomech. 1990, 23: 271-279.CrossRefPubMed Mai MT, Lieber RL: A model of semitendinosus muscle sarcomere length, knee and hip joint interaction in the frog hind limb. J Biomech. 1990, 23: 271-279.CrossRefPubMed
7.
go back to reference Booth FW, Seider MJ: Early change in skeletal muscle protein synthesis after limb immobilization of rats. J Appl Physiol. 1979, 47: 974-977.PubMed Booth FW, Seider MJ: Early change in skeletal muscle protein synthesis after limb immobilization of rats. J Appl Physiol. 1979, 47: 974-977.PubMed
8.
go back to reference Nesterenko S, Morrey ME, Abdel MP, An KN, Steinmann SP, Morrey BF, Sanchez-Sotelo J: New rabbit knee model of posttraumatic joint contracture: indirect capsular damage induces a severe contracture. J Orthop Res. 2009, 27: 1028-1032.CrossRefPubMed Nesterenko S, Morrey ME, Abdel MP, An KN, Steinmann SP, Morrey BF, Sanchez-Sotelo J: New rabbit knee model of posttraumatic joint contracture: indirect capsular damage induces a severe contracture. J Orthop Res. 2009, 27: 1028-1032.CrossRefPubMed
10.
go back to reference Ishikawa T, Shimizu M, Mikawa Y, Zhu BL, Quan L, Li DR, Zhao D, Maeda H: Pathology of experimental disuse muscular atrophy in rats. Connect Tissue Res. 2005, 46: 101-106.CrossRefPubMed Ishikawa T, Shimizu M, Mikawa Y, Zhu BL, Quan L, Li DR, Zhao D, Maeda H: Pathology of experimental disuse muscular atrophy in rats. Connect Tissue Res. 2005, 46: 101-106.CrossRefPubMed
11.
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.CrossRefPubMed 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.CrossRefPubMed
12.
go back to reference Booth FW: Effect of limb immobilization on skeletal muscle. J Appl Physiol. 1982, 52: 1113-1118.PubMed Booth FW: Effect of limb immobilization on skeletal muscle. J Appl Physiol. 1982, 52: 1113-1118.PubMed
13.
go back to reference Spector SA, Simard CP, Fournier M, Sternlicht E, Edgerton VR: Architectural alterations of rat hind-limb skeletal muscles immobilized at different lengths. Exp Neurol. 1982, 76: 94-110.CrossRefPubMed Spector SA, Simard CP, Fournier M, Sternlicht E, Edgerton VR: Architectural alterations of rat hind-limb skeletal muscles immobilized at different lengths. Exp Neurol. 1982, 76: 94-110.CrossRefPubMed
14.
go back to reference Järvinen TA, Józsa L, Kannus P, Järvinen TL, Järvinen M: Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles. An immunohistochemical, polarization and scanning electron microscopic study. J Muscle Res Cell Motil. 2002, 23: 245-254.CrossRefPubMed Järvinen TA, Józsa L, Kannus P, Järvinen TL, Järvinen M: Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles. An immunohistochemical, polarization and scanning electron microscopic study. J Muscle Res Cell Motil. 2002, 23: 245-254.CrossRefPubMed
15.
go back to reference Borg TK, Caulfield JB: Morphology of connective tissue in skeletal muscle. Tissue Cell. 1980, 12: 197-207.CrossRefPubMed Borg TK, Caulfield JB: Morphology of connective tissue in skeletal muscle. Tissue Cell. 1980, 12: 197-207.CrossRefPubMed
16.
go back to reference Okita M, Yoshimura T, Nakano J, Motomura M, Eguchi K: Effects of reduced joint mobility on sarcomere length, collagen fibril arrangement in the endomysium, and hyaluronan in rat soleus muscle. J Muscle Res Cell Motil. 2004, 25: 159-166.CrossRefPubMed Okita M, Yoshimura T, Nakano J, Motomura M, Eguchi K: Effects of reduced joint mobility on sarcomere length, collagen fibril arrangement in the endomysium, and hyaluronan in rat soleus muscle. J Muscle Res Cell Motil. 2004, 25: 159-166.CrossRefPubMed
17.
go back to reference Alnaqeeb MA, Goldspink G: Changes in fibre type, number and diameter in developing and ageing skeletal muscle. J Anat. 1987, 153: 31-45.PubMedPubMedCentral Alnaqeeb MA, Goldspink G: Changes in fibre type, number and diameter in developing and ageing skeletal muscle. J Anat. 1987, 153: 31-45.PubMedPubMedCentral
19.
go back to reference Boonyarom O, Inui K: Atrophy and hypertrophy of skeletal muscles: structural and functional aspects. Acta Physiol. 2006, 188: 77-89.CrossRef Boonyarom O, Inui K: Atrophy and hypertrophy of skeletal muscles: structural and functional aspects. Acta Physiol. 2006, 188: 77-89.CrossRef
20.
go back to reference Zhang P, Chen X, Fan M: Signaling mechanisms involved in disuse muscle atrophy. Med Hypotheses. 2007, 69: 310-321.CrossRefPubMed Zhang P, Chen X, Fan M: Signaling mechanisms involved in disuse muscle atrophy. Med Hypotheses. 2007, 69: 310-321.CrossRefPubMed
21.
go back to reference Zajac FE: Understanding muscle coordination of the human leg with dynamical simulations. J Biomech. 2002, 35: 1011-1018.CrossRefPubMed Zajac FE: Understanding muscle coordination of the human leg with dynamical simulations. J Biomech. 2002, 35: 1011-1018.CrossRefPubMed
22.
go back to reference Rushton A, Spencer S: The effect of soft tissue mobilisation techniques on flexibility and passive resistance in the hamstring muscle-tendon unit: a pilot investigation. Man Ther. 2011, 16: 161-166.CrossRefPubMed Rushton A, Spencer S: The effect of soft tissue mobilisation techniques on flexibility and passive resistance in the hamstring muscle-tendon unit: a pilot investigation. Man Ther. 2011, 16: 161-166.CrossRefPubMed
23.
go back to reference Kwah LK, Herbert RD, Harvey LA, Diong J, Clarke JL, Martin JH, Clarke EC, Hoang PD, Bilston LE, Gandevia SC: Passive mechanical properties of gastrocnemius muscles of people with ankle contracture after stroke. Arch Phys Med Rehabil. 2012, 93: 1185-1190.CrossRefPubMed Kwah LK, Herbert RD, Harvey LA, Diong J, Clarke JL, Martin JH, Clarke EC, Hoang PD, Bilston LE, Gandevia SC: Passive mechanical properties of gastrocnemius muscles of people with ankle contracture after stroke. Arch Phys Med Rehabil. 2012, 93: 1185-1190.CrossRefPubMed
24.
go back to reference Whatman C, Knappstein A, Hume P: Acute changes in passive stiffness and range of motion post-stretching. Phys Ther Sport. 2006, 7: 195-200.CrossRefPubMed Whatman C, Knappstein A, Hume P: Acute changes in passive stiffness and range of motion post-stretching. Phys Ther Sport. 2006, 7: 195-200.CrossRefPubMed
25.
go back to reference Usuba M, Miyanaga Y, Miyakawa S, Maeshima T, Shirasaki Y: Effect of heat in increasing the range of knee motion after the development of a joint contracture: an experiment with an animal model. Arch Phys Med Rehabil. 2006, 87: 247-253.CrossRefPubMed Usuba M, Miyanaga Y, Miyakawa S, Maeshima T, Shirasaki Y: Effect of heat in increasing the range of knee motion after the development of a joint contracture: an experiment with an animal model. Arch Phys Med Rehabil. 2006, 87: 247-253.CrossRefPubMed
26.
go back to reference Fukui N, Tashiro T, Hiraoka H, Oda H, Nakamura K: Adhesion formation can be reduced by the suppression of transforming growth factor-beta1 activity. J Orthop Res. 2000, 18: 212-219.CrossRefPubMed Fukui N, Tashiro T, Hiraoka H, Oda H, Nakamura K: Adhesion formation can be reduced by the suppression of transforming growth factor-beta1 activity. J Orthop Res. 2000, 18: 212-219.CrossRefPubMed
27.
go back to reference Rowe RW, Goldspink G: Muscle fibre growth in five different muscles in both sexes of mice. II Dystrophic Mice J Anat. 1969, 104: 531-538.PubMed Rowe RW, Goldspink G: Muscle fibre growth in five different muscles in both sexes of mice. II Dystrophic Mice J Anat. 1969, 104: 531-538.PubMed
28.
go back to reference Williams PE, Goldspink G: Longitudinal growth of striated muscle fibres. J Cell Sci. 1971, 9: 751-767.PubMed Williams PE, Goldspink G: Longitudinal growth of striated muscle fibres. J Cell Sci. 1971, 9: 751-767.PubMed
29.
go back to reference Lieber RL, Blevins FT: Skeletal muscle architecture of the rabbit hind limb: functional implications of muscle design. J Morphol. 1989, 199: 93-101.CrossRefPubMed Lieber RL, Blevins FT: Skeletal muscle architecture of the rabbit hind limb: functional implications of muscle design. J Morphol. 1989, 199: 93-101.CrossRefPubMed
30.
go back to reference Eng CM, Smallwood LH, Rainiero MP, Lahey M, Ward SR, Lieber RL: Scaling of muscle architecture and fiber types in the rat hind limb. J Exp Biol. 2008, 211: 2336-2345.CrossRefPubMed Eng CM, Smallwood LH, Rainiero MP, Lahey M, Ward SR, Lieber RL: Scaling of muscle architecture and fiber types in the rat hind limb. J Exp Biol. 2008, 211: 2336-2345.CrossRefPubMed
31.
go back to reference Grosset JF, Onambele-Pearson G: Effect of foot and ankle immobilization on leg and thigh muscles' volume and morphology: a cases study using magnetic resonance imaging. Anat Rec. 2008, 291: 1673-1683.CrossRef Grosset JF, Onambele-Pearson G: Effect of foot and ankle immobilization on leg and thigh muscles' volume and morphology: a cases study using magnetic resonance imaging. Anat Rec. 2008, 291: 1673-1683.CrossRef
32.
go back to reference Samukawa M, Hattori M, Sugama N, Takeda N: The effects of dynamic stretching on plantar flexor muscle-tendon tissue properties. Man Ther. 2011, 16: 618-622.CrossRefPubMed Samukawa M, Hattori M, Sugama N, Takeda N: The effects of dynamic stretching on plantar flexor muscle-tendon tissue properties. Man Ther. 2011, 16: 618-622.CrossRefPubMed
33.
go back to reference Blackburn JT, Riemann BL, Padua DA, Guskiewicz KM: Sex comparison of extensibility, passive, and active stiffness of the knee flexors. Clin Biomech. 2004, 19: 36-43.CrossRef Blackburn JT, Riemann BL, Padua DA, Guskiewicz KM: Sex comparison of extensibility, passive, and active stiffness of the knee flexors. Clin Biomech. 2004, 19: 36-43.CrossRef
34.
go back to reference Wakahara T, Ushiyama J, Kanehisa H, Kawakami Y, Fukunaga T: Effect of passive ankle and knee joint motions on the length of fascicle and tendon of the medial gastrocnemius muscle. Int J Sports Health Sci. 2005, 3: 75-82.CrossRef Wakahara T, Ushiyama J, Kanehisa H, Kawakami Y, Fukunaga T: Effect of passive ankle and knee joint motions on the length of fascicle and tendon of the medial gastrocnemius muscle. Int J Sports Health Sci. 2005, 3: 75-82.CrossRef
Metadata
Title
Contributions of biarticular myogenic components to the limitation of the range of motion after immobilization of rat knee joint
Authors
Momoko Nagai
Tomoki Aoyama
Akira Ito
Hirotaka Iijima
Shoki Yamaguchi
Junichi Tajino
Xiangkai Zhang
Haruhiko Akiyama
Hiroshi Kuroki
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2014
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/1471-2474-15-224

Other articles of this Issue 1/2014

BMC Musculoskeletal Disorders 1/2014 Go to the issue