Hindlimb unloading alters ligament healing

Journal of Applied Physiology

Volumn 94, Issue 1, 2003, Pages 314-324

  Provenzano, Paolo P ^a   Martinez, Daniel A ^b   Grindeland, Richard E ^c   Dwyer, Kelley W ^a   Turner, Joanne ^a   Vailas, Arthur C ^b   Vanderby Jr , Ray ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

^c NASA AMES RESEARCH CENTER   (United States)

Author keywords

Biomechanics; Bone; Collagen; Disuse; Hindlimb suspension; Muscle

Indexed keywords

COLLAGEN;

ANIMAL EXPERIMENT; ARTICLE; BIOMECHANICS; BONE; BONE MINERAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMUR; GASTROCNEMIUS MUSCLE; HEALING; HINDLIMB; IMMOBILIZATION; LIGAMENT; LIGAMENT RUPTURE; MALE; MUSCLE; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; RAT; SCAR FORMATION; STRUCTURE ACTIVITY RELATION; TIBIALIS ANTERIOR MUSCLE; YOUNG MODULUS;

EID: 12244298204     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00340.2002     Document Type: Article

References (59)

1. Akeson WH, Amiel D, Abel MF, Garfin SR, and Woo SL. Effects of immobilization on joints. Clin Orthop 219: 28-37, 1987.
2. Almeida-Silveira MI, Lambertz D, Perot C, and Goubel F. Changes in stiffness induced by hindlimb suspension in rat Achilles tendon. Eur J Appl Physiol 81: 252-257, 2000.
3. Amiel D, Akeson WH, Harwood FL, and Frank CB. Stress deprivation effect on metabolic turnover of the medial collateral ligament collagen. A comparison between 9- and 12-week immobilization. Clin Orthop 172: 265-270, 1983.
4. Amiel D, Nagineni CN, Choi SH, and Lee J. Intrinsic properties of ACL and MCL cells and their responses to growth factors. Med Sci Sports Exerc 27: 844-851, 1995.
5. Amiel D, Woo SL, Harwood FL, and Akeson WH. The effect of immobilization on collagen turnover in connective tissue: A biochemical-biomechanical correlation. Acta Orthop Scand 53: 325-332, 1982.
6. Andersen JL, Gruschy-Knudsen T, Sandri C, Larsson L, and Schiaffino S. Bed rest increases the amount of mismatched fibers in human skeletal muscle. J Appl Physiol 86: 455-460, 1999.
7. Bateman TA, Zimmerman RJ, Ayers RA, Ferguson VL, Chapes SK, and Simske SJ. Histomorphometric, physical, and mechanical effects of spaceflight and insulin-like growth factor-I on rat long bones. Bone 23: 527-535, 1998.
8. Bigard AX, Merino D, Lienhard F, Serrurier B, and Guezennec CY. Quantitative assessment of degenerative changes in soleus muscle after hindlimb suspension and recovery. Eur J Appl Physiol 75: 380-387, 1997.
9. Birk DE, Nurminskaya MV, and Zycband EI. Collagen fibrillogenesis in situ: Fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Dev Dyn 202: 229-243, 1995.
10. Birk DE and Trelstad RL. Extracellular compartments in tendon morphogenesis: Collagen fibril, bundle, and macroaggregate formation. J Cell Biol 103: 231-240, 1986.
11. Birk DE, Zycband EI, Winkelmann DA, and Trelstad RL. Collagen fibrillogenesis in situ: Fibril segments are intermediates in matrix assembly. Proc Natl Acad Sci USA 86: 4549-4553, 1989.
12. Birk DE, Zycband EI, Woodruff S, Winkelmann DA, and Trelstad RL. Collagen fibrillogenesis in situ: Fibril segments become long fibrils as the developing tendon matures. Dev Dyn 208:291-298, 1997.
13. Buckwalter JA. Activity vs. rest in the treatment of bone, soft tissue and joint injuries. Iowa Orthop J 15: 29-42, 1995.
14. Collet P, Uebelhart D, Vico L, Moro L, Hartmann D, Roth M, and Alexandre C. Effects of 1- and 6-month spaceflight on bone mass and biochemistry in two humans. Bone 20: 547-551, 1997.
15. Davidson JM, Aquino AM, Woodward SC, and Wilfinger WW. Sustained microgravity reduces intrinsic wound healing and growth factor responses in the rat. FASEB J 13: 325-329, 1999.
16. Frank C, MacFarlane B, Edwards P, Rangayyan R, Liu ZQ, Walsh S, and Bray R. A quantitative analysis of matrix alignment in ligament scars: A comparison of movement versus immobilization in an immature rabbit model. J Orthop Res 9: 219-227, 1991.
17. Frank C, McDonald D, Bray D, Bray R, Rangayyan R, Chimich D, and Shrive N. Collagen fibril diameters in the healing adult rabbit medial collateral ligament. Connect Tissue Res 27: 251-263, 1992.
18. Garber MA, McDowell DL, and Hutton WC. Bone loss during simulated weightlessness: A biomechanical and mineralization study in the rat model. Aviat Space Environ Med 71: 586-592, 2000.
19. Gomez MA, Woo SL, Inoue M, Amiel D, Harwood FL, and Kitabayashi L. Medical collateral ligament healing subsequent to different treatment regimens. J Appl Physiol 66: 245-252, 1989.
20. Graham HK, Holmes DF, Watson RB, and Kadler KE. Identification of collagen fibril fusion during vertebrate tendon morphogenesis. The process relies on unipolar fibrils and is regulated by collagen-proteoglycan interaction. J Mol Biol 295: 891-902, 2000.
21. Hurschler C, Loitz-Ramage B, and Vanderby R Jr. A structurally based stress-stretch relationship for tendon and ligament. J Biomech Eng 119: 392-399, 1997.
22. Hurschler C, Provenzano PP, and Vanderby R Jr. Application of a probabilistic microstructural model to determine reference length and toe-to-linear region transition in fibrous connective tissue. J Biomech Eng. In press.
23. Inoue M, Woo SL, Gomez MA, Amiel D, Ohland KJ, and Kitabayashi LR. Effects of surgical treatment and immobilization on the healing of the medial collateral ligament: A long-term multidisciplinary study. Connect Tissue Res 25: 13-26, 1990.
24. Kannus P, Jarvinen M, Sievanen H, Jarvinen TA, Oja P, and Vuori I. Reduced bone mineral density in men with a previous femur fracture. J Bone Miner Res 9: 1729-1736, 1994.
25. Kannus P, Jarvinen M, Sievanen H, Oja P, and Vuori I. Osteoporosis in men with a history of tibial fracture. J Bone Miner Res 9: 423-429, 1994.
26. Kaplansky AS, Durnova GN, Burkovskaya TE, and Vorotnikova EV. The effect of microgravity on bone fracture healing in rats flown on Cosmos-2044. Physiologist 34 Suppl 1: S196-S199, 1991.
27. Kraemer WJ, Staron RS, Gordon SE, Volek JS, Koziris LP, Duncan ND, Nindl BC, Gomez AL, Marx JO, Fry AC, and Murray JD. The effects of 10 days of spaceflight on the shuttle Endeavor on predominantly fast-twitch muscles in the rat. Histochem Cell Biol 114: 349-355, 2000.
28. Krasnoff J and Painter P. The physiological consequences of bed rest and inactivity. Adv Ren Replace Ther 6: 124-132, 1999.
29. Kubo K, Akima H, Kouzaki M, Ito M, Kawakami Y, Kanehisa H, and Fukunaga T. Changes in the elastic properties of tendon structures following 20 days of bed-rest in humans. Eur J Appl Physiol 83: 463-468, 2000.
30. Law MR, Wald NJ, and Meade TW. Strategies for prevention of osteoporosis and hip fracture. BMJ 303: 453-459, 1991.
31. Majima T, Yasuda K, Fujii T, Yamamoto N, Hayashi K, and Kaneda K. Biomechanical effects of stress shielding of the rabbit patellar tendon depend on the degree of stress reduction. J Orthop Res 14: 377-383, 1996.
32. Morey ER. Spaceflight and bone turnover: Correlation with a new rat model of weightlessness. Bioscience 29: 168-172, 1979.
33. Morey ER and Baylink DJ. Inhibition of bone formation during space flight. Science 201: 1138-1141, 1978.
34. Morey ER, Sabelman EE, Turner RT, and Baylink DJ. A new rat model simulating some aspects of space flight. Physiologist 22: S23-S24, 1979.
35. Noyes FR. Functional properties of knee ligaments and alterations induced by immobilization: A correlative biomechanical and histological study in primates. Clin Orthop 123: 210-242, 1977.
36. Ohno K, Yasuda K, Yamamoto N, Kaneda K, and Hayashi K. Effects of complete stress-shielding on the mechanical properties and histology of in situ frozen patellar tendon. J Orthop Res 11: 592-602, 1993.
37. Padgett LR and Dahners LE. Rigid immobilization alters matrix organization in the injured rat medial collateral ligament. J Orthop Res 10: 895-900, 1992.
38. Provenzano PP, Heisey D, Hayashi K, Lakes R, and Vanderby R Jr. Subfailure damage in ligament: A structural and cellular evaluation. J Appl Physiol 92: 362-371, 2002.
39. Provenzano PP, Hurschler C, and Vanderby R Jr. Microstructural morphology in the transition region between scar and intact residual segments of a healing rat medial collateral ligament. Connect Tissue Res 42: 123-133, 2001.
40. Provenzano PP, Lakes RS, Keenan T, and Vanderby R Jr. Nonlinear ligament viscoelasticity. Ann Biomed Eng 29: 908-914, 2001.
41. Shaw SR, Vailas AC, Grindeland RE, and Zernicke RF. Effects of a 1-wk spaceflight on morphological and mechanical properties of growing bone. Am J Physiol Regul Integr Comp Physiol 254: R78-R83, 1988.
42. Shrive N, Chimich D, Marchuk L, Wilson J, Brant R, and Frank C. Soft-tissue "flaws" are associated with the material properties of the healing rabbit medial collateral ligament. J Orthop Res 13: 923-929, 1995.
43. Smith SM, Nillen JL, Leblanc A, Lipton A, Demers LM, Lane HW, and Leach CS. Collagen cross-link excretion during space flight and bed rest. J Clin Endocrinol Metab 83: 3584-3591, 1998.
44. Stauber WT, Fritz VK, Burkovskaya TE, and Ilyina-Kakueva EI. Effect of spaceflight on the extracellular matrix of skeletal muscle after a crush injury. J Appl Physiol 73: 74-81, 1992.
45. Thornton G, Sorbetti J, Teskey V, Shrive N, and Frank CB. Healing ligament mechanical properties are equivalent after either unilateral or bilateral surgeries. Trans 48th Ann Ortho Res Soc Meet. Paper 0632, 2002.
46. Uebelhart D, Bernard J, Hartmann DJ, Moro L, Roth M, Uebelhart B, Rehailia M, Mauco G, Schmitt DA, Alexandre C, and Vico L. Modifications of bone and connective tissue after orthostatic bedrest. Osteoporos Int 11: 59-67, 2000.
47. Vailas AC, Deluna DM, Lewis LL, Curwin SL, Roy RR, and Alford EK. Adaptation of bone and tendon to prolonged hindlimb suspension in rats. J Appl Physiol 65: 373-376, 1988.
48. Vailas AC, Vanderby R Jr, Martinez DA, Ashman RB, Ulm MJ, Grindeland RE, Durnova GN, and Kaplansky A. Adaptations of young adult rat cortical bone to 14 days of spaceflight. J Appl Physiol 73: 4-9, 1992.
49. Vailas AC, Zernicke RF, Grindeland RE, and Li KC. Suspension effects on rat femur-medial collateral ligament-tibia unit. Am J Physiol Regul Integr Comp Physiol 258: R724-R728, 1990.
50. Van der Poest Clement E, van der Wiel H, Patka P, Roos JC, and Lips P. Long-term consequences of fracture of the lower leg: Cross-sectional study and long-term longitudinal follow-up of bone mineral density in the hip after fracture of lower leg. Bone 24: 131-134, 1999.
51. Vanderby R Jr, Vailas AC, Graf BK, Thielke RJ, Ulm MJ, Kohles SS, and Kunz DN. Acute modification of biomechanical properties of the bone-ligament insertion to rat limb unweighting. FASEB J 4: 2499-2505, 1990.
52. Widrick JJ, Knuth ST, Norenberg KM, Romatowski JG, Bain JL, Riley DA, Karhanek M, Trappe SW, Trappe TA, Costill DL, and Fitts RH. Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J Physiol 516:915-930, 1999.
53. Woo SL, Gomez MA, Sites TJ, Newton PO, Orlando CA, and Akeson WH. The biomechanical and morphological changes in the medial collateral ligament of the rabbit after immobilization and remobilization. J Bone Joint Surg Am 69: 1200-1211, 1987.
54. Woo SL, Inoue M, McGurk-Burleson E, and Gomez MA. Treatment of the medial collateral ligament injury. II. Structure and function of canine knees in response to differing treatment regimens. Am J Sports Med 15: 22-29, 1987.
55. Woo SL, Orlando CA, Camp JF, and Akeson WH. Effects of postmortem storage by freezing on ligament tensile behavior. J Biomech 19: 399-404, 1986.
56. Wronski TJ and Morey ER. Skeletal abnormalities in rats induced by simulated weightlessness. Metab Bone Dis Relat Res 4: 69-75, 1982.
57. Wronski TJ and Morey ER. Effect of spaceflight on periosteal bone formation in rats. Am J Physiol Regul Integr Comp Physiol 244: R305-R309, 1983.
58. Wronski TJ, and Morey-Holton ER. Skeletal response to simulated weightlessness: A comparison of suspension techniques. Aviat Space Environ Med 58: 63-68, 1987.
59. Yamamoto N, Ohno K, Hayashi K, Kuriyama H, Yasuda K, and Kaneda K. Effects of stress shielding on the mechanical properties of rabbit patellar tendon. J Biomech Eng 115: 23-28, 1993.