BMP treatment for improving tendon repair Studies on rat and rabbit Achilles tendons

Acta Orthopaedica Scandinavica

Volumn 74, Issue sup308, 2002, Pages 1-30

  Forslund, Carina ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CARTILAGE DERIVED MORPHOGENETIC PROTEIN; COLLAGEN; FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCAN; GROWTH FACTOR; OSTEOGENIC PROTEIN 1; OSTEOGENIN; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; GROWTH PROMOTOR;

ACHILLES TENDON RUPTURE; BIOMECHANICS; CARTILAGE; EXERCISE; HEALING; HISTOPATHOLOGY; LIGAMENT INJURY; MOBILIZATION; NONHUMAN; RABBIT; REVIEW; SPORT INJURY; SURGICAL TECHNIQUE; TENDINITIS; TENDON INJURY; TENDON RECONSTRUCTION; ACHILLES TENDON; ANIMAL; ARTICLE; CLINICAL TRIAL; COMPARATIVE STUDY; CONTROLLED CLINICAL TRIAL; DISEASE MODEL; IMMOBILIZATION; INJURY; PLASTER CAST; RANDOMIZED CONTROLLED TRIAL; RAT; RUPTURE; TENSILE STRENGTH; TIME; WOUND HEALING;

ACHILLES TENDON; ANIMALS; BIOMECHANICS; BONE MORPHOGENETIC PROTEINS; CASTS, SURGICAL; DISEASE MODELS, ANIMAL; GROWTH SUBSTANCES; IMMOBILIZATION; RABBITS; RANDOMIZED CONTROLLED TRIALS; RATS; RUPTURE; TENDON INJURIES; TENSILE STRENGTH; TIME FACTORS; WOUND HEALING;

EID: 0037324856     PISSN: 00016470     EISSN: 17453682     Source Type: Journal    
DOI: 10.1080/000164702760300006     Document Type: Article

References (102)

1. Ackermann P. 2001. Peptidergic innervation of periarticular tissue -A study in the rat. In: Department of Surgical Sci-ences. Stockholm: Karolinska Institutet. p 70.
2. Ahmed IM, Lagopoulos M, McConnell P, Soames RW, Sefton GK. 1998. Blood supply of the Achilles tendon. J Orthop Res 16: 591 – 596.
3. Akeson WH, Woo SL-Y, Amiel D, Frank CB. 1984. The Biology of ligaments. In: Rehabilitation of the injured knee. St Louis: Mosby.
4. Andersen E, Hvass I. 1986. Suture of achilles tendon rupture under local anesthesia. Acta Orthop Scand 57: 235 – 236.
5. Aracil J, Pina A, Lozano JA, TOITO V, Escriba I. 1992. Per-cutaneous suture of Achilles tendon ruptures. Foot Ankle 13: 350 – 351.
6. Armbrecht A, Zenker W, Egsbers HJ, Havemann D. 1993. Plaster-free, early functional after-care of surgically man-aged Achilles tendon rupture. 64: 926 – 930.
7. Backman C, Friden J, Widmark A. 1991. Blood flow in chronic Achilles tendinosis. Radioactive microsphere study in rabbits. Acta Orthop Scand 62: 386 – 387.
8. Batten ML, Hansen JC, Dahners LE. 1996. Influence of dosage and timing of application of platelet-derived growth factor on early healing of the rat medial collateral ligament. J Orthop Res 14: 736 – 741.
9. Benjamin M, Ralphs JR. 1997. Tendons and ligaments - an overview. Histol Histopathol 12: 1135 – 1144.
10. Bray RC, Rangayyan RM, Frank CB. 1996. Normal and healing ligament vascularity: a quantitative histological assessment in the adult rabbit medial collateral ligament. J Anat. 188: 87 – 95.
11. Carr AJ, Norris SH. 1989. The blood supply of the calcaneal tendon. J Bone Joint Surg Br 71: 100 – 101.
12. Carter DR, van der Muelen MCH, Beaupré GS. 1996. Mechanical factors in bone growth and development. Bone 18: 5 – 10.
13. Cetti R, Christensen SE, Reuther K. 1981. Ruptured achilles tendons treated surgically under local anaesthesia. Acta Orthop Scand 52: 675 – 677.
14. Cetti R, Henriksen LO, Jacobsen KS. 1994. A new treatment of ruptured Achilles tendons. A prospective randomized study. Chin Orthop 308: 155 – 165.
15. Chan BP, Chan KM, Maffulli N, Webb S, Lee KKH. 1997. Effect of basic fibroblast growth factor. Clin Orthop 342: 239 – 247.
16. Chang SC, Hoang B, Thomas JT, Vukiceciv S, Luyten FP, Ryba NJ, Kozak CA, Reddi AH, Moos MJ. 1994. Carti-lage-derived morphogentic proteins. New members of the transforming growth factor-beta superfamily predomi-nantly expressed in long bones during human embryonic development. J Biol Chem 269: 28227 – 28234.
17. Chowdhury P, Matyas JR, Frank CB. 1991. The “epiliga-ment” of the rabbit medial collateral ligament: a quantita-tive morphological study. Connect Tissue Res 27: 33 – 50.
18. Duey P, Karsenty G. 2000. The family of bone morphoge-netic proteins. Kidney Int 57: 2207 – 2214.
19. Ebendal T, Bengtsson H, Soderstrom S. 1998. Bone mor-phogenetic proteins and their receptors: potential func-tions in the brain. J Neurosci Res 51: 139 – 146.
20. Enwemeka CS. 1989. Inflammation, cellularity, an fibril-logenesis in regenerating tendon: Implications for tendon rehabilitation. Physical Therapy 69: 816 – 824.
21. Enwemeka CS. 1992. Functional loading augments the initial tensile strength and energy absorption capacity of regenerating tabbit achilles tendons. Am J Phys Med Rehabil 71: 31 – 38.
22. Enwemeka CS, I. SN, Nelson AJ. 1988. The effect of early functional activities on experimentally tenotomized Achilles tendons in rats. Am J Phys Med Rehabil 67: 264 – 269.
23. Erlacher L, McCartney J, Piek E, Ten Duke P, Yanagishita M, Oppermann H, Luyten F. 1998. Cartilage-derived morphogenetic proteins and osteogenic protein-1 diffren-tially regulate osteogenesis. JBMR 13: 2 – 11.
24. Forslund C, Aspenberg P. 1998. OP-1 has more effect than mechanical signals in the control of tissue differentiation in healing rat tendon. Acta Orthop Scand 69: 622 – 626.
25. Gehlsen GM, Ganion LR, Helfst R. 1999. Fibroblast responses to variation in soft tissue mobilization pressure. Med Sci Sports Exerc 31: 531 – 535.
26. Gillard GC, Reilly HC, Bell-Booth PG, Flint MH. 1979. The influence of mechanical forces on the glycosaminoglycan content of the rabbit flexor digitorum profundus tendon. Connect Tissue Res 7: 37 – 46.
27. Giori NJ, Beaupre GS, Carter DR. 1993. Cellular shape and pressure may mediate mechanical control of tissue com-position in tendons. J Orthop Res 11 (4): 581 – 591.
28. Graff JM. 1997. Embryonic patterning: to BMP or not to BMP, that is the question. Cell 89: 171 – 174.
29. Gruber R, Mayer C, Schulz W, Graninger W, Peterlik M, Watzek G, Luyten FP, Erlacher L. 2000. Stimulatory effects of cartilage-derived morphogenetic proteins 1 and 2 on osteogenic differentiation of bone marrow stromal cells. Cytokine 12: 1630 – 1638.
30. Hart DA, Frank CB, Bray RC. 1985. Inflammatory pro-cesses in repetetive motion and oeveruse syndromes: Potential role of neurogeic mechanisms in tendons and ligaments. In: Repetetive motion disorders of the upper extremity. Rosemont.
31. Helm GA, Li JZ, Alden TD, Hudson SB, Beres EJ, Cun-ningham M, Mikkelsen MM, Pittman DD, Kerns KM, Kallmes DF. 2001. A light and electron microscopic study of ectopic tendon and ligament formation induced by bone morphogenetic protein-13 adenoviral gene therapy. J Neurosurg 95: 298 – 307.
32. Hergenroeder PT, Gelberman RH, Akeson WH. 1982. Yhe vascularity of the flexor pollicis longus tendon. Chin Orthop 162: 298 – 303.
33. Hess GP, Cappiello WL, Poole RM, Hunter SC. 1989. Pre-vention and treatment of overuse tendon injuries. Sports Med 8: 371 – 384.
34. Hildebrand KA, Woo SL, Smith DW, Allen CR, Deie M, Taylor BJ, Schmiddt CC. 1998. The effects of platelet-derived growth factor-BB on healing of the rabbit medial collateral ligament. An in vivo study. Am J Sports Med 26: 549 – 554.
35. Hogan BL. 1996. Bone morphogenetic proteins: multifunc-tional regulators of vertebrate developement. Genes Dev 10: 1580 – 1594.
36. Jones CM, Lyons KM, Hogan BL. 1991. Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Develop-ment 111: 531 – 542.
37. Jozsa L, Lehto M, Kvist M, Balint JB, Reffy A. 1989. Altera-tions in dry mass content of collagen fibers in degenera-tive tendinopathy and tendon-rupture. Matrix 9: 140 – 146.
38. Kannus P. Jozsa L. 1991. Histopathological changes preced-ing spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg [Am] 73: 1507 – 1525.
39. Kannus P. Natri A. 1997. Etiology and pathophysiology of tendon ruptures in sports. Scand J Med Sci Sports 7: 107 – 112.
40. Keller J, Bak B. 1989. The use of anesthesia for surgical treatment of Achilles tendon rupture. Orthopedics 12: 431 – 433.
41. Ketchum LD. 1977. Primary tendon healing: a review. J Hand Surg [Am] 2: 428 – 435.
42. Kolts I, Tillmann B, Lullmann-Rauch R. 1994. The struc-ture and vascularization of the biceps brachii long head tendon. Anat Anz 176: 75 – 80.
43. Koob TJ, Vogel KG. 1987. Proteoglycan synthesis in organ cultures from regions of bovine tendon subjected to dif-ferent mechanical forces. Biochem J 246: 589 – 598.
44. Kurtz CA, Loebig TG, Anderson DD, De Meo PJ, Camp-bell PG. 1999. Insulin-like growth factor 1 accelerates functional recovery from Achilles tendon injury in a rat model. Am J Sports Med 27: 363 – 369.
45. Kvist M, Jozsa L, Jarvinen M. 1992. Vascular changes in the ruptured Achilles tendon and paratenon. Int Orthop 16: 377 – 382.
46. Levander G. 1938. A study of bone regeneration. Surgery, gynecology and obstetrics 67: 705 – 714.
47. Lou J, Tu Y, Burns M, Silva MJ, Manske PR. 2001. BMP-12 gene transfer augmentation of lacerated tendon repair. J Orthop Res 19: 1199 – 1202.
48. Lou J, Tu Y, Ludwig FJ, Zhang J, Manske PR. 1999. Effect of bone morphogenetic protein-12 gene transfer on mes-enchymal progenitor cells. Chin Orthop 369: 333 – 339.
49. Lundborg G, Holm S, Myrhage R. 1980. The role of the synovial fluid and tendon sheath for flexor tendon nutri-tion. An experimental tracer study on diffusional path-ways in dogs. Scand J Plast Reconstr Surg 14: 99 – 107.
50. Lundborg G, Myrhage R, Rydevik B. 1977. The vasculariza-tion of human flexor tendons within the digital synovial sheath region--structureal and functional aspects. J Hand Surg [Am] 2: 417 – 427.
51. Luyten FP, Cunningham NS, Ma S, Muthukumaran N, Hammonds RG, Nevins WB, Woods WI, Reddi AH. 1989. Purification and partial amino acid sequence of osteogenin, a protein initiating bone differentiation. J Biol Chem 264: 13377 – 13380.
52. McComis GP, Nawoczenski DA, DeHaven KE. 1997. Func-tional bracing for rupture of the Achilles tendon. Clinical results and analysis of ground-reaction forces and tempo-ral data. J Bone Joint Surg [Am] 79-A: 1799 – 1808.
53. Merrilees MJ, Flint MH. 1980. Ultrastructural study of ten-sion and pressure zones in a rabbit flexor tendon. Am J Anat 157: 87 – 106.
54. Messner K, Wei Y, Andersson B, Gillquist J, Rasanen T. 1999. Rat model of Achilles tendon disorder. A pilot study. Cells Tissues Organs 165: 30 – 39.
55. Mikic B, Schalet BJ, Clark RT, Gaschen V, Hunziker EB. 2001. GDF-5 deficiency in mice alters the ultrastructure, mechanical properties and composition of the Achilles tendon. J Orthop Res 19: 365 – 371.
56. Mortensen HM, Skov O, Jensen PE. 1999. Early motion of the ankle after operative treatment of a rupture of the Achilles tendon. A prospective, randomized clinical and radiographic study. J Bone Joint Surg [Am] 81: 983 – 990.
57. Murrell GA, Jong D, Deng XH, Hannafin JA, Warren RF. 1998. Effects of exercise on Achilles tendon healing in a rat model. Foot Ankle Int 19: 598 – 603.
58. Murrell GAC, Lilly EG, Goldner RD, Seaber AV, Best TM. 1994. Effects of immobilization on Achilles tendon heal-ing in a rat model. J Orthop Res 12: 582 – 591.
59. Moller M. 2001. On the treatment of Achilles Tendon rup-ture. A Prospective, randomised study of the results after surgical and non-surgical treatment. In: Department of Orthopedics, Institute of Surgical Science. Goteborg: Goteborg University.
60. Moller M, Movin T, Granhed H, Lind K, Faxen E, Karlson J. 2001. Acute rupture of tendon Achilles. A prospec-tive randomised study of comparison between surgical and non-surgical treatment. J Bone Joint Surg [Br] 83: 843 – 848.
61. Naito M, Ogata K. 1983. The blood supply of the tendon with a paratenon. An experimental study using hydrogen washout technique. Hand 15: 9 – 14.
62. Nakase T, Ariga K, Yonenobu K, Tsumaki N, Luyten FP, Mukai Y, Sato I, Yoshikawa H. 2001. Activation and localization of cartilage-derived morphogenetic protein-1 at the site of ossification of the ligamentum flavum. Eur Spine J 10: 289 – 294.
63. Neuberger A, Slack HGB. 1953. The metabolism of collagen from lover, bone, skin and tednon on the normal rat. Bio-chem J 53: 47 – 52.
64. Nistor L. 1981. Surgical and Non-Surgical Treatment of Achilles Tendon Rupture. J Bone Joint Surg [Am] 63-A: 394 – 399.
65. Okuda Y, Gorski JP, An KN, Amadio PC. 1987. Biochemi-cal, histological, and biomechanical analyses of canine tendon. J Orthop Res 5: 60 – 68.
66. Pauwels. 1960. Eine neue Theorie -fiber den Einflu B mecha-nischer Reize auf die Differenzierung der Stazgewebe. Z Anat Entwicklungsgeschichte 121: 478 – 515.
67. Ploetz E. 1938. Funktioneller Bau und funktioneller Anpas-sung der Gleitsehnen (D 25). Z Orthopedie 67: 212 – 234.
68. Rantanen J, Hurme T, Kalimo H. 1999. Calf muscle atro-phy and Achilles tendon healing following experimental tendon division and surgery in rats. Comparison of post-operative immibilisation of the muscle-tendon complex in relaxed and tensioned positions. Scand J Med Sci Sports 9: 57 – 61.
69. Reddi AH. 1994. Bone and Cartilage Differentiation. CUIT Opin Genet Dev 4: 737 – 744.
70. Reddi AH. 1997. Bone morphogenetic proteins: an uncon-ventional approach to isolation of first mammalian mor-phogens. Cytokine Growth Factor Rev 8: 11 – 20.
71. Reddi AH, Wientroub S, Muthukumaran N. 1987. Biologic principles of bone induction. Orthop Clin North Am 18: 207 – 212.
72. Reddy GK, Stehno-Bittel L, Enwemeka CS. 1999. Matrix remodeling in healing rabbit Achilles tendon. Wound Repair Regen 7: 518 – 527.
73. Rooney P, Grant ME, McClure J. 1992. Endochondral ossifi-cation and de novo collagen synthesis during repair of the rat Achilles tendon. Matrix 12: 274 – 281.
74. Saleh M, Marshall PD, Senior R, MacFarlane A. 1992. The Sheffield splint for controlled early mobilisation after rupture of the calcaneal tendon. A prospective, ran-domised comparison with plaster treatment. J Bone Joint Surg [Br] 74: 206 – 209.
75. Sampath TK, Reddi AH. 1983. Homology of bone-inductive proteins from human, monkey, bovine, and rat extracellu-lar matrix. Proc Natl Acad Sci U S A 80: 6591 – 6595.
76. Sejberg D, Hansen LB, Dalsgaard S. 1991. Achilles tendon ruptures operated on under local anesthesia. Retrospec-tive study of 81 nonhospitalized patients. Acta Orthop Scand 61: 549 – 550.
77. Solursh M, Langille MR, Wood J, Sampath TK. 1996. Osteogenic protein-1 is required for mammalian eye development. Biochem Biophys Res Commun 218: 438 – 443.
78. Solveborn SA, Moberg A. 1994. Immediate free ankle motion after surgical repair of acute Achilles tendon rup-tures. Am J Sports Med 22: 607 – 610.
79. Spiro RC, Liu L-S, Heidaran A, Thompson AY, Ng CK, Pohl J, Poser JW. 2000. Inductive activity of recombinant human growth and differentiation factor-5. Biochem Soc Trans 28: 362 – 368.
80. Stein V, Laprell H, Tinnemeyer S, Petersen W. 2000. Quan-titative assessment of intravascular volume of the human Achilles tendon. Acta Orthop Scand 71: 60 – 63.
81. Storm EE, Huynh TV, Copeland NG, Jenkins NA, Kingsley DM, Lee SJ. 1994. Limb alterations in brachypodism mice due to mutations in a new member of TGF beta superfamily. Nature 14: 639 – 643.
82. Storm EE, Kingsley DM. 1996. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122: 3969 – 3979.
83. Sullo A, Maffulli N, Capasso G, Testa V. 2001. The effect of prolonged peritendinous administration of PGE 1 to the rat Achilles tendon: a possible animal model of chronic Achilles tendinopathy. J Orthop Sci 6: 349 – 357.
84. Thomas JT, Kilpatrick MW, Lin K, Erlacher L, Lembes-sis P, Costa T, Tsipoura P, Luyten FP. 1997. Disruption of human limb morphogenesis by a dominant megative mutation in CDMP1. Nat Genet 17: 58 – 64.
85. Thompson. 1962. A Test for rupture of the tendon Achilles. Acta Orthop Scand 32: 461
86. Tipton CM, Vailas AC, Matthes RD. 1986. Experimental studies on the influences of physical activity on liga-ments, tendons and joints: a brief review. Acta Med Scand Suppl 711: 157 – 168.
87. Tsumaki N, Tanaka K, Arikawa-Hirasawa E, Nakase T, Kimura T, Thomas JT, Ochi T, Luyten FP, Yamada Y. 1999. Role of CDMP-1 in skeletal morphogenesis: pro-motion of mesenchymal cell recruitment and chondrocyte differentiation. J of Cell Biology 144: 161 – 173.
88. Urist MRI. 1965. Bone: formation by autoinduction. Science 150: 893 – 899.
89. Waggett A, D., Kwan APL, Woodnut DJ, Rufai A, Ralphs JR, Benjamin M. 1996. Collagens in fibrocartilages at the Achilles tendon insertion - a biochemical, molecu-lar biolgical and immunohistochemical study. In: Trans Orthop Res Soc
90. Wang J-S, Aspenberg P. 1993. Basic Fibroblast growth factor and bone induction in rats. Acta Orthop Scand 64: 557 – 561.
91. Webb JM, Bannister GC. 1999. Percutaneous repair of the ruptured tendo Achillis. J Bone Joint Surg [Br] 81: 877 – 880.
92. White NB, Ter-Pogossian MM, Stein AH. 1964. A method to determine blood glow in long bone and selected soft tis-sues. Surgery, gynecology and obstetrics 119: 535 – 540.
93. Viidik A, Danielson CC, Oxlund H. 1982. On fundamental and phenomenological models, structure and mechanical properties of collagen, elastin and glycosaminoglycan complexes. Biorheology 19: 437 – 451.
94. Vogel KG. 1995. Fibrocartilage in tendon: A response to compressive load. In: Repetitive motion disorders of the upper extremity. Rosemont: Am Acad Orthop Surg.
95. Wolfman NM, Hattersley G, Cox K, Celeste AJ, Nelson R, Yamaji N, Dube JL, DiBlasio- Smith E, Nove J, Song JJ, Wozney JM, Rosen V. 1997. Ectopic Induction of Tendon and Ligament in Rats by Growth and Differentiation Fac-tors 5, 6, and 7, Members of the TGF-13 Gene Family. J Clin Invest 100: 321 – 330.
96. Woo SL, Gelberman RH, Cobb NG, Amiel D, Lothringer K, Akeson WH. 1981. The importance of controlled passive mobilization on flexor tendon healing. A biomechanical study. Acta Orthop Scand 52: 615 – 622.
97. Woo SL, Ritter MA, Amiel D, Sanders TM, Gomez MA, Kuei SC, Garfin SR, Akeson WH. 1980. The biomechani-cal and biochemical properties of swine tendons - long term effects of exercise on the digital extensors. Connect Tissue Res. 7: 177 – 183.
98. Woo SL, Smith D, W., Hildebrand K, A., Zeminski J, A., Johnson L, A. 1998. Engineering the healing of the rabbit medial collateral ligament. Med Biol Eng Comput 36: 359 – 364.
99. Wozney JM. 1998. The bone morphogenetic protein family: multifunctional cellular regulators in the embryo and adult. Eur J Oral Sci. 106 Suppl 1: 160 – 166.
100. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. 1988. Novel regu-lators of bone formation: molecular clones and activities. Science 16; 242: 1528 – 1534.
101. Wredmark T, Carlstedt CA. 1992. Tendon elongation and muscle function after repair of Achilles tednon rupture. Scand J Med Sci Sports 2: 139 – 42.
102. Wren TA, Beaupré GS, Carter DR. 2000. Tendon and liga-ment adaptation to exercise, immobilization and remobi-lization. J Rehabil Res Dev 37: 217 – 224.