The vasculature and its role in the damaged and healing tendon

Springer Science and Business Media LLC - Tập 4 - Trang 1-9 - 2002
Steven A Fenwick1, Brian L Hazleman2, Graham P Riley2
1AstraZeneca, Macclesfield, UK
2Rheumatology Research Unit, Addenbrookes Hospital, Cambridge, UK

Tóm tắt

Tendon pathology has many manifestations, from spontaneous rupture to chronic tendinitis or tendinosis; the etiology and pathology of each are very different, and poorly understood. Tendon is a comparatively poorly vascularised tissue that relies heavily upon synovial fluid diffusion to provide nutrition. During tendon injury, as with damage to any tissue, there is a requirement for cell infiltration from the blood system to provide the necessary reparative factors for tissue healing. We describe in this review the response of the vasculature to tendon damage in a number of forms, and how and when the revascularisation or neovascularisation process occurs. We also include a section on the revascularisation of tendon during its use as a tendon graft in both ligament reconstruction and tendon–tendon grafting.

Tài liệu tham khảo

Manske PR, Lesker PA: Biochemical evidence of flexor tendon participation in the repair process – an in vitro study. J Hand Surg. 1984, 9B: 117-120. Gelberman RH, Manske PR, Van de Berg JS, Lesker PA, Akeson WH: Flexor tendon repair. in-vitro:. 1984, a comparitive histologic study of the rabbit, chicken, dog and monkey: 39-48. Potenza AD: Tendon healing within the flexor digital sheath in the dog. J Bone Joint Surg. 1962, 44A: 49-64. Gelberman RH, Manske PR, Akeson WH, Woo SL, Lundborg G, Amiel D: Flexor tendon repair. J Orthop Res. 1986, 4: 119-128. Li BH, Hong GX, Zu TB: A histological observation on the flexor tendon healing within intact sheath. J Tongji Med Univ. 1991, 11: 169-173. Matthews JP: Vascular changes in flexor tendons after injury and repair: an experimental study. Injury. 1977, 8: 227-233. Kain CC, Russell JE, Burri R, Dunlap J, McCarthy J, Manske PR: The effect of vascularization on avian flexor tendon repair. A biochemical study. Clin Orthop. 1988, 233: 295-303. Mass DP, Tuel R: Human flexor tendon participation in the in vitro repair process. J Hand Surg Am. 1989, 14: 64-71. Packer DL, Dombi GW, Yu PY, Zidel P, Sullivan WG: An in vitro model of fibroblast activity and adhesion formation during flexor tendon healing. J Hand Surg Am. 1994, 19: 769-776. Gelberman RH, Amifl D, Gonsalves M, Woo S, Akeson WH: The influence of protected passive mobilization on the healing of flexor tendons: a biochemical and microangiographic study. Hand. 1981, 13: 120-128. Gelberman RH, Vande-Berg JS, Lundborg GN, Akeson WH: Flexor tendon healing and restoration of the gliding surface. An ultrastructural study in dogs. J Bone Joint Surg Am. 1983, 65: 70-80. Riley GP, Harrall RL, Cawston TE, Hazleman BL, Mackie EJ: Tenascin-C and human tendon degeneration. Am J Pathol. 1996, 149: 933-943. Riley GP, Harrall RL, Constant CR, Chard MD, Cawston TE, Hazleman BL: Glycosaminoglycans of human rotator cuff tendons: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis. 1994, 53: 367-376. Jarvinen M, Jozsa L, Kannus P, Jarvinen TL, Kvist M, Leadbetter W: Histopathological findings in chronic tendon disorders. Scand J Med Sci Sports. 1997, 7: 86-95. Josza L, Reffy A, Kannus P, Demel S, Elek E: Pathological alterations in human tendons. Arch Orthop Trauma Surg. 1990, 110: 15-21. Jozsa L, Kannus P: Histopathological findings in spontaneous tendon ruptures. Scand J Med Sci Sports. 1997, 7: 113-118. Kannus P, Jozsa L: Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg Am. 1991, 73: 1507-1525. Frey C, Shereff M, Greenidge N: Vascularity of the posterior tibial tendon. J Bone Joint Surg Am. 1990, 72: 884-888. Rathbun JB, Macnab I: The microvascular pattern of the rotator cuff. J Bone Joint Surg Br. 1970, 52: 540-553. Peacock EE: A study of the circulation in normal tendons and healing grafts. Ann Surg. 1959, 149: 415-428. Yu JS, Popp JE, Kaeding CC, Lucas J: Correlation of MR imaging and pathologic findings in athletes undergoing surgery for chronic patellar tendinitis. Am J Roentgenol. 1995, 165: 115-118. Astrom M, Rausing A: A survey of surgical and histopathologic findings. Clin Orthop. 1995, 316: 151-164. Kvist M, Jozsa L, Jarvinen MJ, Kvist H: Chronic Achilles paratenonitis in athletes: a histological and histochemical study. Pathology. 1987, 19: 1-11. Takasugi H, Akahori O, Nishihara K, Tada K: Three-dimensional architecture of blood vessels of tendons demonstrated by corrosion casts. Hand. 1978, 10: 9-15. Schmidt-Rohlfing B, Graf J, Schneider U, Niethard FU: The blood supply of the Achilles tendon. Int Orthop. 1992, 16: 29-31. Ahmed IM, Lagopoulos M, McConnell P, Soames RW, Sefton GK: Blood supply of the Achilles tendon. J Orthop Res. 1998, 16: 591-596. Gelberman RH: Flexor tendon physiology: tendon nutrition and cellular activity in injury and repair. Instr Course Lect. 1985, 34: 351-360. Ochiai N, Matsui T, Miyaji N, Merklin RJ, Hunter JM: Vascular anatomy of flexor tendons. I. Vincular system and blood supply of the profundus tendon in the digital sheath. J Hand Surg Am. 1979, 4: 321-330. Zhang ZZ, Zhong SZ, Sun B, Ho GT: Blood supply of the flexor digital tendon in the hand and its clinical significance. Surg Radiol Anat. 1990, 12: 113-117. Chansky HA, Iannotti JP: The vascularity of the rotator cuff. Clin Sports Med. 1991, 10: 807-822. Schatzker J, Branemark PI: Intravital observations on the microvascular anatomy and microcirculation of the tendon. Acta Orthop Scand. 1969, 126 (suppl): 1-23. Brockis JG: The blood supply of the flexor and the extensor tendons of the fingers in man. J Bone Joint Surg Br. 1953, 35B: 131-138. Chaplin DM: The vascular anatomy within normal tendons, divided tendons, free tendon grafts and pedicle tendon grafts in rabbits. A microradioangiographic study. J Bone Joint Surg Br. 1973, 55: 369-389. Ling SC, Chen CF, Wan RX: A study on the vascular supply of the supraspinatus tendon. Surg Radiol Anat. 1990, 12: 161-165. Stein V, Laprell H, Tinnemeyer S, Petersen W: Quantitative assessment of intravascular volume of the human Achilles tendon. Acta Orthop Scand. 2000, 71: 60-63. 10.1080/00016470052943919. Clancy-WG Jr, Narechania RG, Rosenberg TD, Gmeiner JG, Wis-nefske DD, Lange TA: Anterior and posterior cruciate ligament reconstruction in rhesus monkeys. J Bone Joint Surg Am. 1981, 63: 1270-1284. Brewer BJ: Aging of the rotator cuff. Am J Sports Med. 1979, 7: 102-110. Codman EA, Akerson IB: The pathology associated with rupture of the supraspinatus tendon. Ann Surg. 1931, 93: 348-359. McFarland EG, Morrey BF, An KN, Wood MB: The relationship of vascularity and water content to tensile strength in a patellar tendon replacement of the anterior cruciate in dogs. Am J Sports Med. 1986, 14: 436-448. Marumoto JM, Mitsunaga MM, Richardson AB, Medoff RJ, Mayfield GW: Late patellar tendon ruptures after removal of the central third for anterior cruciate ligament reconstruction. A report of two cases. Am J Sports Med. 1996, 24: 698-701. Zanotti RM, Freiberg AA, Matthews LS: Use of patellar allograft to reconstruct a patellar tendon-deficient knee after total joint arthroplasty. J Arthroplasty. 1995, 10: 271-274. Kasperczyk WJ, Bosch U, Oestern HJ, Tscherne H: Staging of patellar tendon autograft healing after posterior cruciate ligament reconstruction. A biomechanical and histological study in a sheep model. Clin Orthop. 1993, 286: 271-282. Bosch U, Kasperczyk WJ: Healing of the patellar tendon autograft after posterior cruciate ligament reconstruction – a process of ligamentization? An experimental study in a sheep model. Am J Sports Med. 1992, 20: 558-566. Noyes FR, Butler DL, Paulos LE, Grood ES: Intra-articular cruciate reconstruction. I: Perspectives on graft strength, vascularization, and immediate motion after replacement. Clin Orthop. 1983, 172: 71-77. Paulos LE, Butler DL, Noyes FR, Grood ES: Intra-articular cruciate reconstruction. II: Replacement with vascularized patellar tendon. Clin Orthop. 1983, 172: 78-84. Noyes FR, Butler DL, Grood ES, Zernicke RF, Hefzy MS: Biomechanical analysis of human ligament grafts used in knee-ligament repairs and reconstructions. J Bone Joint Surg Am. 1984, 66: 344-352. Alm A: Survival of part of patellar tendon transposed for reconstruction of anterior cruciate ligament. Acta Chir Scand. 1973, 139: 443-447. Amiel D, Kleiner JB, Akeson WH: The natural history of the anterior cruciate ligament autograft of patellar tendon origin. Am J Sports Med. 1986, 14: 449-462. Arnoczky SP, Tarvin GB, Marshall JL: Anterior cruciate ligament replacement using patellar tendon. An evaluation of graft revascularization in the dog. J Bone Joint Surg Am. 1982, 64: 217-224. Nikolaou PK, Seaber AV, Glisson RR, Ribbeck BM, Bassett FH: Anterior cruciate ligament allograft transplantation. Long-term function, histology, revascularization, and operative technique. Am J Sports Med. 1986, 14: 348-360. Rougraff B, Shelbourne KD, Gerth PK, Warner J: Arthroscopic and histologic analysis of human patellar tendon autografts used for anterior cruciate ligament reconstruction. Am J Sports Med. 1993, 21: 277-284. Alm A, Stromberg B: Transposed medial third of patellar ligament in reconstruction of the anterior cruciate ligament. A surgical and morphologic study in dogs. Acta Chir Scand. 1974, 445 (suppl): 37-49. Ginsburg JH, Whiteside LA, Piper TL: Nutrient pathways in transferred patellar tendon used for anterior cruciate ligament reconstruction. Am J Sports Med. 1980, 8: 15-18. Whiston TB, Walmsley R: Some observations of bone and tendon after tunnelling of bone and insertion of tendon. J Bone Joint Surg Am. 1960, 42A: 377-386. Liu TK, Yang RS: Flexor tendon graft for late management of isolated rupture of the profundus tendon. J Trauma. 1997, 43: 103-106. Wehbe MA, Mawr B, Hunter JM, Schneider LH, Goodwyn BL: Two-stage flexor-tendon reconstruction. Ten-year experience. J Bone Joint Surg Am. 1986, 68: 752-763. McClinton MA, Curtis RM, Wilgis EF: One hundred tendon grafts for isolated flexor digitorum profundus injuries. J Hand Surg Am. 1982, 7: 224-229. Seiler JG, Gelberman RH, Williams CS, Woo SL, Dickersin GR, Sofranko R, Chu CR, Rosenberg AE: Autogenous flexor-tendon grafts. A biomechanical and morphological study in dogs. J Bone Joint Surg Am. 1993, 75: 1004-1014. Gelberman RH, Chu CR, Williams CS, Seiler JG, Amiel D: Angiogenesis in healing autogenous flexor-tendon grafts. J Bone Joint Surg Am. 1992, 74: 1207-1216. Singer DI, Morrison WA, Gumley GJ, O'Brien BM, Mitchell GM, Barton RM, Frykman GK: Comparative study of vascularized and nonvascularized tendon grafts for reconstruction of flexor tendons in zone 2: an experimental study in primates. J Hand Surg Am. 1989, 14: 55-63. Eiken O, Lundborg G: Experimental tendon grafting within intact tendon sheath. Scand J Plast Reconstr Surg. 1983, 17: 127-131. Kakar S, Khan U, McGrouther DA: Differential cellular response within the rabbit tendon unit following tendon injury. J Hand Surg Br. 1998, 23: 627-632. 10.1016/S0266-7681(98)80017-X. Richards HJ: Repair and healing of the divided digital flexor tendon. Injury. 1980, 12: 1-12. Bank RA, TeKoppele JM, Oostingh G, Hazleman BL, Riley GP: Lysylhydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen: changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis. 1999, 58: 35-41. Riley GP, Harrall RL, Constant CR, Chard MD, Cawston TE, Hazleman BL: Tendon degeneration and chronic shoulder pain: changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis. Ann Rheum Dis. 1994, 53: 359-366. Lagergren C, Lindholm A: Vascular distribution in the Achilles tendons: an angiographic and micro-angiographic study. Acta Chir Scand. 1959, 116 (suppl): 491-495. Macnab I: Rotator cuff tendinitis. Ann R Coll Surg Engl. 1973, 53: 271-287. Cofield RH: Rotator cuff disease of the shoulder. J Bone Joint Surg Am. 1985, 67: 974-979. Backman C, Boquist L, Friden J, Lorentzon R, Toolanen G: Chronic achilles paratenonitis with tendinosis: an experimental model in the rabbit. J Orthop Res. 1990, 8: 541-547. Backman C, Friden J, Widmark A: Blood flow in chronic Achilles tendinosis. Radioactive microsphere study in rabbits. Acta Orthop Scand. 1991, 62: 386-387. Khan KM, Bonar F, Desmond PM, Cook JL, Young DA, Visentini PJ, Fehrmann MW, Kiss ZS, O'Brien PA, Harcourt PR, Dowling RJ, O'Sullivan RM, Crichton KJ, Tress BM, Wark JD: Patellar tendinosis (jumper's knee): findings at histopathologic examination, US, and MR imaging. Victorian Institute of Sport Tendon Study Group. Radiology. 1996, 200: 821-827. Kannus P, Natri A: Etiology and pathophysiology of tendon ruptures in sports. Scand J Med Sci Sports. 1997, 7: 107-112. Davidsson L, Salo M: Pathogenesis of subcutaneous tendon ruptures. Acta Chir Scand. 1969, 135: 209-212. Fox JM, Blazina ME, Jobe FW, Kerlan RK, Carter VS, Shields-CL J, Carlson GJ: Degeneration and rupture of the Achilles tendon. Clin Orthop. 1975, 107: 221-224. Gibson W: Are 'spontaneous' Achilles tendon ruptures truly spontaneous? [letter]. Br J Sports Med. 1998, 32: 266- Williams JG: Achilles tendon lesions in sport. Sports Med. 1986, 3: 114-135. Barfred T: Achilles tendon rupture. Aetiology and pathogenesis of subcutaneous rupture assessed on the basis of the literature and rupture experiments on rats. Acta Orthop Scand. 1973, 152 (suppl): 3-126. Barfred T: Histology of the rat Achilles tendon before and after tendon rupture. Acta Pathol Microbiol Scand A. 1971, 79: 287-292. Kalebo P, Goksor LA, Sward L, Peterson L: Soft-tissue radiography, computed tomography, and ultrasonography of partial Achilles tendon ruptures. Acta Radiol. 1990, 31: 565-570. Arner O, Lindholm A: Subcutaneous rupture of the Achilles tendon: a study of 92 cases. Acta Chir Scand. 1959, 239 (suppl): 1-51. Bidder M, Towler DA, Gelberman RH, Boyer MI: Expression of mRNA for vascular endothelial growth factor at the repair site of healing canine flexor tendon. J Orthop Res. 2000, 18: 247-252. Kuroda R, Kurosaka M, Yoshiya S, Mizuno K: Localization of growth factors in the reconstructed anterior cruciate ligament: immunohistological study in dogs. Knee Surg Sports Traumatol Arthrosc. 2000, 8: 120-126. 10.1007/s001670050198. Chang J, Most D, Stelnicki E, Siebert JW, Longaker MT, Hui K, Lineaweaver WC: Gene expression of transforming growth factor beta-1 in rabbit zone II flexor tendon wound healing: evidence for dual mechanisms of repair. Plast Reconstr Surg. 1997, 100: 937-944. 10.1097/00006534-199709001-00016. Chang J, Most D, Thunder R, Mehrara B, Longaker MT, Lin-eaweaver WC: Molecular studies in flexor tendon wound healing: the role of basic fibroblast growth factor gene expression. J Hand Surg Am. 1998, 23: 1052-1058. Duffy-FJ Jr, Seiler JG, Gelberman RH, Hergrueter CA: Growth factors and canine flexor tendon healing: initial studies in uninjured and repair models. J Hand Surg Am. 1995, 20: 645-649. Kuroda R, Kurosaka M, Yoshiya S, Mizuno K: Localization of growth factors in the reconstructed anterior cruciate ligament: immunohistological study in dogs. Knee Surg Sports Traumatol Arthrosc. 2000, 8: 120-126. 10.1007/s001670050198. Harwood L, Goomer RS, Gelberman RH, Silva MJ, Amiel D: Regulation of αvβ5 and α5β1 integrin receptors by basic fibro-blast growth factor and platelet-derived growth factor-BB in intrasynovial flexor tendon cells. Wound Repair Regen. 1999, 7: 381-388. 10.1046/j.1524-475X.1999.00381.x. Lee J, Harwood FL, Akeson WH, Amiel D: Growth factor expression in healing rabbit medial collateral and anterior cruciate ligaments. Iowa Orthop J. 1998, 18: 19-25. Panossian V, Liu SH, Lane JM, Finerman GA: Fibroblast growth factor and epidermal growth factor receptors in ligament healing. Clin Orthop. 1997, 342: 173-180. 10.1097/00003086-199709000-00025. Brown MF, Hukkanen MV, McCarthy ID, Redfern DR, Batten JJ, Crock HV, Hughes SP, Polak JM: Sensory and sympathetic innervation of the vertebral endplate in patients with degenerative disc disease. J Bone Joint Surg Br. 1997, 79: 147-153. 10.1302/0301-620X.79B1.6814. Birch HL, Rutter GA, Goodship AE: Oxidative energy metabolism in equine tendon cells. Res Vet Sci. 1997, 62: 93-97. Stone KR, Bowman HF, Boland A, Steadman JR: Ligament and tendon oxygenation measurements using polargraphic oxygen sensors. Arthroscopy. 1987, 3: 187-195. Shweiki D, Itin A, Soffer D, Keshet E: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 1992, 359: 843-845. 10.1038/359843a0. Kastelic J, Galeski A, Baer E: The multicomposite structure of tendon. Connect Tissue Res. 1978, 6: 11-23. Agur AMR, Lee MJ: The Upper Limb. In Grant's Atlas of Anatomy. 1999, Philadelphia: Lippincott Williams & Wilkins;, 414-517. 10th