Tendon tissue engineering: Progress, challenges, and translation to the clinic

Journal of Musculoskeletal Neuronal Interactions

Volumn 11, Issue 2, 2011, Pages 163-173

  Shearn, J T ^a   Kinneberg, K R C ^a   Dyment, N A ^a   Galloway, M T ^b   Kenter, K ^c   Wylie, C ^d   Butler, D L ^a  

^a University of Cincinnati   (United States)

^b Cincinnati Sportsmedicine and Orthopaedic Center   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Commercialization; Tendon injury; Tendon tissue engineering; Translation

Indexed keywords

BONE MORPHOGENETIC PROTEIN 12; COLLAGENASE 3; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR 8; GROWTH DIFFERENTIATION FACTOR; GROWTH DIFFERENTIATION FACTOR 5; GROWTH DIFFERENTIATION FACTOR 6; INTERLEUKIN 1BETA; INTERSTITIAL COLLAGENASE; PROSTAGLANDIN E2; SCLERAXIS; SCLEROPROTEIN; TISSUE SCAFFOLD; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG;

ACHILLES TENDON RUPTURE; DISEASE MODEL; FLEXOR TENDON; HUMAN; MECHANICAL STRESS; MUSCLE DEVELOPMENT; NONHUMAN; PATELLA TENDON; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; ROTATOR CUFF RUPTURE; SIGNAL TRANSDUCTION; TENDINITIS; TENDON GRAFT; TENDON INJURY; TENDON RECONSTRUCTION; TISSUE ENGINEERING; WEIGHT BEARING;

ANIMALS; COMMERCE; DISEASE MODELS, ANIMAL; HUMANS; STRESS, MECHANICAL; TENDINOPATHY; TENDONS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 79958063381     PISSN: 11087161     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (91)

1. Clayton RAE, Court-Brown CM. The epidemiology of musculoskeletal tendinous and ligamentous injuries. Injury 2008;39(12):1338-44.
2. Leppilahti J, Puranen J, Orava S. Incidence of Achilles tendon rupture. Acta Orthop Scand 1996;67(3):277-9.
3. Zhao C, Moran SL, Cha SS, Kai-Nan-An, Amadio PC. An analysis of factors associated with failure of tendon repair in the canine model. J Hand Surg 2007;32(4):518-25.
4. Harris SB, Harris D, Foster AJ, Elliot D. The aetiology of acute rupture of flexor tendon repairs in zones 1 and 2 ofthe fingers during early mobilization. J Hand Surg 1999;24 B(3):275-80.
5. Baktir A, Turk CY, Kabak S, Sahin V, Kardas Y. Flexor tendon repair in zone 2 followed by early active mobilization. J Hand Surg 1996;21 B(5):624-8.
6. Khan RJK, Fick D, Keogh A, Crawford J, Brammar T, Parker M. Treatment of acute achilles tendon ruptures: A meta-analysis of randomized, controlled trials. Journal of Bone and Joint Surgery-Series A 2005;87(10):2202-10.
7. Strauss EJ, Ishak C, Jazrawi L, Sherman O, Rosen J. Operative treatment of acute achilles tendon ruptures: An institutional review of clinical outcomes. Injury 2007; 38(7):832-8.
8. Galatz LM, Ball CM, Teefey SA, Middleton WD, Yamaguchi K. The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. Journal of Bone and Joint Surgery - Series A 2004; 86(2):219-24.
9. Harryman II DT, Mack LA, Wang KY, Jackins SE, Richardson ML, Matsen III FA. Repairs of the rotator cuff. correlation of functional results with integrity of the cuff. Journal of Bone and Joint Surgery-Series A 1991; 73(7):982-9.
10. Lafosse L, Brozska R, Toussaint B, Gobezie R. The outcome and structural integrity of arthroscopic rotator cuff repair with use of the double-row suture anchor technique. Journal of Bone and Joint Surgery-Series A 2007; 89(7):1533-41.
11. Sharma P, Maffulli N. Biology of tendon injury: Healing, modeling and remodeling. Journal of Musculoskeletal Neuronal Interactions 2006;6(2):181-90.
12. Thomopoulos S, Williams GR, Soslowsky LJ. Tendon to bone healing: Differences in biomechanical, structural, and compositional properties due to a range of activity levels. J Biomech Eng 2003;125(1):106-13.
13. Hasslund S, Jacobson JA, Dadali T, Basile P, Ulrich-Vinther M, Søalle K, et al. Adhesions in a murine flexor tendon graft model: Autograft versus allograft reconstruction. Journal of Orthopaedic Research 2008;26(6):824-33.
14. Kryger GS, Chong AKS, Costa M, Pham H, Bates SJ, Chang J. A comparison of tenocytes and mesenchymal stem cells for use in flexor tendon tissue engineering. J Hand Surg 2007;32(5):597-605.
15. Rees JD, Wilson AM, Wolman RL. Current concepts in the management of tendon disorders. Rheumatology (UK) 2006;45(5):508-21.
16. Greca FH, Ramos EJB, Dallolmo VC, Silva APG, Mima WH, Okawa L, et al. Evaluation of porcine small intestinal submucosa in achilles tendon repair. Journal of Applied Research 2005;5(1):115-23.
17. Fredberg U, Stengaard-Pedersen K. Chronic tendinopathy tissue pathology, pain mechanisms, and etiology with a special focus on inflammation: Review. Scandinavian Journal of Medicine and Science in Sports 2008;18(1):3-15.
18. Juncosa-Melvin N, Boivin GP, Galloway MT, Gooch C, West JR, Butler DL. Effects of cell-to-collagen ratio in stem cell-seeded constructs for achilles tendon repair. Tissue Eng 2006;12(4):681-9.
19. West JR, Juncosa N, Galloway MT, Boivin GP, Butler DL. Characterization of in vivo achilles tendon forces in rabbits during treadmill locomotion at varying speeds and inclinations. J Biomech 2004;37(11):1647-53.
20. Ouyang HW, Goh JCH, Thambyah A, Teoh SH, Lee EH. Knitted poly-lactide-co-glycolide scaffold loaded with bone marrow stromal cells in repair and regeneration of rabbit achilles tendon. Tissue Eng 2003;9(3):431-9.
21. Sato M, Maeda M, Kurosawa H, Inoue Y, Yamauchi Y, Iwase H. Reconstruction of rabbit achilles tendon with three bioabsorbable materials: Histological and biomechanical studies. Journal of Orthopaedic Science 2000; 5(3):256-67.
22. Gilbert TW, Stewart-Akers AM, Simmons-Byrd A, Badylak SF. Degradation and remodeling of small intestinal submucosa in canine achilles tendon repair. Journal of Bone and Joint Surgery - Series A 2007;89(3):621-30.
23. Badylak SF, Tullius R, Kokini K, Shelbourne KD, Klootwyk T, Voytik SL, et al. The use of xenogeneic small intestinal submucosa as a biomaterial for achille's tendon repair in a dog model. J Biomed Mater Res 1995; 29(8):977-85.
24. Derwin KA, Baker AR, Spragg RK, Leigh DR, Iannotti JP. Commercial extracellular matrix scaffolds for rotator cuff tendon repair: Biomechanical, biochemical, and cellular properties. Journal of Bone and Joint Surgery - Series A 2006;88(12):2665-72.
25. Barber FA, Herbert MA, Boothby MH. Ultimate tensile failure loads of a human dermal allograft rotator cuff augmentation. Arthroscopy - Journal of Arthroscopic and Related Surgery 2008;24(1):20-4.
26. Wong I, Burns J, Snyder S. Arthroscopic GraftJacket repair of rotator cuff tears. Journal of Shoulder and Elbow Surgery 2010;19(2Suppl.):104-9.
27. Snyder SJ, Arnoczky SP, Bond JL, Dopirak R. Histologic evaluation of a biopsy specimen obtained 3 months after rotator cuff augmentation with GraftJacket matrix. Arthroscopy - Journal of Arthroscopic and Related Surgery 2009;25(3):329-33.
28. Nicholson GP, Breur GJ, Van Sickle D, Yao JQ, Kim J, Blanchard CR. Evaluation of a cross-linked acellular porcine dermal patch for rotator cuff repair augmentation in an ovine model. Journal of Shoulder and Elbow Surgery 2007;16(5Suppl.):S184-90.
29. Thomopoulos S, Soslowsky LJ, Flanagan CL, Tun S, Keefer CC, Mastaw J, et al. The effect of fibrin clot on healing rat supraspinatus tendon defects. Journal of Shoulder and Elbow Surgery 2002;11(3):239-47.
30. Rodeo SA, Potter HG, Kawamura S, Turner AS, Hyon JK, Atkinson BL. Biologic augmentation of rotator cuff tendon-healing with use of a mixture of osteoinductive growth factors. Journal of Bone and Joint Surgery-Series A 2007;89(11):2485-97.
31. Kovacevic D, Rodeo SA. Biological augmentation of rotator cuff tendon repair. Clin Orthop 2008;466(3):622-33.
32. Seeherman HJ, Archambault JM, Rodeo SA, Turner AS, Zekas L, D'Augusta D, et al. rhBMP-12 accelerates healing of rotator cuff repairs in a sheep model. Journal of Bone and Joint Surgery - Series A 2008;90(10):2206-19.
33. Gulotta LV, Rodeo SA. Growth factors for rotator cuff repair. Clin Sports Med 2009;28(1):13-23.
34. Butler DL, Gooch C, Kinneberg KR, Boivin GP, Galloway MT, Nirmalanandhan VS, et al. The use of mesenchymal stem cells in collagen-based scaffolds for tissue-engineered repair of tendons. Nature protocols 2010;5(5): 849-63.
35. Awad HA, Boivin GP, Dressler MR, Smith FNL, Young RG, Butler DL. Repair of patellar tendon injuries using a cell-collagen composite. Journal of Orthopaedic Research 2003;21(3): 420-31.
36. Awad HA, Butler DL, Boivin GP, Smith FNL, Malaviya P, Huibregtse B, et al. Autologous mesenchymal stem cellmediated repair of tendon. Tissue Eng 1999;5(3): 267-77.
37. Harris MT, Butler DL, Boivin GP, Florer JB, Schantz EJ, Wenstrup RJ. Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs. Journal of Orthopaedic Research 2004;22(5): 998-1003.
38. Juncosa-Melvin N, Matlin KS, Holdcraft RW, Nirmalanandhan VS, Butler DL. Mechanical stimulation increases collagen type I and collagen type III gene expression of stem cell-collagen sponge constructs for patellar tendon repair. Tissue Eng 2007;13(6): 1219-26.
39. Juncosa-Melvin N, Shearn JT, Boivin GP, Gooch C, Galloway MT, West JR, et al. Effects of mechanical stimulation on the biomechanics and histology of stem cell-collagen sponge constructs for rabbit patellar tendon repair. Tissue Eng 2006;12(8): 2291-300.
40. Juncosa-Melvin N, Boivin GP, Gooch C, Galloway MT, West JR, Dunn MG, et al. The effect of autologous mesenchymal stem cells on the biomechanics and histology of gel-collagen sponge constructs used for rabbit patellar tendon repair. Tissue Eng 2006;12(2): 369-79.
41. Shearn JT, Juncosa-Melvin N, Boivin GP, Galloway MT, Goodwin W, Gooch C, et al. Mechanical stimulation of tendon tissue engineered constructs: Effects on construct stiffness, repair biomechanics, and their correlation. J Biomech Eng 2007;129(6): 848-54.
42. Nirmalanandhan VS, Juncosa-Melvin N, Shearn JT, Boivin GP, Galloway MT, Gooch C, et al. Combined effects of scaffold stiffening and mechanical preconditioning cycles on construct biomechanics, gene expression, and tendon repair biomechanics. Tissue Engineering - Part A 2009;15(8): 2103-11.
43. Juncosa-Melvin N, Boivin GP, Galloway MT, Gooch C, West JR, Sklenka AM, et al. Effects of cell-to-collagen ratio in mesenchymal stem cell-seeded implants on tendon repair biomechanics and histology. Tissue Eng 2005; 11(3-4): 448-57.
44. Juncosa N, West JR, Galloway MT, Boivin GP, Butler DL. In vivo forces used to develop design parameters for tissue engineered implants for rabbit patellar tendon repair. J Biomech 2003;36(4): 483-8.
45. Guilak F, Butler DL, Goldstein SA, Mooney D. Functional Tissue Engineering, 2003.
46. Butler DL, Goldstein SA, Guilak F. Functional tissue engineering: The role of biomechanics. J Biomech Eng 2000;122(6): 570-5.
47. Butler DL, Shearn JT, Juncosa N, Dressler MR, Hunter SA. Functional tissue engineering parameters toward designing repair and replacement strategies. Clin Orthop 2004;(427Suppl.):S 190-9.
48. Korvick DL, Cummings JF, Grood ES, Holden JP, Feder SM, Butler DL. The use of an implantable force transducer to measure patellar tendon forces in goats. J Biomech 1996;29(4): 557-61.
49. Hankemeier S, Hurschler C, Zeichen J, Van Griensven M, Miller B, Meller R, et al. Bone marrow stromal cells in a liquid fibrin matrix improve the healing process of patellar tendon window defects. Tissue Engineering - Part A 2009;15(5): 1019-30.
50. Karaoglu S, Fisher MB, Woo SL-, Fu Y-, Liang R, Abramowitch SD. Use of a bioscaffold to improve healing of a patellar tendon defect after graft harvest for ACL reconstruction: A study in rabbits. Journal of Orthopaedic Research 2008;26(2): 255-63.
51. Lyras DN, Kazakos K, Verettas D, Botaitis S, Agrogiannis G, Kokka A, et al. The effect of platelet-rich plasma gel in the early phase of patellar tendon healing. Arch Orthop Trauma Surg 2009;129(11): 1577-82.
52. Cserjesi P, Brown D, Ligon K, Lyons G, Copeland N, Gilbert D, et al. Scleraxis: A basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development. 1995 01/01;121(4): 1099-110.
53. Schweitzer R, Zelzer E, Volk T. Connecting muscles to tendons: Tendons and musculoskeletal development in flies and vertebrates. Development 2010 09/01;137(17): 2807-17.
54. Asou Y, Nifuji A, Tsuji K, Shinomiya K, Olson E, Koopman P, et al. Coordinated expression of scleraxis and Sox9 genes during embryonic development of tendons and cartilage. J Orthop Res 2002 01/01;20(4): 827-33.
55. Murchison N, Price B, Conner D, Keene D, Olson E, Tabin C, et al. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 2007 01/01; 134(14): 2697-708.
56. Brent A, Tabin C. FGF acts directly on the somitic tendon progenitors through the ets transcription factors Pea3 and erm to regulate scleraxis expression. Development 2004 01/01; 131(16): 3885-96.
57. Kuo C, Petersen B, Tuan R. Spatiotemporal protein distribution of TGF-betas, their receptors, and extracellular matrix molecules during embryonic tendon development. Dev Dyn 2008 05/01;237(5): 1477-89.
58. Mikic B, Bierwert L, Tsou D. Achilles tendon characterization in GDF-7 deficient mice. J Orthop Res 2006 04/01; 24(4): 831-41.
59. Edom-Vovard F, Schuler B, Bonnin M, Teillet M, Duprez D. Fgf4 positively regulates scleraxis and tenascin expression in chick limb tendons. Developmental Biology 2002 01/01;247(2): 351-66.
60. Pryce B, Watson S, Murchison N, Staverosky J, Düker N, Schweitzer R. Recruitment and maintenance of tendon progenitors by TGFB signaling are essential for tendon formation. Development 2009 01/01;136(8): 1351-61.
61. Mikic B, Schalet B, Clark R, Gaschen V, Hunziker E. GDF-5 deficiency in mice alters the ultrastructure, mechanical properties and composition of the achilles tendon. J Orthop Res 2001 01/01;19(3): 365-71.
62. Mikic B, Rossmeier K, Bierwert L. Sexual dimorphism in the effect of GDF-6 deficiency on murine tendon. J Orthop Res 2009 12/01;27(12): 1603-11.
63. Maffulli N, Khan KM, Puddu G. Overuse tendon conditions: Time to change a confusing terminology. Arthroscopy 1998;14(8): 840-3.
64. Kannus P, Jósa L. Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. The Journal of bone and joint surgery American volume 1991 12/01;73(10): 1507-25.
65. Riley G. Chronic tendon pathology: Molecular basis and therapeutic implications. Exp Rev Mol Med. 2005 03/24;7(5): 1-25.
66. Sun H, Li Y, Fung D, Majeska R, Schaffler M, Flatow E. Coordinate regulation of IL-1β and MMP-13 in rat tendons following subrupture fatigue damage. Clinical Orthopaedics and Related Research 2008 01/01;466(7): 1555-61.
67. Soslowsky LJ, Thomopoulos S, Tun S, Flanagan CL, Keefer CC, Mastaw J, et al. Overuse activity injures the supraspinatus tendon in an animal model: A histologic and biomechanical study. Journal of Shoulder and Elbow Surgery 2000;9(2): 79-84.
68. Sharma P, Maffulli N. Tendon injury and tendinopathy: Healing and repair. Journal of Bone and Joint Surgery - Series A 2005;87(1): 187-202.
69. Xu Y, Murrell G. The basic science of tendinopathy. Clin Orthop Relat Res 2008 01/01: 1-11.
70. Longo U, Oliva F, Olivia F, Denaro V, Maffulli N. Oxygen species and overuse tendinopathy in athletes. Disability and Rehabilitation 2008 01/01;30(20-22): 1563-71.
71. Arnoczky S, Lavagnino M, Egerbacher M, The mechanobiological aetiopathogenesis of tendinopathy: Is it the over-stimulation or the under-stimulation of tendon cells? International Journal of Experimental Pathology 2007 01/01 217-66.
72. Jelinsky S, Lake S, Archambault J, Soslowsky L. Gene expression in rat supraspinatus tendon recovers from overuse with rest. Clin Orthop Relat Res 2008 07/01; 466(7): 1612-7.
73. Flick J, Devkota A, Tsuzaki M, Almekinders L, Weinhold P. Cyclic loading alters biomechanical properties and secretion of PGE 2 and NO from tendon explants. Clinical Biomechanics 2006;21(1): 99-106.
74. Riley G. Tendinopathy - from basic science to treatment. Nat Clin Pract Rheumatol 2008 02/01;4(2): 82-9.
75. Yang G, Im H, Wang J. Repetitive mechanical stretching modulates IL-1β induced COX-2, MMP-1 expression, and PGE production in human patellar tendon fibroblasts. Gene 2005 12/19;363: 166-72.
76. Archambault J, Tsuzaki M, Herzog W, Banes A. Stretch and interleukin-1beta induce matrix metalloproteinases in rabbit tendon cells in vitro. J Orthop Res 2002 01/01;20(1): 36-9.
77. Cilli F, Khan M, Fu F, Wang J. Prostaglandin E2 affects proliferation and collagen synthesis by human patellar tendon fibroblasts. Clinical Journal of Sport Medicine 2004;14(4):232.
78. Bolon B, Campagnuolo G, Zhu L, Duryea D, Zack D, Feige U. Interleukin-1beta and tumor necrosis factor-alpha produce distinct, time-dependent patterns of acute arthritis in the rat knee. Vet Pathol 2004 05/01;41(3): 235-43.
79. Hashimoto T, Nobuhara K, Hamada T. Pathologic evidence of degeneration as a primary cause of rotator cuff tear. Clinical Orthopaedics and Related Research 2003;(415): 111-20.
80. Lake SP, Ansorge HL, Soslowsky LJ. Animal models of tendinopathy. Disabil Rehabil 2008;30(20-22): 1530-41.
81. Dahlgren LA, Mohammed HO, Nixon AJ. Temporal expression of growth factors and matrix molecules in healing tendon lesions. Journal of Orthopaedic Research 2005;23(1): 84-92.
82. Khan MH, Li Z, Wang JH. Repeated exposure of tendon to prostaglandin-E2 leads to localized tendon degeneration. Clin J Sport Med 2005;15(1): 27-33.
83. Stone D, Green C, Rao U, Aizawa H, Yamaji T, Niyibizi C, et al. Cytokine-induced tendinitis: A preliminary study in rabbits. J Orthop Res 1999 03/01;17(2): 168-77.
84. Tapper JE, Fukushima S, Azuma H, Sutherland C, Marchuk L, Thornton GM, et al. Dynamic in vivo three-dimensional (3D) kinematics of the anterior cruciate ligament/ medial collateral ligament transected ovine stifle joint. Journal of Orthopaedic Research 2008;26(5): 660-72.
85. Murray MM, Magarian E, Zurakowski D, Fleming BC. Bone-to-bone fixation enhances functional healing of the porcine anterior cruciate ligament using a collagenplatelet composite. Arthroscopy - Journal of Arthroscopic and Related Surgery 2010;26(9Suppl. 1):S49,S57+e156.
86. Fan H, Liu H, Toh SL, Goh JCH. Anterior cruciate ligament regeneration using mesenchymal stem cells and silk scaffold in large animal model. Biomaterials 2009; 30(28): 4967-77.
87. Mueller XM, Tevaearai HT, Jegger D, Tucker O, Von Segesser LK. Are standard human coagulation tests suitable in pigs and calves during extracorporeal circulation? Artif Organs 2001;25(7): 579-84.
88. Safran O, Derwin KA, Powell K, Iannotti JP. Changes in rotator cuff muscle volume, fat content, and passive mechanics after chronic detachment in a canine model. Journal of Bone and Joint Surgery - Series A 2005;87(12 I): 2662-70.
89. Ker RF, Alexander RM, Bennett MB. Why are mammalian tendons so thick? J Zool 1988;216: 309-24.
90. Adachi N, Ochi M, Uchio Y, Sakai Y, Kuriwaka M, Fujihara A. Harvesting hamstring tendons for ACL reconstruction influences postoperative hamstring muscle performance. Arch Orthop Trauma Surg 2003;123(9): 460-5.
91. Baer GS, Harner CD. Clinical outcomes of allograft versus autograft in anterior cruciate ligament reconstruction. Clin Sports Med 2007;26(4): 661-81.