Preclinical animal models in single site cartilage defect testing: a systematic review

Osteoarthritis and Cartilage

Volumn 17, Issue 6, 2009, Pages 705-713

  Ahern, B J ^a   Parvizi, J ^b   Boston, R ^a   Schaer, T P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ROTHMAN INSTITUTE   (United States)

Author keywords

Animal model; Cartilage; Literature review; Osteoarthritis; Preclinical

Indexed keywords

BIOMATERIAL;

AGE; CARTILAGE INJURY; CLUSTER ANALYSIS; DISEASE MODEL; DISEASE SEVERITY; DOG; GOAT; HORSE; HUMAN; MATERIALS TESTING; MEDICAL LITERATURE; MEDICAL RESEARCH; METHODOLOGY; MOUSE; NONHUMAN; ORTHOPEDIC SURGERY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RABBIT; REVIEW; SHEEP; SPECIES DIFFERENCE; STANDARDIZATION; SURGICAL TECHNIQUE; SWINE; SYSTEMATIC REVIEW;

ANIMALS; ANIMALS, DOMESTIC; BIOMECHANICS; CARTILAGE, ARTICULAR; CLUSTER ANALYSIS; FRACTURE HEALING; HUMANS; MICE; MODELS, ANIMAL; SPECIES SPECIFICITY;

EID: 67349242012     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2008.11.008     Document Type: Review

References (118)

1. Felson D.T., Lawrence R.C., Dieppe P.A., Hirsch R., Helmick C.G., Jordan J.M., et al. Osteoarthritis new insights. Part I: the disease and it's risk factors. Ann Intern Med (2000) 635-646
2. Saraf A., and Mikos A.G. Gene delivery strategies for cartilage tissue engineering. Adv Drug Deliv Rev 58 (2006) 592-603
3. Hunziker E.B. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 10 (2002) 432-463
4. Cellular Products for Joint Surface Repair - Briefing Document. Cellular, Tissue, and Gene Therapies Advisory Committee, 2005, Meeting 38, March 3-4.
5. Beris A.E., Lykissas M., Papageorgiou C.D., and Georgoulis A.D. Advances in articular cartilage repair. Int J Care Inj 36 (2005) 14-23
6. Brittberg M. Autologous chondrocyte transplantation. Clin Orthop Relat Res (1999) S147-S155
7. Gelse K., and Schneider H. Ex vivo gene therapy approaches to cartilage repair. Adv Drug Deliv Rev 58 (2006) 259-284
8. Wakitani S., Imoto K., Yamamoto T., Saito M., Murata N., and Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritis knees. Osteoarthritis Cartilage 10 (2002) 199-206
9. Hjelle K., Solheim E., Strand T., Muri R., and Brittberg M. Articular cartilage defects in 1,000 knee arthroscopies. Arthroscopy 18 (2002) 730-734
10. Bouwmeester P., Kuijer R., Homminga G.N., Bulstra S.K., and Geesink R. A retrospective analysis of two independent prospective cartilage repair studies: autogenous perichondrial grafting versus subchondral drilling 10 years post-surgery. J Orthop Res 20 (2002) 267-273
11. Hunziker E.B. Biologic repair of articular cartilage. Clin Orthop Relat Res (1999) S135-S146
12. Frisbie D.D., Cross M.W., and McIlwraith C.W. A comparative study of articular cartilage thickness in the stifle of animal species used in human pre-clinical studies compared to articular cartilage thickness in the human knee. Vet Comp Orthop Traumatol 19 (2006) 142-146
13. Everitt B., Landau S., and Leese M. Cluster Analysis. 4th edn. (2001), Arnold Publisher, New York
14. Milligan G.M., and Cooper M.C. An examination of procedures for determining the number of clusters in a data set. Psychometrika 50 (1985) 159-179
15. Calinski R., and Harabasz J. A dendrite method for cluster analysis. Commun Stat 3 (1974) 1-27
16. Hoemann C.D., Sun J., Legare A., McKee M.D., and Buschmann M.D. Tissue engineering of cartilage using an injectable and adhesive chitosan-based-cell delivery vehicle. Osteoarthritis Cartilage (2005) 318-329
17. Kruyt M.C., Stijns M.M., Fedorovich N.E., de Bruijn J.D., van Blitterswijk C.A., Verbout A.J., et al. Genetic marking with the DeltaLNGFR-gene for tracing goat cells in bone tissue engineering. J Orthop Res 22 (2004) 697-702
18. Sato T., Chen G., Ushida T., Ishii T., Ochiai N., and Tateishi T. Evaluation of PLLA-collagen hybrid sponge as a scaffold for cartilage tissue engineering. Mater Sci Eng 24 (2004) 365-372
19. Chen G., Sato T., Ushida T., Hirochika R., Ochiai N., and Tateishi T. Regeneration of cartilage tissue by combination of canine chondrocyte and a hybrid mesh scaffold. Mater Sci Eng 24 (2004) 373-378
20. Dell'Accio F., De Bari C., and Luyten F.P. Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Exp Cell Res 287 (2003) 16-27
21. Marijnissen W.J., van Osch G.J., Aigner J., van der Veen S.W., Hollander A.P., Verwoerd-Verhoef H.L., et al. Alginate as a chondrocyte-delivery substance in combination with a non-woven scaffold for cartilage tissue engineering. Biomaterials 23 (2002) 1511-1517
22. Sato T., Chen G., Ushida T., Ishii T., Ochiai N., and Tateishi T. Tissue-engineered cartilage by in vivo culturing of chondrocytes in PLGA-collagen hybrid sponge. Mater Sci Eng 17 (2001) 83-89
23. Amiel G.E., Yoo J.J., Kim B., and Atala A. Tissue engineered stents created from chondrocytes. J Urol 165 (2001) 2091-2095
24. Lohmann C.H., Schwartz Z., Niederauer G.G., Carnes D.L., Dean D.D., and Boyan B.D. Pretreatment with platelet derived growth factor-BB modulates the ability of costochondral resting zone chondrocytes incorporated into PLA/PGA scaffolds to form new cartilage in vivo. Biomaterials 21 (2000) 49-61
25. Puelacher W.C., Kim S.W., Vacanti J.P., Schloo B., Mooney D., and Vacanti C.A. Tissue-engineered growth of cartilage: the effect of varying the concentration of chondrocytes seeded onto synthetic polymer matrices. Int J Oral Maxillofac Surg 23 (1994) 49-53
26. Haisch A., Groger A., Radke C., Ebmeyer J., Sudhoff H., Grasnick G., et al. Macroencapsulation of human cartilage implants: pilot study with polyelectrolyte complex membrane encapsulation. Biomaterials 21 (2000) 1561-1566
27. Dausse Y., Grossin L., Miralles G., Pelletier S., Mainard D., Hubert P., et al. Cartilage repair using new polysaccharidic biomaterials: macroscopic, histological and biochemical approaches in a rat model of cartilage defect. Osteoarthritis Cartilage 11 (2003) 16-28
28. Oshima Y., Watanabe N., Matsuda K., Takai S., Kawata M., and Kubo T. Behaviour of transplanted bone marrow-derived GFP mesenchymal cells in osteochondral defect as a simulation of autologous transplantation. J Histochem Cytochem 53 (2005) 207-216
29. Lammi P.E., Lammi M.J., Tammi R.H., Helminen H.J., and Espanha M.M. Strong hyaluronan expression in the full-thickness rat articular cartilage repair tissue. Histochem Cell Biol 115 (2001) 301-308
30. Grundnes O., and Reikeras O. Effects of function and weight-bearing on the healing of full-thickness cartilage defects in rats. Scand J Med Sci Sports 5 (1995) 297-301
31. Goransson H., Lehtosalo J., Vuola J., Patiala H., and Rokkanen P. Regeneration of defects in articular cartilage with callus and cortical bone grafts. An experimental study. Scand J Plast Reconstr Surg Hand Surg 29 (1995) 281-287
32. An Y.H., and Freidman R.J. Animal Models in Orthopaedic Research (1999), CRC Press LLC
33. Tamai N., Myoui A., Hirao M., Kaito T., Ochi T., Tanaka J., et al. A new biotechnology for articular cartilage repair: subchondral implantation of a composite of interconnected porous hydroxyapatite, synthetic polymer (PLA-PEG), and bone morphogenetic protein-2 (rhBMP-2). Osteoarthritis Cartilage 13 (2005) 405-417
34. Trzeciak T., Kruczynski J., Jaroszewski J., and Lubiatowski P. Evaluation of cartilage reconstruction by means of autologous chondrocyte versus periosteal graft transplantation: an animal study. Transplant Proc 38 (2006) 305-311
35. Shao X.X., Hutmacher D.W., Ho S.T., Goh J., and Lee E.H. Evaluation of a hybrid scaffold/cell construct in repair of high-load-bearing osteochondral defects in rabbits. Biomaterials 27 (2006) 1071-1080
36. Chuma H., Mizuta H., Kudo S., Takagi K., and Hiraki Y. One day exposure to FGF-2 was sufficient for the regenerative repair of full-thickness defects of articular cartilage in rabbits. Osteoarthritis Cartilage 12 (2004) 834-842
37. Wei X., and Messner K. Maturation-dependent durability of spontaneous cartilage repair in rabbit knee joint. J Biomed Mater Res 46 (1999) 539-548
38. Han C.W., Chu C.R., Adachi N., Usas A., Fu F.H., Huard J., et al. Analysis of rabbit articular cartilage repair after chondrocyte implantation using optical coherence tomography. Osteoarthritis Cartilage 11 (2003) 111-121
39. Buma P., Pieper J.S., vanTienen T., van Susante J.C., van der Kraan P.M., Veerkamp J.H., et al. Cross-linked type I and type II collagenous matrices for the repair of full-thickness articular cartilage defects-a study in rabbits. Biomaterials 24 (2003) 3255-3263
40. Rudert M., Wilms U., Hoberg M., and Wirth C.J. Cell-based treatment of osteochondral defects in the rabbit knee with natural and synthetic matrices: cellular seeding determines the outcome. Arch Orthop Trauma Surg 125 (2005) 598-608
41. Fan H., Hu Y., Zhang C., Li X., Lv R., Qin L., et al. Cartilage regeneration using mesenchymal stem cells and a PLGA-gelatin/chondroitin/hyaluronate hybrid scaffold. Biomaterials 27 (2006) 4573-4580
42. Fukuda A., Kato K., Hasegawa M., Hirata H., Sudo A., Okazaki K., et al. Enhanced repair of large osteochondral defects using a combination of artificial cartilage and basic fibroblast growth factor. Biomaterials 26 (2005) 4301-4308
43. Mierisch C.M., Cohen S.B., Jordan L.C., Robertson P.G., Balian G., and Diduch D.R. Transforming growth factor-β in calcium alginate beads for the treatment of articular cartilage defects in the rabbit. Arthroscopy 18 (2002) 892-900
44. Makino T., Fujioka H., Kurosaka M., Matsui N., Yoshihara H., and Tsunoda M. Histologic analysis of the implanted cartilage in an exact-fit osteochondral transplantation model. Arthroscopy 17 (2001) 747-751
45. Uematsu K., Hattori K., Ishimoto Y., Yamauchi J., Habata T., Takakura Y., et al. Cartilage regeneration using mesenchymal stem cells and a three-dimensional poly-lactic-glycolic acid (PLGA) scaffold. Biomaterials 26 (2005) 4273-4279
46. Ptonczak M., Czubak J., and Kawiak J. Repair of articular cartilage defects with cultured chondrocytes on polysulphonic membrane: experimental studies in rabbits. Transplant Proc 38 (2006) 312-313
47. Kuo A.C., Rodrigo J.J., Reddi A.H., Curtiss S., Grotkopp E., and Chiu M. Microfracture and bone morphogenetic protein 7 (BMP-7) synergistically stimulate articular cartilage repair. Osteoarthritis Cartilage 14 (2006) 1126-1135
48. Kose G.T., Korkusuz F., Ozkul A., Soysal Y., Ozdemir T., Yildiz C., et al. Tissue engineered cartilage on collagen and PHBV matrices. Biomaterials 26 (2005) 5187-5197
49. Ito Y.I., Ochi M., Adachi N., Sugawara K., Yanada S., Ikada Y., et al. Repair of osteochondral defect with tissue-engineered chondral plug in a rabbit model. Arthroscopy 21 (2005) 1155-1163
50. Brittberg M., Sjogren-Jansson E., Llindahl A., and Peterson L. Influence of fibrin sealant (Tiseel) on osteochondral defect repair in the rabbit knee. Biomaterials 18 (1997) 235-242
51. Freed L.E., Grande D., Lingbin Z., Emmanual J., Marquis J.C., and Langer R. Joint resurfacing using allograft chondrocytes and synthetic biodegradable polymer scaffolds. J Biomed Mater Res 28 (1994) 891-899
52. Sellers R.S., Zhang R., Glasson S., Kim H.D., Peluso D., D'Augusta D.A., et al. Repair of articular cartilage defects one year after treatment with recombinant human bone morphogenic protein-2 (rhBMP-2). J Bone Joint Surg 82 (2000) 151-160
53. Ramallal M., Maneiro E., Lopez E., Fuentes-Boquete I., Lopez-Armada M.J., Fernandez-Sueiro J.L., et al. Xeno-implantation of pig chondrocytes into rabbit to treat localized articular cartilage defects: an animal model. Wound Repair Regen 12 (2004) 337-345
54. Reinholz G.G., Lu L., Saris D.F., Yaszemski M.J., and O'Driscoll S.W. Animal models for cartilage reconstruction. Biomaterials 25 (2004) 1511-1521
55. Wei X., Gao J., and Messner K. Maturation-dependant repair of untreated osteochondral defects in the rabbit knee joint. J Biomed Mater Res 34 (1997) 63-72
56. Dell'Accio F., Vanlauwe J., Bellemans J., Neys J., De Bari C., and Luyten F.P. Expanded phenotypically stable chondrocytes persist in the repair tissue and contribute to cartilage matrix formation and structural integration in a goat model of autologous chondrocyte implantation. J Orthop Res 21 (2003) 123-131
57. Rudert M. Histological evaluation of osteochondral defects: consideration of animal models with emphasis on the rabbit, experimental setup, follow-up and applied methods. Cells Tissues Organs 17 (2002) 229-240
58. Breinan H.A., Minas T., Hsu H., Nehrer S., Sledge B., and Spector M. Effects of cultured autologous chondrocytes on repair of chondral defects in a canine model. J Bone Joint Surg 79 (1997) 1439-1451
59. Breinan H.A., Minas T., Hsu H., Nehrer S., Shortkroff S., and Spector M. Autologous chondrocyte implantation in a canine model: change in composition of reparative tissue with time. J Orthop Res 19 (2001) 482-492
60. Chen G., Sato T., Tanaka J., and Tateishi T. Preparation of a biphasic scaffold for osteochondral tissue engineering. Mater Sci Eng 26 (2006) 118-123
61. Cook S.D., Patron L.P., Salkeld S.L., and Rueger D.C. Repair of articular cartilage defects with osteogenic protein-1 (BMP-7) in dogs. J Bone Joint Surg Am 85 (2003) 116-123
62. van Dyk G.E., Dejardin L.M., Flo G., and Johnson L.L. Cancellous bone grafting of large osteochondral defects: an experimental study in dogs. Arthroscopy 14 (1998) 311-320
63. Feczko P., Hangody L., Varga J., Bartha L., Dioszegi Z., Bodo G., et al. Experimental results of donor site filling with autologous osteochondral mosaicplasty. Arthroscopy 19 (2003) 755-761
64. Lee C.R., Grodzinsky A.J., Hsu H.P., and Spector M. Effects of a cultured autologous chondrocyte-seeded type II collagen scaffold on the healing of a chondral defect in a canine model. J Orthop Res 21 (2003) 272-281
65. Nehrer S., Breinan H.A., Ramappa A., Hsu H.P., Minas T., Shortkroff S., et al. Chondrocyte-seeded collagen matrices implanted in a chondral defect in a canine model. Biomaterials 19 (1998) 2313-2328
66. Shortkroff S., Barone L., Hsu H.P., Wrenn C., Gagne T., Chi T., et al. Healing of chondral and osteochondral defects in a canine model: the role of cultures chondrocytes in regeneration of articular cartilage. Biomaterials 17 (1996) 147-154
67. Lu Y., Hayashi K., Hecht P., Fanton G., Thabit G., Cooley A.J., et al. The effect of monopolar radiofrequency energy on partial-thickness defects of articular cartilage. Arthroscopy 16 (2000) 527-536
68. Frosch K., Drengk A., Krause P., Viereck V., Miosge N., Werner C., et al. Stem cell-coated titanium implants for the partial joint resurfacing of the knee. Biomaterials 27 (2006) 2542-2549
69. Kandel R.A., Grynpas M., Pilliar R., Lee J., Wang J., Waldman S., et al. Repair of osteochondral defects with biphasic cartilage-calcium polyphosphate constructs in a sheep model. Biomaterials 27 (2006) 4120-4131
70. Siebert C.H., Miltner O., Weber M.W., Sopka S., Koch S., and Niedhart C. Healing of osteochondral grafts in an ovine model under the influence of bFGF. Arthroscopy 19 (2003) 182-187
71. Tibesku C.O., Szuwart T., Kleffner T.O., Schlegel P.M., Jahn U.R., van Aken H., et al. Hyaline cartilage degenerated after autologous osteochondral transplantation. J Orthop Res 22 (2004) 1210-1214
72. Tytherleigh-Strong G., Hurtig M., and Miniaci A. Intra-articular hyaluronan following autogenous osteochondral grafting of the knee. Arthroscopy 21 (2005) 999-1005
73. Chiang H., Kuo T., Tsai C., Lin M., She B., Huang Y., et al. Repair of porcine articular cartilage defect with autologous chondrocyte transplantation. J Orthop Res 23 (2005) 584-593
74. Burks R.T., Greis P.E., Arnoczky S.P., and Scher C. The use of a single osteochondral autograft plug in the treatment of a large osteochondral lesion in the femoral condyle: an experimental study in sheep. Am J Sports Med 34 (2006) 247-255
75. Pearce S.G., Hurtig M.B., Clarnette R., Kalra M., Cowan B., and Miniaci A. An investigation of 2 techniques for optimizing joint surface congruency using multiple cylindrical osteochondral autografts. Arthroscopy 17 (2001) 50-55
76. Dorotka R., Windberger U., Macfelda K., Bindreiter U., Toma C., and Nehrer S. Repair of articular cartilage defects treated by microfracture and a three-dimensional collagen matrix. Biomaterials 26 (2005) 3617-3629
77. Uhl M., Lahm T., Bley T.A., Haberstroh J., Mrosek E., Ghanem N., et al. Experimental autologous osteochondral plug transfer in the treatment of focal chondral defects: magnetic resonance imaging signs of technical success in sheep. Acta Radiol 46 (2005) 875-880
78. von Rechenberg B., Akens M.K., Nadler D., Bittmann P., Zlinszky K., Kutter A., et al. Changes in subchondral bone in cartilage resurfacing - an experimental study in sheep using different types of osteochondral grafts. Osteoarthritis Cartilage 11 (2003) 265-277
79. Brehm W., Aklin B., Yamashita T., Rieser F., Trub T., Jokob R.P., et al. Repair of superficial osteochondral defects with an autologous scaffold-free cartilage construct in a caprine model: implantation method and short-term. Osteoarthritis Cartilage 14 (2006) 1214-1226
80. Niederauer G.G., Slivka M.A., Leatherbury N.C., Korvick D.L., Harroff H.H., Ehler W.C., et al. Evaluation of multiphase implants for repair of focal osteochondral defects in goats. Biomaterials 21 (2000) 2561-2574
81. Jackson D.W., Lalor P.A., Aberman H.M., and Simon T.M. Spontaneous repair of full-thickness defects of articular cartilage in a goat model: a preliminary study. J Bone Joint Surg 83 (2001) 53-64
82. Kangarlu A., and Gahunia H.K. Magnetic resonance imaging characterization of osteochondral defect repair in a goat model at 8T. Osteoarthritis Cartilage 14 (2006) 52-62
83. Lane J.G., Massie J.B., Ball S.T., Amiel M.E., Chen A.C., Bae W.C., et al. Follow-up of osteochondral plug transfer in a goat model: a 6-month study. Am J Sports Med 32 (2004) 1440-1450
84. Louwerse R.T., Heyligers I.C., Klein-Nulend J., Sugihara S., van Kampen G.P.J., and Semeins C.M. Use of recombinant human osteogenic protein-1 for the repair of subchondral defects in articular cartilage in goats. J Biomed Mater Res 49 (2000) 506-516
85. Quintavalla J., Uziel-Fusi S., Yin J., Boehnlein, Pastor G., Blancuzzi V., et al. Fluorescently labeled mesenchymal stem cells (MSCs) maintain multilineage potential and can be detected following implantation into articular cartilage defects. Biomaterials 23 (2002) 109-119
86. Shahgaldi B.F. Repair of large osteochondral defects: load-bearing and structural properties of osteochondral repair tissue. Knee 5 (1998) 111-117
87. von Susante J., Buma P., Schuman L., Homminga G.N., van den Berg, and Veth R. Resurfacing potential of heterologous chondrocytes suspended in fibrin glue in large full-thickness defects of femoral articular cartilage: an experimental study in the goat. Biomaterials 20 (1999) 1167-1175
88. Welch R.D., Berry B.H., Crawford K., Zhang H., Zobitz M., Bronson D., et al. Subchondral defects in caprine femora augmented with in situ setting hydroxyapatite cement, polymethylmethacrylate, or autogenous bone graft: biomechanical and histomorphological analysis after two-years. J Orthop Res (2002) 464-472
89. Lane J.G., Tontz W.L., Scott T.B., Jennifer B.M., Chen A.C., Bae W.C., et al. A morphogenic, biochemical, and biomechanical assessment of short-term effects of osteochondral autograft plug transfer in an animal model. Arthroscopy 17 (2001) 856-863
90. Kirker-Head C.A., Van Sickle D.C., Ek S.W., and McCool J.C. Safety of, and biological and functional response to, a novel metallic implant for the management of focal full-thickness cartilage defects: preliminary assessment in an animal model to 1 year. J Orthop Res 24 (2006) 1095-1108
91. Hembry R.M., Dyce J., Driesang I., Hunziker E.B., Fosang A.J., Tyler J., et al. Immunolocalization of matrix metalloproteinases in partial-thickness defects in pig articular cartilage: a preliminary report. J Bone Joint Surgery 83 (2001) 826-838
92. Vasara A.I., Hyttinen M.M., Pulliainen P., Lammi M.J., Jurvelin J.S., and Peterson L. Immature porcine knee cartilage lesions show good healing with or without autologous chondrocyte transplantation. Osteoarthritis Cartilage 14 (2006) 1066-1074
93. Harman B.D., Weeden S.H., Lichota D.K., and Brindley G.W. Osteochondral autograft transplantation in the porcine knee. Am J Sports Med 34 (2006) 913-918
94. Gotterbarm T., Richter W., Jung M., Berardi Vilei S., Mainil-Varlet P., Yamashita T., et al. An in vivo study of a growth-factor enhanced, cell free, two layered collagen-tricalcium phosphate in deep osteochondral defects. Biomaterials 27 (2006) 3387-3395
95. Mainil-Varlet P., Rieser F., Grogan S., Mueller W., Saager C., and Jakob R.P. Articular cartilage repair using a tissue-engineered cartilage-like implant: an animal study. Osteoarthritis Cartilage 9 (2001) S6-S15
96. Chang C.H., Kuo T.F., Lin C.C., Chou C.H., Chen K.H., Lin F.H., et al. Tissue engineering-based cartilage repair with allogenous chondrocytes and gelatin-chondroitin-hyaluronan tri-copolymer scaffold: a porcine model assessed at 18,24, and 36 weeks. Biomaterials 27 (2006) 1876-1888
97. Gal P., Necas A., Adler J., Teyschl O., Fabian P., and Bibrova S. Transplantation of the autogenous chondrocyte graft to physeal defects: an experimental study in pigs. Acta Vet Brno 71 (2002) 327-332
98. Bryant S.J., and Anseth K.S. The effects of scaffold thickness on tissue engineered cartilage in photo cross linked poly(ethylene oxide) hydrogels. Biomaterials 22 (2001) 619-626
99. Worster A.A., Brower-Toland B.D., Fortier A.L., Bent S.J., Williams J., and Nixon A.J. Chondrocytic differentiation of mesenchymal stem cells sequentially exposed to transforming growth factor-beta1 in monolayer and insulin-like growth factor-I in a three-dimensional matrix. J Orthop Res 19 (2001) 738-749
100. Wilke M.M., Nydam D.V., and Nixon A.J. Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model. J Orthop Res 25 (2007) 913-925
101. Strauss E.J., Goodrich L.R., Chen C., Hidaka C., and Nixon A.J. Biochemical and biomechanical properties of lesion and adjacent articular cartilage after chondral defect repair in an equine model. Am J Sports Med 33 (2005) 1647-1653
102. Nixon A.J., Fortier L.A., Williams J., and Mohammed H. Enhanced repair of extensive articular defects by insulin-like growth factor-I-laden fibrin composites. J Orthop Res 17 (1999) 475-487
103. Hidaka C., Goodrich L.R., Chen C.T., Warren R.F., Crystal R.G., and Nixon A.J. Acceleration of cartilage repair by genetically modified chondrocytes over expressing bone morphogenetic protein-7. J Orthop Res 21 (2003) 573-583
104. Hendrickson D.A., Nixon A.J., Grande D.A., Todhunter R.J., Minor R.M., Erb H., et al. Chondrocyte-fibrin matrix transplants for resurfacing extensive articular cartilage defects. J Orthop Res 12 (1994) 485-497
105. Gratz K.R., Wong V.W., Chen A.C., Fortier L.A., Nixon A.J., and Sah R.L. Biomechanical assessment of tissue retrieved after in vivo cartilage defect repair: tensile modulus of repair tissue and integration with host cartilage. J Biomech 39 (2006) 138-146
106. Fortier L.A., Nixon A.J., Williams J., and Cable C.S. Isolation and chondrocytic differentiation of equine bone marrow-derived mesenchymal stem cells. Am J Vet Res 59 (1998) 1182-1187
107. Fortier L.A., Mohammed H.O., Lust G., and Nixon A.J. Insulin-like growth factor-I enhances cell-based repair of articular cartilage. J Bone Joint Surg 84 (2002) 276-288
108. Hurtig M.B., Fretz P.B., Doige C.E., and Schnurr D.L. Effects of lesion size and location on equine articular cartilage repair. Can J Vet Res 52 (1998) 137-146
109. Vachon A.M., McIlwraith C.W., and Keeley F.W. Biochemical-study of repair of induced osteochondral defects of the distal portion of the radial carpal bone in horses by use of periosteal autografts. Am J Vet Res 52 (1991) 328-332
110. Vachon A.M., McIlwraith C.W., Powers C.W., McFadden B.E., and Amiel P.R. Morphologic and biochemical study of sternal cartilage autografts for resurfacing induced osteochondral defects in horses. Am J Vet Res 53 (1992) 1038-1047
111. Shoemaker R.S., Bertone A.L., Martin G.S., McIlwraith C.W., Roberts E.D., Pechman R., et al. Effects of intraarticular administration of methylprednisolone acetate on normal articular-cartilage and on healing of experimentally induced osteochondral defects in horses. Am J Vet Res 53 (1992) 1446-1453
112. Kisiday J.D., Kopesky P.W., Evans C.H., Grodzinsky A.J., McIlwraith C.W., and Frisbie D.D. Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J Orthop Res 26 (2007) 322-331
113. Howard R.D., McIlwraith C.W., Trotter G.W., Powers B.E., McFadden P.R., Harwood F.L., et al. Long-term fate and effects of exercise on sternal cartilage autografts used for repair of large osteochondral defects in horses. Am J Vet Res 55 8 (1994) 1158-1167
114. Frisbie D.D., Trotter G.W., Powers B.E., Rodkey W.G., Steadman J.R., Howard R.D., et al. Arthroscopic subchondral bone plate microfracture technique augments healing of large chondral defects in the radial carpal bone and medial femoral condyle of horses. Vet Surg 28 (1999) 242-255
115. Bertone A.L., Bramlage L.R., McIlwraith C.W., and Malemud C.L. Comparison of proteoglycan and collagen in articular cartilage of horses with naturally developing osteochondrosis and healing osteochondral fragments of experimentally induced fractures. Am J Vet Res 66 (2005) 1881-1890
116. Litzke L.F., Wagner E., Baumgaertner W., Hetzel U., Josimovic-Alasevic O., and Libera J. Repair of extensive articular cartilage defects in horses by autologous chondrocyte transplantation. Ann Biomed Eng 32 (2004) 57-69
117. Barnewitz D., Endres M., Kruger I., Becker A., Zimmermann J., Wilke I., et al. Treatment of articular cartilage defects in horses with polymer-based cartilage tissue engineering grafts. Biomaterials 27 (2006) 2882-2889
118. Frisbie D.D., Oxford J.T., Southwood L., Trotter G.W., Rodkey W.G., Steadman J.R., et al. Early events in cartilage repair after subchondral bone microfracture. Clin Orthop Relat Res 407 (2003) 215-227