Operative Techniques in Orthopaedics
Volume 20, Issue 2 , Pages 76-89 , June 2010

Advances in Tissue Engineering Techniques for Articular Cartilage Repair

  • Amgad M. Haleem, MD
    • ,
  • Constance R. Chu, MD

      Affiliations

    • Corresponding Author InformationAddress reprint requests to Constance R. Chu, MD, Department of Orthopedic Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA

References 

  1. Chu CR, Convery FR, Akeson WH, et al. Cartilage transplantation (Clinical results in the knee). Clin Orthop Relat Res. 1999;360:159–168
  2. Brittberg M, Lindahl A, Nilsson A, et al. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med. 1994;331:889–895
  3. Saris DB, Vanlauwe J, Victor J, et al. Characterized chondrocyte implantation results in better structural repair when treating symptomatic cartilage defects of the knee in a randomized controlled trial versus microfracture. Am J Sports Med. 2008;36:235–246
  4. Salgado AJ, Oliveira JT, Pedro AJ, et al. Adult stem cells in bone and cartilage tissue engineering. Curr Stem Cell Res Ther. 2006;1:345–364
  5. Kisiday JD, Kopesky PW, Evans CH, et al. Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J Orthop Res. 2008;26:322–331
  6. Vidal MA, Robinson SO, Lopez MJ, et al. Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow. Vet Surg. 2008;37:713–724
  7. Miljkovic ND, Cooper GM, Marra KG. Chondrogenesis, bone morphogenetic protein-4 and mesenchymal stem cells. Osteoarthritis Cartilage. 2008;16:1121–1130
  8. Wakitani S, Imoto K, Yamamato T, et al. Human autologous culture expanded bone marrow mesenchymal stem cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage. 2002;10:199–206
  9. Kramer J, Böhrnsen F, Lindner U, et al. In vivo matrix-guided human mesenchymal stem cells. Cell Mol Life Sci. 2006;63:616–626
  10. Devine SM, Peter S, Martin BJ, et al. Mesenchymal stem cells: Stealth and expression. Cancer J. 2001;7(suppl 2):76–82
  11. Le Blanc K, Tammik C, Rosendahl K, et al. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31:890–896
  12. Kleinman HK, Klebe RJ, Martin GR. Role of collagenous matrices in the adhesion and growth of cells. J Cell Biol. 1981;88:473–485
  13. Kim HD, Valentini RF. Retention and activity of BMP-2 in hyaluronic acid-based scaffolds in vitro. J Biomed Mater Res. 2002;59:573–584
  14. Aigner J, Tegeler J, Hutzler P, et al. Cartilage tissue engineering with novel nonwoven structured biomaterial based on hyaluronic acid benzyl ester. J Biomed Mater Res. 1998;42:172–181
  15. Brun P, Abatangelo G, Radice M, et al. Chondrocyte aggregation and reorganization into three-dimensional scaffolds. J Biomed Mater Res. 1999;46:337–346
  16. Solchaga LA, Yoo JU, Lundberg M, et al. Hyaluronic acid-based polymers in the treatment of osteochondral defects. J Orthop Res. 2000;18:773–780
  17. Grigolo B, Lisignoli G, Piacentini A, et al. Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAff 11): Molecular, immunohistochemical and ultrastructural analysis. Biomaterials. 2002;23:1187–1195
  18. Knudson W, Casey B, Nishida Y, et al. Hyaluronan oligosacchrarides perturb cartilage matrix homeostasis and induce chondrocytic chondrolysis. Arthritis Rheum. 2000;43:1165–1174
  19. Häuselmann HJ, Fernandes RJ, Mok SS, et al. Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads. J Cell Sci. 1994;107(Pt. 1):17–27
  20. Suh JK, Matthew HW. Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: A review. Biomaterials. 2000;21:2589–2598
  21. Kim SE, Park JH, Cho YW, et al. Porous chitosan scaffold containing microspheres loaded with transforming growth factor-beta1: Implications for cartilage tissue engineering. J Control Release. 2003;91:365–374
  22. Visna P, Pasa L, Hart R, et al. Treatment of deep chondral defects of the knee using autologous chondrocytes cultured on a support: Results after one year. Acta Chir Orthop Traumatol Cech. 2003;70:356–362
  23. Visna P, Pasa L, Cizmár I, et al. Treatment of deep cartilage defects of the knee using autologous chondrograft transplantation and by abrasive techniques (A randomized controlled study). Acta Chir Belg. 2004;104:709–714
  24. van Susante JL, Buma P, Schuman L, et al. 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. 1999;20:1167–1175
  25. Kawabe N, Yoshinao M. The repair of full-thickness articular cartilage defects (Immune responses to reparative tissue formed by allogeneic growth plate chondrocyte implants). Clin Orthop Relat Res. 1991;268:279–293
  26. Marx RE. Platelet-rich plasma: Evidence to support its use. J Oral Maxillofac Surg. 2004;62:489–496
  27. Lundquist R, Dziegiel MH, Agren MS. Bioactivity and stability of endogenous fibrogenic factors in platelet-rich fibrin. Wound Repair Regen. 2008;16:356–363
  28. Ferretti M, Marra KG, Kobayashi K, et al. Controlled in vivo degradation of genipin crosslinked polyethylene glycol hydrogels within osteochondral defects. Tissue Eng. 2006;12:2657–2663
  29. Chu CR, Coutts RD, Yoshioka M, et al. Cartilage repair using allogeneic perichondrocyte-seeded biodegradable porous polylactic acid (PLA): A tissue-engineering study. J Biomed Mater Res. 1995;29:1147–1154
  30. Grande DA, Halberstadt C, Naughton G, et al. Evaluation of matrix scaffolds for tissue engineering of articular cartilage grafts. J Biomed Mater Res. 1997;34:211–220
  31. Caterson EJ, Nesti LJ, Li WJ, et al. Three-dimensional cartilage formation by bone marrow-derived cells seeded in polylactide/alginate amalgam. J Biomed Mater Res. 2001;57:394–403
  32. McNickle AG, Provencher MT, Cole BJ. Overview of existing cartilage repair technology. Sports Med Arthrosc. 2008;16:196–201
  33. Falez F, Sciarretta F. Treatment of osteochondral symptomatic defects of the knee with SaluCartilage. J Bone Joint Surg Br. 2005;87(suppl II):202
  34. Getgood A, Brooks R, Fortier L, et al. Cartilage tissue engineering: Today's research, tomorrow's practice?. J Bone Joint Surg Br. 2009;91:565–576
  35. Cassiede P, Dennis JE, Ma F, et al. Osteochondrogenic potential of marrow mesenchymal progenitor cells exposed to TGF-beta 1 or PDGF-BB as assayed in vivo and in vitro. J Bone Miner Res. 1996;11:1264–1273
  36. Pagnotto MR, Wang Z, Karpie JC, et al. Adeno-associated viral gene transfer of transforming growth factor-β1 to human mesenchymal stem cells improves cartilage repair. Gene Ther. 2007;14:804–813
  37. Sekiya I, Colter DC, Prockop DJ. BMP-6 enhances chondrogenesis in a subpopulation of human marrow stromal cells. Biochem Biophys Res Commun. 2001;284:411–418
  38. Longobardi L, O'Rear L, Aakula S, et al. Effect of IGF-1 in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signalling. J Bone Miner Res. 2006;21:626–636
  39. Cuevas P, Burgos J, Baird A. Basic fibroblast growth factor (FGF) promotes cartilage repair in vivo. Biochem Biophys Res Commun. 1988;156:611–618
  40. Solchaga LA, Penick K, Porter JD, et al. FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells. J Cell Physiol. 2005;203:398–409
  41. Kieswetter K, Schwartz Z, Alderete M, et al. Platelet derived growth factor stimulates chondrocyte proliferation but prevents endochondral maturation. Endocrine. 1997;6:257–264
  42. Schmidt MB, Chen EH, Lynch SE. A review of the effects of insulin-like growth factor and platelet derived growth factor on in vivo cartilage healing and repair. Osteoarthritis Cartilage. 2006;14:403–412
  43. Williams Iii RJ, Brophy RH. Cartilage repair procedures: Clinical approach and decision making. Instr Course Lect. 2008;57:553–561
  44. Blanke M, Carl HD, Klinger P, et al: Transplanted chondrocytes inhibit endochondral ossification within cartilage repair tissue. Calcif Tissue Int (in press)
  45. Coyle CH, Izzo NJ, Chu CR. Sustained hypoxia enhances chondrocyte matrix synthesis. J Orthop Res. 2009;27:793–799
  46. Zscharnack M, Poesel C, Galle J, et al. Low oxygen expansion improves subsequent chondrogenesis of ovine bone-marrow-derived mesenchymal stem cells in collagen type I hydrogel. Cells Tissues Organs. 2009;190:81–93
  47. Wood JJ, Malek MA, Frassica FJ, et al. Autologous cultured chondrocytes: Adverse events reported to the United States Food and Drug Administration. J Bone Joint Surg Am. 2006;88:503–507
  48. Brittberg M. Autologous chondrocyte implantation-technique and long-term follow-up. Injury. 2008;39(suppl 1):S40–S49
  49. Abelow SP, Guillen P, Ramos T. Arthroscopic technique for matrix induced autologous chondrocyte implantation for the treatment of large chondral defects in the knee and ankle. Oper Tech Orthop. 2006;16:257–261
  50. Krishnan SP, Skinner JA, Carrington J, et al. Collagen-covered autologous chondrocyte implantation for osteochondritis dissecans of the knee. J Bone Joint Surg Br. 2006;88:203–205
  51. Steinwachs M. New technique for cell-seeded collagen-matrix-supported autologous chondrocyte transplantation. Arthroscopy. 2009;25:208–211
  52. Gobbi A, Kon E, Berruto M, et al. Patellofemoral full-thickness chondral defects treated with Hyalograft-C: A clinical, arthroscopic, and histologic review. Am J Sports Med. 2006;34:1763–1773
  53. Erggelet C, Sittinger M, Lahm A. The arthroscopic implantation of autologous chondrocytes for the treatment of full-thickness cartilage defects of the knee joint. Arthroscopy. 2003;19:108–110
  54. Ossendorf C, Kaps C, Kreuz PC, et al. Treatment of posttraumatic and focal osteoarthritic cartilage defects of the knee with autologous polymer-based three-dimensional chondrocyte grafts: 2-year clinical results. Arthritis Res Ther. 2007;9:41
  55. Freed LE, Marquis JC, Nohria A, et al. Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J Biomed Mater Res. 1993;27:11–23
  56. Bonaventure J, Kadhom N, Cohen-Solal L, et al. Reexpression of cartilage specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. Exp Cell Res. 1994;212:97–104
  57. Waldman SD, Spiteri CG, Grynpas MD, et al. Long-term intermittent shear deformation improves the quality of cartilaginous tissue formed in vitro. J Orthop Res. 2003;21:590–596
  58. Waldman SD, Spiteri CG, Grynpas MD, et al. Effect of biomechanical conditioning on cartilaginous tissue formation in vitro. J Bone Joint Surg Am. 2003;85-A(suppl 2):101–105
  59. Crawford DC, Heveran CM, Cannon WD, et al. An autologous cartilage tissue implant NeoCart for treatment of grade III chondral injury to the distal femur: Prospective clinical safety trial at 2 years. Am J Sports Med. 2009;37:1334–1343
  60. Selmi TA, Verdonk P, Chambat P, et al. Autologous chondrocyte implantation in a novel alginate-agarose hydrogel: Outcome at two years. J Bone Joint Surg Br. 2008;90:597–604
  61. Almqvist KF, Dhollander AA, Verdonk PC, et al. Treatment of cartilage defects in the knee using alginate beads containing human mature allogenic chondrocytes. Am J Sports Med. 2009;37:1920–1929
  62. Almqvist KF, Wang L, Broddelez C, et al. Biological freezing of human articular chondrocytes. Osteoarthritis Cartilage. 2001;9:341–350
  63. Adkisson HD, Gillis MP, Davis EC, et al. In vitro generation of scaffold independent neocartilage. Clin Orthop Relat Res. 2001;391(suppl):S280–S294
  64. Lu Y, Dhanaraj S, Wang Z, et al. Minced cartilage without cell culture serves as an effective intraoperative cell source for cartilage repair. J Orthop Res. 2006;24:1261–1270
  65. McCormick F, Yanke A, Provencher MT, et al. Minced articular cartilage—Basic science, surgical technique, and clinical application. Sports Med Arthrosc. 2008;16:217–220
  66. Kitchel SH, Wang MY, Lauryssen CL. Techniques for aspirating bone marrow for use in spinal surgery. Neurosurgery. 2005;57(4 suppl):286–289
  67. Lee HS, Huang GT, Chiang H, et al. Multipotential mesenchymal stem cells from femoral bone marrow near the site of osteonecrosis. Stem Cells. 2003;21:190–199
  68. Elvenes J, Knutsen G, Johansen O, et al. Development of a new method to harvest chondroprogenitor cells from underneath cartilage defects in the knees. J Orthop Sci. 2009;14:410–417
  69. Minas T, Gomoll AH, Rosenberger R, et al. Increased failure rate of autologous chondrocyte implantation after previous treatment with marrow stimulation techniques. Am J Sports Med. 2009;37:902–908
  70. Sánchez M, Azofra J, Anitua E, et al. Plasma rich in growth factors to treat an articular cartilage avulsion: A case report. Med Sci Sports Exerc. 2003;35:1648–1652
  71. Driesang IM, Hunziker EB. Delamination rates of tissue flaps used in articular cartilage repair. J Orthop Res. 2000;18:909–911
  72. Peterson L, Brittberg M, Lindahl A. Autologous chondrocyte transplantation of the ankle. Foot Ankle Clin. 2003;8:291–303
  73. Hoemann CD, Hurtig M, Rossomacha E, et al. Chitosan-glycerol phosphate/blood implants improve hyaline cartilage repair in ovine microfracture defects. J Bone Joint Surg Am. 2005;87:2671–2686
  74. Shive MS, Hoemann CD, Restrepo A, et al. BST-CarGel: In situ chondroinduction for cartilage repair. Oper Tech Orthop. 2006;16:271–278
  75. Giannini S, Buda R, Vannini F, et al. One-step bone marrow-derived cell transplantation in talar osteochondral lesions. Clin Orthop Relat Res. 2009;467:3307–3320
  76. Hermann PC, Huber SL, Herrler T, et al. Concentration of bone marrow total nucleated cells by a point-of-care device provides a high yield and preserves their functional activity. Cell Transplant. 2008;16:1059–1069
  77. Trukor Plus (Surgical technique Guide). Smith & Nephew Endoscopy; 2006;
  78. Kerker JT, Leo AJ, Sgaglione NA. Cartilage repair: Synthetics and scaffolds: Basic science, surgical techniques, and clinical outcomes. Sports Med Arthrosc. 2008;16:208–216
  79. Ochi M, Uchio Y, Kawasaki K, et al. Transplantation of cartilage like tissue made by tissue engineering in the treatment of cartilage defects of the knee. J Bone Joint Surg Br. 2002;84:571–578
  80. Friedlaender GE. Immune responses to osteochondral allografts: Current knowledge and future directions. Clin Orthop. 1983;174:58–68
  81. Hunziker EB, Stähli A. Surgical suturing of articular cartilage induces osteoarthritis-like changes. Osteoarthritis Cartilage. 2008;16:1067–1073
  82. Wakitani S, Goto T, Pineda SJ, et al. Repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am. 1994;76:579–592
  83. Wehling N, Palmer GD, Pilapil C, et al. Interleukin-1beta and tumor necrosis factor alpha inhibit chondrogenesis by human mesenchymal stem cells through NF-kappaB-dependent pathways. Arthritis Rheum. 2009;60:801–812
  84. Kubo S, Cooper GM, Matsumoto T, et al. Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle-derived stem cells. Arthritis Rheum. 2009;60:155–165
  85. Sgaglione NA, Florence AS. Bone graft substitute plug failure with giant cell reaction in the treatment of osteochondral lesions of the distal femur: A report of 2 cases with operative revision. Arthroscopy. 2009;25:815–819
  86. Jakobsen RB, Engebretsen L, Slauterbeck JR. An analysis of the quality of cartilage repair studies. J Bone Joint Surg Am. 2005;87:2232–2239
  87. Steadman JR, Briggs KK, Rodrigo JJ, et al. Outcomes of microfracture for traumatic chondral defects of the knee: Average 11-year follow-up. Arthroscopy. 2003;19:477–484
  88. Kreuz PC, Steinwachs MR, Erggelet C, et al. Results after microfracture of full-thickness chondral defects in different compartments in the knee. Osteoarthritis Cartilage. 2006;14:1119–1125
  89. Mithoefer K, Williams RJ, Warren RF, et al. High-impact athletics after knee articular cartilage repair: A prospective evaluation of the microfracture technique. Am J Sports Med. 2006;34:1413–1418
  90. Knutsen G, Drogset JO, Engebretsen L, et al. A randomized trial comparing autologous chondrocyte implantation with microfracture (Findings at five years). J Bone Joint Surg Am. 2007;89:2105–2112
  91. Bartlett W, Skinner JA, Gooding CRM, et al. Autologous chondrocyte implantation versus matrix-induced autologous chondrocyte implantation for osteochondral defects of the knee: A prospective, randomised study. J Bone Joint Surg Br. 2005;87-B:640–645
  92. Nejadnik H, Hui JHP, Choong PF, et al: Is stem cell a good source for autologous chondrocyte implantation? A comparative study. Presented at the 8th World Congress of the International Cartilage Repair Society (ICRS), May 2009, Miami, FL
  93. Dorotka R, Bindreiter U, Macfelda K, et al. Marrow stimulation and chondrocyte transplantation using a collagen matrix for cartilage repair. Osteoarthritis Cartilage. 2005;13:655–664
  94. Volpi P, de Girolamo L, Cervellin M, et al: Treatment of chondral defects with AMIC technique (Autologous Matrix Induced Chondrogenesis) compared to AMIC enhanced by concentrated bone marrow. Presented at the 8th World Congress of the International Cartilage Repair Society (ICRS), May 2009, Miami, FL
  95. Gobbi A, Nunag P, Malinowski K. Treatment of full thickness chondral lesions of the knee with microfracture in a group of athletes. Knee Surg Sports Traumatol Arthrosc. 2005;13:213–221
  96. Gudas R, Kalesinskas RJ, Kimtys V, et al. A prospective randomized clinical study of mosaic osteochondral autologous transplantation versus microfracture for the treatment of osteochondral defects in the knee joint in young athletes. Arthroscopy. 2005;21:1066–1075
  97. Wakitani S, Mitsuoka T, Nakamura N, et al. Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: Two case reports. Cell Transplant. 2004;13:595–600
  98. Wakitani S, Nawata M, Tensho K, et al. Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: Three case reports involving nine defects in five knees. J Tissues Eng Regen Med. 2007;1:74–79
  99. Archer CW, Redman S, Khan I, et al. Enhancing tissue integration in cartilage repair procedures. J Anat. 2006;209:481–493
  100. Li WJ, Tuli R, Huang X, et al. Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials. 2005;26:5158–5166
  101. Evans CH, Robbins PD, Ghivizzani SC, et al. Clinical trial to assess the safety, feasibility, and efficacy of transferring a potentially anti-arthritic cytokine gene to human joints with rheumatoid arthritis. Hum Gene Ther. 1996;7:1261–1280
  102. Gelse K, von der MK, Aigner T, et al. Cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis Rheum. 2003;48:430–441
  103. Madry H, Kaul G, Cucchiarini M, et al. Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther. 2005;12:1171–1179
  104. Guo T, Zhao J, Chang J, et al. Porous chitosan-gelatin scaffold containing plasmid DNA encoding transforming growth factor-beta1 for chondrocytes proliferation. Biomaterials. 2006;27:1095–1103
  105. Capito RM, Spector M. Collagen scaffolds for nonviral IGF-1 gene delivery in articular cartilage tissue engineering. Gene Ther. 2007;14:721–732
  106. Caplan AI. Mesenchymal stem cells and gene therapy. Clin Orthop. 2000;379(suppl):67–70

PII: S1048-6666(09)00144-X

doi: 10.1053/j.oto.2009.10.004

Operative Techniques in Orthopaedics
Volume 20, Issue 2 , Pages 76-89 , June 2010

Article Tools

* Image Usage & Resolution