Osteochondral tissue engineering: Current strategies and challenges

Biotechnology Advances

Volumn 31, Issue 5, 2013, Pages 706-721

  Nukavarapu, Syam P ^a   Dorcemus, Deborah L ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Articular cartilage; Challenges; Gradient scaffolds; Osteochondral interface; Osteochondral plug; Subchondral bone; Tissue engineering

Indexed keywords

ARTICULAR CARTILAGES; BONE AND CARTILAGES; BONE-CARTILAGE INTERFACE; CHALLENGES; GRADIENT SCAFFOLD; OSTEOCHONDRAL; OSTEOCHONDRAL DEFECTS; OSTEOCHONDRAL TISSUE ENGINEERING;

BONE; CARTILAGE; CELL CULTURE; CELLS; DEFECTS; REPAIR; TISSUE; TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

TISSUE SCAFFOLD;

BIOENGINEERING; BONE; DAMAGE; OSTEOLOGY;

ANIMAL; ARTICULAR CARTILAGE; CARTILAGE CELL; CYTOLOGY; HUMAN; METHODOLOGY; REVIEW; TISSUE ENGINEERING;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROCYTES; HUMANS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84879418183     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2012.11.004     Document Type: Review

References (153)

1. Acebes C., Roman-Blas J.A., Delgado-Baeza E., Palacios I., Herrero-Beaumont G. Correlation between arthroscopic and histopathological grading systems of articular cartilage lesions in knee osteoarthritis. Osteoarthritis Cartilage 2009, 17.
2. Aigner T., Reichenberger E., Bertling W., Kirsch T., Stoss H., Vondermark K. Type-X collagen expression in osteoarthritic and rheumatoid articular-cartilage. Virchows Arch B Cell Pathol Incl Mol Pathol 1993, 63.
3. Alberts B., Bray D., Lewis J., Raff M., Roberts K., Watson J.D. Molecular biology of the cell 1994, Garland Publishing, Inc., New York, NY.
4. Alexander A.H. Surgical-treatment of transchondral talar-dome fractures (osteochondritis dissecans) - long-term follow-up. J Bone Joint Surg Am 1980, 62.
5. Amini A.R., Adams D.J., Laurencin C.T., Nukavarapu S.P. Optimally porous and biomechanically compatible scaffolds for large-area bone regeneration. Tissue Eng Part A 2012, 18.
6. Amini A, Laurencin C, Nukavarapu S. (in press). Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng.
7. Angele P., Kujat R., Nerlich M., Yoo J., Goldberg V., Johnstone B. Engineering of osteochondral tissue with bone marrow mesenchymal progenitor: cells in a derivatized hyaluronan-gelatin composite sponge. Tissue Eng 1999, 5.
8. Asawa Y., Ogasawara T., Takahashi T., Yamaoka H., Nishizawa S., Matsudaira K., et al. Aptitude of auricular and nasoseptal chondrocytes cultured under a monolayer or three-dimensional condition for cartilage tissue engineering. Tissue Eng Part A 2009, 15.
9. Athanasiou K.A., Zhu C.F., Wang X., Agrawal C.M. Effects of aging and dietary restriction on the structural integrity of rat articular cartilage. Ann Biomed Eng 2000, 28.
10. Athanasiou K.A., Darling E.M., Hu J.C. Articular cartilage tissue engineering 2009, Morgan & Claypool.
11. Ball L.M., Bernardo M.E., Roelofs H., Lankester A., Cometa A., Egeler R.M., et al. Cotransplantation of ex vivo-expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem-cell transplantation. Blood 2007, 110.
12. Benazet J.-D., Bischofberger M., Tiecke E., Goncalves A., Martin J.F., Zuniga A., et al. A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 2009, 323.
13. Berndt A.L., Harty M. Transchondral fractures (osteochondritis dissecans) of the talus. J Bone Joint Surg Am 1959, 41-A.
14. Bian L., Zhai D.Y., Mauck R.L., Burdick J.A. Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage. Tissue Eng Part A 2011, 17.
15. Blevins F.T., Steadman J.R., Rodrigo J.J., Silliman J. Treatment of articular cartilage defects in athletes: an analysis of functional outcome and lesion appearance. Orthopedics 1998, 21.
16. Boas A.V. Abrasion arthroplasty http://clinicadacartilagem.com.br/index.php?option=com_content&view=article&id=34&Itemid=78&lang=en.
17. Bodine P.V.N., Zhao W.G., Kharode Y.P., Bex F.J., Lambert A.J., Goad M.B., et al. The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol Endocrinol 2004, 18.
18. Brittberg M., Lindahl A., Nilsson A., Ohlsson C., Isaksson O., Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994, 331:889-895.
19. Burr D.B. Anatomy and physiology of the mineralized tissues: role in the pathogenesis of osteoarthrosis. Osteoarthritis Cartilage 2004, 12(Suppl. A).
20. Caffey S., McPherson E., Moore B., Hedman T., Vangsness C.T. Effects of radiofrequency energy on human articular cartilage - an analysis of 5 systems. Am J Sports Med 2005, 33.
21. Carrier R.L., Rupnick M., Langer R., Schoen F.J., Freed L.E., Vunjak-Novakovic G. Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 2002, 8.
22. Chen G.P., Sato T., Tanaka J., Tateishi T. Preparation of a biphasic scaffold for osteochondral tissue engineering. Mater Sci Eng C Biomim Supramol Syst 2006, 26.
23. Chu C.R., Coutts R.D., Yoshioka M., Harwood F.L., Monosov A.Z., Amiel D. Articular-cartilage repair using allogeneic perichondrocyte-seeded biodegradable porous polylactic acid (Pla) - a tissue-engineering study. J Biomed Mater Res 1995, 29.
24. Claus S., Aubert-Foucher E., Demoor M., Camuzeaux B., Paumier A., Piperno M., et al. Chronic exposure of bone morphogenetic protein-2 favors chondrogenic expression in human articular chondrocytes amplified in monolayer cultures. J Cell Biochem 2010, 111.
25. Coburn J.M., Gibson M., Monagle S., Patterson Z., Elisseeff J.H. Bioinspired nanofibers support chondrogenesis for articular cartilage repair. Proc Natl Acad Sci U S A 2012, 109.
26. Connelly J.T., Wilson C.G., Levenston M.E. Characterization of proteoglycan production and processing by chondrocytes and BMSCs in tissue engineered constructs. Osteoarthritis Cartilage 2008, 16.
27. Cooke M.E., Allon A.A., Cheng T., Kuo A.C., Kim H.T., Vail T.P., et al. Structured three-dimensional co-culture of mesenchymal stem cells with chondrocytes promotes chondrogenic differentiation without hypertrophy. Osteoarthritis Cartilage 2011, 19.
28. Csaki C., Schneider P.R.A., Shakibaei M. Mesenchymal stem cells as a potential pool for cartilage tissue engineering. Ann Anat 2008, 190.
29. Curl W.W., Krome J., Gordon E.S., Rushing J., Smith B.P., Poehling G.G. Cartilage injuries: a review of 31,516 knee arthroscopies. Arthroscopy 1997, 13.
30. Custers R.J.H., Creemers L.B., Verbout A.J., van Rijen M.H.P., Dhert W.J.A., Saris D.B.F. Reliability, reproducibility and variability of the traditional Histologic/Histochemical Grading System vs the new OARSI Osteoarthritis Cartilage Histopathology Assessment System. Osteoarthritis Cartilage 2007, 15.
31. Danisovic L., Fau-Varga I., Varga R., Fau-Zamborsky I., Zamborsky D., Fau-Bohmer R., et al. The tissue engineering of articular cartilage: cells, scaffolds and stimulating factors 2011.
32. Darling E.M., Athanasiou K.A. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 2005, 23.
33. Davisson T., Sah R.L., Ratcliffe A. Perfusion increases cell content and matrix synthesis in chondrocyte three-dimensional cultures. Tissue Eng 2002, 8.
34. Deng T, Lv J, Pang J, Liu B, Ke J. Construction of tissue-engineered osteochondral composites and repair of large joint defects in rabbit. J Tissue Eng Regen Med in press.
35. Draper S.D., Fallat L.M. Autogenous bone grafting for the treatment of talar dome lesions. J Foot Ankle Surg 2000, 39.
36. Duncan H., Riddle J., Jundt J., Pitchford W. Osteoarthritis and the subchondral bone plate 1987, Elsevier Sciences.
37. Eckstein F., Milz S., Anetzberger H., Putz R. Thickness of the subchondral mineralised tissue zone (SMZ) in normal male and female and pathological human patellae. J Anat 1998, 192.
38. Eggli P.S., Hunziker E.B., Schenk R.K. Quantitation of structural features characterizing weight-bearing and less-weight-bearing regions in articular-cartilage - a stereological analysis of medial femoral condyles in young-adult rabbits. Anat Rec 1988, 222.
39. Ellman M.B., An H.S., Muddasani P., Im H.-J. Biological impact of the fibroblast growth factor family on articular cartilage and intervertebral disc homeostasis. Gene 2008, 420.
40. Eyre D.R., Wu J.J. Collagen structure and cartilage matrix integrity. J Rheumatol Suppl 1995, 43.
41. Fischer J., Dickhut A., Rickert M., Richter W. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 2010, 62.
42. Flannery C.R., Hughes C.E., Schumacher B.L., Tudor D., Aydelotte M.B., Kuettner K.E., et al. Articular cartilage superficial zone protein (SZP) is homologous to megakaryocyte stimulating factor precursor and is a multifunctional proteoglycan with potential growth-promoting, cytoprotective, and lubricating properties in cartilage metabolism. Biochem Biophys Res Commun 1999, 254.
43. Frohlich M., Malicev E., Gorensek M., Knezevic M., Velikonja N.K. Evaluation of rabbit auricular chondrocyte isolation and growth parameters in cell culture. Cell Biol Int 2007, 31.
44. Gao J.Z., Dennis J.E., Solchaga L.A., Awadallah A.S., Goldberg V.M., Caplan A.I. Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng 2001, 7.
45. Garrett W.E., Speer K.P., Kirkendall D.T. Orthopaedic sports medicine 2000, Lippincott Williams & Wilkins, Philadelphia, PA.
46. Gelse K., von der Mark K., Aigner T., Park J., Schneider H. Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis Rheum 2003, 48.
47. Gelse K., Klinger P., Koch M., Surmann-Schmitt C., von der Mark K., Swoboda B., et al. Thrombospondin-1 prevents excessive ossification in cartilage repair tissue induced by osteogenic protein-1. Tissue Eng Part A 2011, 17.
48. Gelse K., Beyer C., Welsch G., Blanke M. Endochondral Ossification in Cartilage Repair Tissue Hampers Bone Marrow Stimulating Techniques. Rheumatology 2012, S3:002. 10.4172/2161-1149.S3-002.
49. Getgood A.M.J., Kew S.J., Brooks R., Aberman H., Simon T., Lynn A.K., et al. Evaluation of early-stage osteochondral defect repair using a biphasic scaffold based on a collagen-glycosaminoglycan biopolymer in a caprine model. Knee 2012, 19.
50. Giannoudis P.V., Pountos I., Morley J., Perry S., Tarkin H.I., Pape H.-C. Growth factor release following femoral nailing. Bone 2008, 42.
51. Glowacki J., Trepman E., Folkman J. Cell-shape and phenotypic-expression in chondrocytes. Proc Soc Exp Biol Med 1983, 172.
52. Gobbi A., Kon E., Berruto M., Francisco R., Filardo G., Marcacci M. Patellofemoral full-thickness chondral defects treated with hyalograft-C - a clinical, arthroscopic, and histologic review. Am J Sports Med 2006, 34.
53. Gobbi A., Kon E., Berruto M., Filardo G., Delcogliano M., Boldrini L., et al. Patellofemoral full-thickness chondral defects treated with second-generation autologous chondrocyte implantation. Am J Sports Med 2009, 37.
54. Guo X., Liao J., Park H., Saraf A., Raphael R.M., Tabata Y., et al. Effects of TGF-beta 3 and preculture period of osteogenic cells on the chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in a bilayered hydrogel composite. Acta Biomater 2010, 6.
55. Haasper C., Zeichen J., Meister R., Krettek C., Jagodzinski M. Tissue engineering of osteochondral constructs in vitro using bioreactors. Injury 2008, 39.
56. Haene R., Qamirani E., Story R.A., Pinsker E., Daniels T.R. Intermediate outcomes of fresh talar osteochondral allografts for treatment of large osteochondral lesions of the talus. J Bone Joint Surg Am 2012, 94A.
57. Hangody L., Karpati Z. New possibilities in the management of severe circumscribed cartilage damage in the knee (Sulyos, korulirt terdizuleti porckarosodas sebeszi kezelesenek uj lehetosege.). Magy Traumatol Ortop Kezseb Plasztikai Seb 1994, 37.
58. Harley B.A.C., Gibson L.J. In vivo and in vitro applications of collagen-GAG scaffolds. Chem Eng J 2008, 137.
59. Harris J.D., Brophy R.H., Siston R.A., Flanigan D.C. Treatment of chondral defects in the athlete's knee. Arthroscopy 2010, 26.
60. Health U S N I o. 2012. Osteochondral. In clinicaltrials.gov.
61. Heng B.C., Cao T., Lee E.H. Directing stem cell differentiation into the chondrogenic lineage in vitro. Stem Cells 2004, 22.
62. Holland T.A., Bodde E.W.H., Cuijpers V.M.J.I., Baggett L.S., Tabata Y., Mikos A.G., et al. Degradable hydrogel scaffolds for in vivo delivery of single and dual growth factors in cartilage repair. Osteoarthritis Cartilage 2007, 15.
63. Huckle J., Dootson G., Medcalf N., McTaggart S., Wright E., Carter A., et al. Differentiated chondrocytes for cartilage tissue engineering. Novartis Found Symp 2003, 249.
64. Hung C.T., Lima E.G., Mauck R.L., Taki E., LeRoux M.A., Lu H.H., et al. Anatomically shaped osteochondral constructs for articular cartilage repair. J Biomech 2003, 36.
65. Hunter D.J. Risk stratification for knee osteoarthritis progression: a narrative review. Osteoarthritis Cartilage 2009, 17.
66. Hunziker E.B., Michel M., Studer D. Ultrastructure of adult human articular cartilage matrix after cryotechnical processing. Microsc Res Tech 1997, 37.
67. Im G.-I., Lee J.H. Repair of osteochondral defects with adipose stem cells and a dual growth factor-releasing scaffold in rabbits. J Biomed Mater Res B Appl Biomater 2010, 92B.
68. In 't Anker P.S., Noort W.A., Scherjon S.A., Kleijburg-van der Keur C., Kruisselbrink A.B., van Bezooijen R.L., et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 2003, 88.
69. Jeong C.G., Zhang H., Hollister S.J. Three-dimensional polycaprolactone scaffold-conjugated bone morphogenetic protein-2 promotes cartilage regeneration from primary chondrocytes in vitro and in vivo without accelerated endochondral ossification. J Biomed Mater Res A 2012, 100A.
70. Jiang J., Tang A., Ateshian G.A., Guo X.E., Hung C.T., Lu H.H. Bioactive stratified polymer ceramic-hydrogel scaffold for integrative osteochondral repair. Ann Biomed Eng 2010, 38.
71. Johnstone B., Hering T.M., Caplan A.I., Goldberg V.M., Yoo J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998, 238.
72. Jurgens W.J., Kroeze R.J., Bank R.A., Ritt M.J.P.F., Helder M.N. Rapid attachment of adipose stromal cells on resorbable polymeric scaffolds facilitates the one-step surgical procedure for cartilage and bone tissue engineering purposes. J Orthop Res 2011, 29.
73. Kawcak C.E., McIlwraith C.W., Norrdin R.W., Park R.D., James S.P. The role of subchondral bone in joint disease: a review. Equine Vet J 2001, 33.
74. Keeney M., Pandit A. The osteochondral junction and its repair via bi-phasic tissue engineering scaffolds. Tissue Eng Part B Rev 2009, 15.
75. Khanarian N.T., Haney N.M., Burga R.A., Lu H.H. A functional agarose-hydroxyapatite scaffold for osteochondral interface regeneration. Biomaterials 2012, 33.
76. Kon E., Verdonk P., Condello V., Delcogliano M., Dhollander A., Filardo G., et al. Matrix-assisted autologous chondrocyte transplantation for the repair of cartilage defects of the knee: systematic clinical data review and study quality analysis. Am J Sports Med 2009, 37:156S-166S.
77. Kon E., Filardo G., Delcogliano M., Fini M., Salamanna F., Giavaresi G., et al. Platelet autologous growth factors decrease the osteochondral regeneration capability of a collagen-hydroxyapatite scaffold in a sheep model. BMC Musculoskelet Disord 2010, 11.
78. Langer R., Vacanti J.P. Tissue engineering. Science 1993, 260.
79. Laskin R.S. Unicompartmental tibiofemoral resurfacing arthroplasty. J Bone Joint Surg Am 1978, 60.
80. Laupattarakasem W., Laopaiboon M., Laupattarakasem P., Sumananont C. Arthroscopic debridement for knee osteoarthritis. Cochrane Database Syst Rev 2008, 10.1002/14651858.CD005118.pub2.
81. Lee D.A., Noguchi T., Frean S.P., Lees P., Bader D.L. The influence of mechanical loading on isolated chondrocytes seeded in agarose constructs. Biorheology 2000, 37.
82. Lee J-C, Lee SY, Min HJ, Han SA, Jang J, Lee S, et al. Synovium-derived mesenchymal stem cells encapsulated in a novel injectable gel can repair steochondral defects in a rabbit model. Tissue Eng Part A in press. http://dx.doi.org/10.1089/ten.TEA.2011.0643.
83. Liao C.-J., Lin Y.-J., Chiang H., Chiang S.-F., Wang Y.-H., Jiang C.-C. Injecting partially digested cartilage fragments into a biphasic scaffold to generate osteochondral composites in a nude mice model. J Biomed Mater Res A 2007, 81A.
84. Lubowitz J.H., Amhad C.H., Anderson K. All-Inside Anterior Cruciate Ligament Graft-Link Technique: Second-Generation, No-Incision Anterior Cruciate Ligament Reconstruction. Arthroscopy-the Journal of Arthroscopic and Related Surgery 2011, 27.
85. Luo Z.J., Seedhom B.B. Light and low-frequency pulsatile hydrostatic pressure enhances extracellular matrix formation by bone marrow mesenchymal cells: an in-vitro study with special reference to cartilage repair. Proc Inst Mech Eng H J Eng Med 2007, 221.
86. Madry H., van Dijk C.N., Mueller-Gerbl M. The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc 2010, 18.
87. Mahmoudifar N., Doran P.M. Tissue engineering of human cartilage and osteochondral composites using recirculation bioreactors. Biomaterials 2005, 26.
88. Mahmoudifar N., Doran P.M. Tissue engineering of human cartilage in bioreactors using single and composite cell-seeded scaffolds. Biotechnol Bioeng 2005, 91.
89. Malda J., Woodfield T.B.F., van der Vloodt F., Wilson C., Martens D.E., Tramper J., et al. The effect of PEGT/PBT scaffold architecture on the composition of tissue engineered cartilage. Biomaterials 2005, 26.
90. Marcacci M., Berruto M., Brocchetta D., Delcogliano A., Ghinelli D., Gobbi A., et al. Articular cartilage engineering with Hyalograft (R) C - 3-year clinical results. Clin Orthop Relat Res 2005.
91. Marieb E.N., Hoehn K. Structure of long bone 2009, Pearson Education, Inc. Benjamin Cummings.
92. Mauck R.L., Yuan X., Tuan R.S. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 2006, 14.
93. McNickle A.G., Provencher M.T., Cole B.J. Overview of existing cartilage repair technology. Sports Med Arthrosc 2008, 16.
94. Meachim G., Sheffield S.R. Surface ultrastructure of mature adult human articular cartilage. J Bone Joint Surg Br 1969, 51.
95. Minina E., Kreschel C., Naski M.C., Ornitz D.M., Vortkamp A. Interaction of FGF, lhh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 2002, 3.
96. Miyanishi K., Trindade M.C.D., Lindsey D.P., Beaupre G.S., Carter D.R., Goodman S.B., et al. Dose- and time-dependent effects of cyclic hydrostatic pressure on transforming growth factor-beta 3-induced chondrogenesis by adult human mesenchymal stem cells in vitro. Tissue Eng 2006, 12.
97. Mizuno S., Allemann F., Glowacki J. Effects of medium perfusion on matrix production by bovine chondrocytes in three-dimensional collagen sponges. J Biomed Mater Res 2001, 56.
98. Mohan N., Dormer N.H., Caldwell K.L., Key V.H., Berkland C.J., Detamore M.S. Continuous gradients of material composition and growth factors for effective regeneration of the osteochondral interface. Tissue Eng Part A 2011, 17.
99. Moisio K., Eckstein F., Chmiel J.S., Guermazi A., Prasad P., Almagor O., et al. Denuded subchondral bone and knee pain in persons with knee osteoarthritis. Arthritis Rheum 2009, 60.
100. Moseley J.B., O'Malley K., Petersen N.J., Menke T.J., Brody B.A., Kuykendall D.H., et al. A controlled trial of arthroscopic surgery for osteoarthritis of the knee. N Engl J Med 2002, 347.
101. Muir H., Bullough P., Maroudas A. The distribution of collagen in human articular cartilage with some of its physiological implications. J Bone Joint Surg Br 1970, 52.
102. Murray R.C., DeBowes R.M., Gaughan E.M., Zhu C.F., Athanasiou K.A. The effects of intra-articular methylprednisolone and exercise on the mechanical properties of articular cartilage in the horse. Osteoarthritis Cartilage 1998, 6.
103. Nagai T., Sato M., Kutsuna T., Kokubo M., Ebihara G., Ohta N., et al. Intravenous administration of anti-vascular endothelial growth factor humanized monoclonal antibody bevacizumab improves articular cartilage repair. Arthritis Res Ther 2010, 12.
104. Nehrer S., Chiari C., Domayer S., Barkay H., Yayon A. Results of chondrocyte implantation with a fibrin-hyaluronan matrix: a preliminary study. Clin Orthop Relat Res 2008, 466:1849-1855.
105. Neilssien T. BioMedGPS 2012, http://biomedgps.com/smarttrak-start-up-spotlight-cartiheal-ltd.
106. Noyes F.R., Stabler C.L. A system for grading articular-cartilage lesions at arthroscopy. Am J Sports Med 1989, 17.
107. Nukavarapu S.P., Amini A.R. Optimal scaffold design and effective progenitor cell identification for the regeneration of vascularized bone. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society Conference 2011.
108. Nukavarapu S., Laurencin C., Amini A. Method of making gradient porous polymer structures as osteochondral plugs 2012.
109. Ohyabu Y., Kida N., Kojima H., Taguchi T., Tanaka J., Uemura T. Cartilaginous tissue formation from bone marrow cells using rotating wall vessel (RWV) bioreactor. Biotechnol Bioeng 2006, 95.
110. Oliveira J.M., Rodrigues M.T., Silva S.S., Malafaya P.B., Gomes M.E., Viegas C.A., et al. Novel hydroxyapatite/chitosan bilayered scaffold for osteochondral tissue-engineering applications: scaffold design and its performance when seeded with goat bone marrow stromal cells. Biomaterials 2006, 27.
111. Ollat D., Lebel B., Thaunat M., Jones D., Mainard L., Dubrana F., et al. Mosaic osteochondral transplantations in the knee joint, midterm results of the SFA multicenter study. Orthop Traumatol Surg Res 2011, 97.
112. Ornitz D.M. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev 2005, 16.
113. Pearle A.D., Warren R.F., Rodeo S.A. Basic science of articular cartilage and osteoarthritis. Clin Sports Med 2005, 24.
114. Pool R.R., Meagher D.M. Pathological findings and pathogenesis of racetrack injuries. Vet Clin North Am Equine Pract 1990, 6.
115. Radin E.L., Paul I.L. Importance of bone in sparing articular cartilage from impact. Clin Orthop Relat Res 1971, 78.
116. Radin E.L., Rose R.M. Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 1986, (213):34-40.
117. Radin E.L., Paul I.L., Lowy M. A comparison of the dynamic force transmitting properties of subchondral bone and articular cartilage. J Bone Joint Surg Am 1970, 52.
118. Radin E.L., Martin R.B., Burr D.B., Caterson B., Boyd R.D., Goodwin C. Effects of mechanical loading on the tissues of the rabbit knee. J Orthop Res 1984, 2.
119. Rodrigues M.T., Lee S.J., Gomes M.E., Reis R.L., Atala A., Yoo J.J. Bilayered constructs aimed at osteochondral strategies: the influence of medium supplements in the osteogenic and chondrogenic differentiation of amniotic fluid-derived stem cells. Acta Biomater 2012, 8.
120. Sakai S., Mishima H., Ishii T., Akaogi H., Yoshioka T., Uemura T., et al. Concentration of bone marrow aspirate for osteogenic repair using simple centrifugal methods. Acta Orthop 2008, 79.
121. Schek R.M., Taboas J.M., Segvich S.J., Hollister S.J., Krebsbach P.H. Engineered osteochondral grafts using biphasic composite solid free-form fabricated scaffolds. Tissue Eng 2004, 10.
122. Schmidmaier G., Herrmann S., Green J., Weber T., Scharfenberger A., Haas N.P., et al. Quantitative assessment of growth factors in reaming aspirate, iliac crest, and platelet preparation. Bone 2006, 39.
123. Shapiro F., Flynn E., Calicchio M.L. Molecular differentiation in epiphyseal and physeal cartilage. Prominent role for gremlin in maintaining hypertrophic chondrocytes in epiphyseal cartilage. Biochem Biophys Res Commun 2009, 390.
124. Sheehy E.J., Buckley C.T., Kelly D.J. Chondrocytes and bone marrow-derived mesenchymal stem cells undergoing chondrogenesis in agarose hydrogels of solid and channelled architectures respond differentially to dynamic culture conditions. J Tissue Eng Regen Med 2011, 5.
125. Shen G. The role of type X collagen in facilitating and regulating endochondral ossification of articular cartilage. Orthod Craniofac Res 2005, 8.
126. Shukunami C., Oshima Y., Hiraki Y. Chondromodulin-I and tenomodulin: a new class of tissue-specific angiogenesis inhibitors found in hypovascular connective tissues. Biochem Biophys Res Commun 2005, 333.
127. Soltan M., Smiler D., Choi J.H. Bone marrow: orchestrated cells, cytokines, and growth factors for bone regeneration. Implant Dent 2009, 18.
128. Spahn G., Kahl E., Mueckley T., Hofmann G.O., Klinger H.M. Arthroscopic knee chondroplasty using a bipolar radiofrequency-based device compared to mechanical shaver: results of a prospective, randomized, controlled study. Knee Surg Sports Traumatol Arthrosc 2008, 16.
129. Steadman J.R., Rodkey W.G., Rodrigo J.J. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res 2001, (391 Suppl):S362-S369.
130. Steadman J.R., Briggs K.K., Rodrigo J.J., Kocher M.S., Gill T.J., Rodkey W.G. Outcomes of microfracture for traumatic chondral defects of the knee: average 11-year follow-up. Arthroscopy 2003, 19.
131. Steinert A.F., Proffen B., Kunz M., Hendrich C., Ghivizzani S.C., Noeth U., et al. Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res Ther 2009, 11.
132. Stock U.A., Vacanti J.P. Tissue engineering: current state and prospects. Annu Rev Med 2001, 52.
133. Stockwell R.A. The interrelationship of cell density and cartilage thickness in mammalian articular cartilage. J Anat 1971, 109.
134. Tang G., Zhang H., Zhao Y., Zhang Y., Li X., Yuan X. Preparation of PLGA scaffolds with graded pores by using a gelatin-microsphere template as porogen. J Biomater Sci Polym Ed 2011.
135. Turner A.S., Athanasiou K.A., Zhu C.F., Alvis M.R., Bryant H.U. Biochemical effects of estrogen on articular cartilage in ovariectomized sheep. Osteoarthritis Cartilage 1997, 5.
136. Upmeier H., Brueggenjuergen B., Weiler A., Flamme C., Laprell H., Willich S.N. Follow-up costs up to 5years after conventional treatments in patients with cartilage lesions of the knee. Knee Surg Sports Traumatol Arthrosc 2007, 15.
137. Vasita R., Katti D.S. Growth factor-delivery systems for tissue engineering: a materials perspective. Expert Rev Med Devices 2006, 3.
138. Venn M., Maroudas A. Chemical composition and swelling of normal and osteoarthrotic femoral-head cartilage.1. Chemical composition. Ann Rheum Dis 1977, 36.
139. Vinardell T., Thorpe S.D., Buckley C.T., Kelly D.J. Chondrogenesis and integration of mesenchymal stem cells within an in vitro cartilage defect repair model. Ann Biomed Eng 2009, 37.
140. Vinardell T., Sheehy E.J., Buckley C.T., Kelly D.J. A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources. Tissue Eng Part A 2012, 18.
141. Volk S.W., Luvalle P., Leask T., Leboy P.S. A BMP responsive transcriptional region in the chicken type X collagen gene. J Bone Miner Res 1998, 13.
142. Vondermark K., Gauss V., Vondermark H., Muller P. Relationship between cell-shape and type of collagen synthesized as chondrocytes lose their cartilage phenotype in culture. Nature 1977, 267.
143. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273.
144. Vunjak-Novakovic G., Meinel L., Altman G., Kaplan D. Bioreactor cultivation of osteochondral grafts. Orthod Craniofac Res 2005, 8.
145. Wagner D.R., Lindsey D.P., Li K.W., Tummala P., Chandran S.E., Smith R.L., et al. Hydrostatic pressure enhances chondrogenic differentiation of human bone marrow stromal cells in osteochondrogenic medium. Ann Biomed Eng 2008, 36.
146. Wang X., Wenk E., Zhang X., Meinel L., Vunjak-Novakovic G., Kaplan D.L. Growth factor gradients via microsphere delivery in biopolymer scaffolds for osteochondral tissue engineering. J Control Release 2009, 134.
147. Wang L., Zhao L., Detamore M.S. Human umbilical cord mesenchymal stromal cells in a sandwich approach for osteochondral tissue engineering. J Tissue Eng Regen Med 2011, 5.
148. Wheeless C.R. Wheeless' textbook of orthopaedics [last accessed]; 2012. http://www.wheelessonline.com/ortho/classification_of_chondral_and_osteochondral_injuries_of_the_knee.
149. Widuchowski W., Widuchowski J., Trzaska T. Articular cartilage defects: study of 25,124 knee arthroscopies. Knee 2007, 14.
150. Winter A., Breit S., Parsch D., Benz K., Steck E., Hauner H., et al. Cartilage-like gene expression in differentiated human stem cell spheroids - a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 2003, 48.
151. Yonenaga K., Nishizawa S., Fujihara Y., Asawa Y., Sanshiro K., Nagata S., et al. The optimal conditions of chondrocyte isolation and its seeding in the preparation for cartilage tissue engineering. Tissue Eng Part C Methods 2010, 16.
152. Yunos DM, Ahmad Z, Salih V, Boccaccini AR. Stratified scaffolds for osteochondral tissue engineering applications: electrospun PDLLA nanofibre coated Bioglass®-derived foams. J Biomater Appl in press.
153. Zhou J., Xu C., Wu G., Cao X., Zhang L., Zhai Z., et al. In vitro generation of osteochondral differentiation of human marrow mesenchymal stem cells in novel collagen-hydroxyapatite layered scaffolds. Acta Biomater 2011, 7.