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Published in: Clinical Orthopaedics and Related Research® 8/2008

01-08-2008 | Symposium: New Approaches to Allograft Transplantation

Chondrocyte Apoptosis: Implications for Osteochondral Allograft Transplantation

Authors: Hubert T. Kim, MD, PhD, Margie S. Teng, BS, Alexis C. Dang, MD

Published in: Clinical Orthopaedics and Related Research® | Issue 8/2008

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Abstract

Osteochondral allograft transplantation is a useful technique to manage larger articular cartilage injuries. One factor that may compromise the effectiveness of this procedure is chondrocyte cell death that occurs during the storage, preparation, and implantation of the osteochondral grafts. Loss of viable chondrocytes may negatively affect osteochondral edge integration and long-term function. A better understanding of the mechanisms responsible for chondrocyte loss could lead to interventions designed to decrease cell death and improve results. Recent studies indicate that apoptosis, or programmed cell death, is responsible for much of the chondrocyte death associated with osteochondral allograft transplantation. Theoretically, some of these cells can be rescued by blocking important apoptotic mediators. We review the role of apoptosis in cartilage degeneration, focusing on apoptosis associated with osteochondral transplantation. We also review the pathways thought to be responsible for regulating chondrocyte apoptosis, as well as experiments testing inhibitors of the apoptotic pathway. These data suggest that key contributors to the apoptotic process can be manipulated to enhance chondrocyte survival. This knowledge may lead to better surgical outcomes for osteochondral transplantation.
Literature
1.
go back to reference Aigner T, Hemmel M, Neureiter D, Gebhard PM, Zeiler G, Kirchner T, McKenna L. Apoptotic cell death is not a widespread phenomenon in normal aging and osteoarthritis human articular knee cartilage: a study of proliferation, programmed cell death (apoptosis), and viability of chondrocytes in normal and osteoarthritic human knee cartilage. Arthritis Rheum. 2001;44:1304–1312.PubMedCrossRef Aigner T, Hemmel M, Neureiter D, Gebhard PM, Zeiler G, Kirchner T, McKenna L. Apoptotic cell death is not a widespread phenomenon in normal aging and osteoarthritis human articular knee cartilage: a study of proliferation, programmed cell death (apoptosis), and viability of chondrocytes in normal and osteoarthritic human knee cartilage. Arthritis Rheum. 2001;44:1304–1312.PubMedCrossRef
2.
go back to reference Aizawa T, Kon T, Einhorn TA, Gerstenfeld LC. Induction of apoptosis in chondrocytes by tumor necrosis factor-alpha. J Orthop Res. 2001;19:785–96.PubMedCrossRef Aizawa T, Kon T, Einhorn TA, Gerstenfeld LC. Induction of apoptosis in chondrocytes by tumor necrosis factor-alpha. J Orthop Res. 2001;19:785–96.PubMedCrossRef
3.
go back to reference Asada S, Fukuda K, Nishisaka F, Matsukawa M, Hamanisi C. Hydrogen peroxide induces apoptosis of chondrocytes; involvement of calcium ion and extracellular signal-regulated protein kinase. Inflamm Res. 2001;50:19–23.PubMedCrossRef Asada S, Fukuda K, Nishisaka F, Matsukawa M, Hamanisi C. Hydrogen peroxide induces apoptosis of chondrocytes; involvement of calcium ion and extracellular signal-regulated protein kinase. Inflamm Res. 2001;50:19–23.PubMedCrossRef
4.
go back to reference Baars DC, Rundell SA, Haut RC. Treatment with the non-ionic surfactant poloxamer P188 reduces DNA fragmentation in cells from bovine chondral explants exposed to injurious unconfined compression. Biomechan Model Mechanbiol. 2006;5:133–139.CrossRef Baars DC, Rundell SA, Haut RC. Treatment with the non-ionic surfactant poloxamer P188 reduces DNA fragmentation in cells from bovine chondral explants exposed to injurious unconfined compression. Biomechan Model Mechanbiol. 2006;5:133–139.CrossRef
5.
go back to reference Ball ST, Amiel D, Williams SK, Tontz W, Chen AC, Sah RL, Bugbee WD. The effects of storage on fresh human osteochondral allografts. Clin Orthop Relat Res. 2004;418:246–252.PubMedCrossRef Ball ST, Amiel D, Williams SK, Tontz W, Chen AC, Sah RL, Bugbee WD. The effects of storage on fresh human osteochondral allografts. Clin Orthop Relat Res. 2004;418:246–252.PubMedCrossRef
6.
go back to reference Blanco FJ, Ochs RL, Schwarz H, Lotz M. Chondrocyte apoptosis induced by nitric oxide. Am J Pathol. 1995;146:75–85.PubMed Blanco FJ, Ochs RL, Schwarz H, Lotz M. Chondrocyte apoptosis induced by nitric oxide. Am J Pathol. 1995;146:75–85.PubMed
7.
go back to reference Blanco FJ, Guitian R, Vázquez-Martul E, de Toro FJ, Galdo F. Osteoarthritis chondrocytes die by apoptosis. A possible pathway for osteoarthritis pathology. Arthritis Rheum. 1998;41:284–289.PubMedCrossRef Blanco FJ, Guitian R, Vázquez-Martul E, de Toro FJ, Galdo F. Osteoarthritis chondrocytes die by apoptosis. A possible pathway for osteoarthritis pathology. Arthritis Rheum. 1998;41:284–289.PubMedCrossRef
8.
go back to reference Borazjani BH, Chen AC, Bae WC, Patil S, Sah RL, Firestein GS, Bugbee WD. Effect of impact on chondrocyte viability during insertion of human osteochondral grafts. J Bone Joint Surg Am. 2006;88:1934–1943.PubMedCrossRef Borazjani BH, Chen AC, Bae WC, Patil S, Sah RL, Firestein GS, Bugbee WD. Effect of impact on chondrocyte viability during insertion of human osteochondral grafts. J Bone Joint Surg Am. 2006;88:1934–1943.PubMedCrossRef
9.
go back to reference Cao L, Lee V, Adams ME, Kiani C, Zhang Y, Hu W, Yang BB. Beta-integrin-collagen interaction reduces chondrocyte apoptosis. Matrix Biol. 1999;18:343–355.PubMedCrossRef Cao L, Lee V, Adams ME, Kiani C, Zhang Y, Hu W, Yang BB. Beta-integrin-collagen interaction reduces chondrocyte apoptosis. Matrix Biol. 1999;18:343–355.PubMedCrossRef
10.
go back to reference Cao L, Yang BB. Chondrocyte apoptosis induced by aggrecan G1 domain as a result of decreased cell adhesion. Exp Cell Res. 1999;246:527–537.PubMedCrossRef Cao L, Yang BB. Chondrocyte apoptosis induced by aggrecan G1 domain as a result of decreased cell adhesion. Exp Cell Res. 1999;246:527–537.PubMedCrossRef
11.
go back to reference Costouros JG, Dang AC, Kim HT. Inhibition of chondrocyte apoptosis in vivo following osteochondral injury. Osteoarthritis Cartilage. 2003;11:756–759.PubMedCrossRef Costouros JG, Dang AC, Kim HT. Inhibition of chondrocyte apoptosis in vivo following osteochondral injury. Osteoarthritis Cartilage. 2003;11:756–759.PubMedCrossRef
12.
go back to reference Costouros JG, Dang AC, Kim HT. Comparison of chondrocyte apoptosis in vivo and in vitro following acute osteochondral injury. J Orthop Res. 2004;22:678–683.PubMedCrossRef Costouros JG, Dang AC, Kim HT. Comparison of chondrocyte apoptosis in vivo and in vitro following acute osteochondral injury. J Orthop Res. 2004;22:678–683.PubMedCrossRef
13.
go back to reference Dang AC, Warren A, Kim HT. Beneficial effects of intra-articular caspase inhibition therapy following osteochondral injury. Osteoarthritis Cartilage. 2006;14:526–532.PubMedCrossRef Dang AC, Warren A, Kim HT. Beneficial effects of intra-articular caspase inhibition therapy following osteochondral injury. Osteoarthritis Cartilage. 2006;14:526–532.PubMedCrossRef
14.
go back to reference D’Lima DD, Hashimoto S, Chen PC, Colwell CW Jr, Lotz MK. Human chondrocyte apoptosis in response to mechanical injury. Osteoarthritis Cartilage. 2001;9:712–719.PubMedCrossRef D’Lima DD, Hashimoto S, Chen PC, Colwell CW Jr, Lotz MK. Human chondrocyte apoptosis in response to mechanical injury. Osteoarthritis Cartilage. 2001;9:712–719.PubMedCrossRef
15.
go back to reference D’Lima DD, Hashimoto S, Chen PC, Lotz MK, Colwell CW Jr. In vitro and in vivo models of cartilage injury. J Bone Joint Surg Am. 2001;83(Suppl 2 Pt 1):22–24.PubMed D’Lima DD, Hashimoto S, Chen PC, Lotz MK, Colwell CW Jr. In vitro and in vivo models of cartilage injury. J Bone Joint Surg Am. 2001;83(Suppl 2 Pt 1):22–24.PubMed
16.
go back to reference D’Lima DD, Hashimoto S, Chen PC, Lotz MK, Colwell CW Jr. Prevention of chondrocyte apoptosis. J Bone Joint Surg Am. 2001;83(Suppl 2 Pt 1):25–26.PubMed D’Lima DD, Hashimoto S, Chen PC, Lotz MK, Colwell CW Jr. Prevention of chondrocyte apoptosis. J Bone Joint Surg Am. 2001;83(Suppl 2 Pt 1):25–26.PubMed
17.
go back to reference D’Lima D, Hermida J, Hashimoto S, Colwell C, Lotz M. Caspase inhibitors reduce severity of cartilage lesions in experimental osteoarthritis. Arthritis Rheum. 2006;54:1814–1821.PubMedCrossRef D’Lima D, Hermida J, Hashimoto S, Colwell C, Lotz M. Caspase inhibitors reduce severity of cartilage lesions in experimental osteoarthritis. Arthritis Rheum. 2006;54:1814–1821.PubMedCrossRef
18.
go back to reference Evans PJ, Miniaci A, Hurtig MB. Manual punch versus power harvesting of osteochondral grafts. Arthroscopy. 2004;20:306–310.PubMedCrossRef Evans PJ, Miniaci A, Hurtig MB. Manual punch versus power harvesting of osteochondral grafts. Arthroscopy. 2004;20:306–310.PubMedCrossRef
19.
go back to reference Frankfurt OS, Krishan A. Identification of apoptotic cells by formamide-induced DNA denaturation in condensed chromatin. J Histochem Cytochem. 2001;49:369–378.PubMed Frankfurt OS, Krishan A. Identification of apoptotic cells by formamide-induced DNA denaturation in condensed chromatin. J Histochem Cytochem. 2001;49:369–378.PubMed
20.
go back to reference Green DM, Noble PC, Ahuero JS, Birdsall HH. Cellular events leading to chondrocyte death after cartilage impact injury. Arthritis Rheum. 2006;54:1509–1517.PubMedCrossRef Green DM, Noble PC, Ahuero JS, Birdsall HH. Cellular events leading to chondrocyte death after cartilage impact injury. Arthritis Rheum. 2006;54:1509–1517.PubMedCrossRef
21.
go back to reference Gross AE, Shasha N, Aubin P. Long-term followup of the use of fresh osteochondral allografts for posttraumatic knee defects. Clin Orthop Relat Res. 2005;435:79–87.PubMedCrossRef Gross AE, Shasha N, Aubin P. Long-term followup of the use of fresh osteochondral allografts for posttraumatic knee defects. Clin Orthop Relat Res. 2005;435:79–87.PubMedCrossRef
22.
go back to reference Hashimoto S, Ochs RL, Komiya S, Lotz M. Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis. Arthritis Rheum. 1998;41:1632–1638.PubMedCrossRef Hashimoto S, Ochs RL, Komiya S, Lotz M. Linkage of chondrocyte apoptosis and cartilage degradation in human osteoarthritis. Arthritis Rheum. 1998;41:1632–1638.PubMedCrossRef
23.
go back to reference Hashimoto S, Takahashi K, Amiel D, Coutts RD, Lotz M. Chondrocyte apoptosis and nitric oxide production during experimentally induced osteoarthritis. Arthritis Rheum. 1998;417:1266–1274.CrossRef Hashimoto S, Takahashi K, Amiel D, Coutts RD, Lotz M. Chondrocyte apoptosis and nitric oxide production during experimentally induced osteoarthritis. Arthritis Rheum. 1998;417:1266–1274.CrossRef
24.
go back to reference Hirsch MS, Lunsford LE, Trinkaus-Randall V, Svoboda KK. Chondrocyte survival and differentiation in situ are integrin mediated. Dev Dyn. 1997;210:249–263.PubMedCrossRef Hirsch MS, Lunsford LE, Trinkaus-Randall V, Svoboda KK. Chondrocyte survival and differentiation in situ are integrin mediated. Dev Dyn. 1997;210:249–263.PubMedCrossRef
25.
go back to reference Huntley JS, Bush PG, McBernie JM, Simpson AH, Hall AC. Chondrocyte death associate with femoral osteochondral harvest as performed for mosaicplasty. J Bone Joint Surg Am. 2005;87:351–360.PubMedCrossRef Huntley JS, Bush PG, McBernie JM, Simpson AH, Hall AC. Chondrocyte death associate with femoral osteochondral harvest as performed for mosaicplasty. J Bone Joint Surg Am. 2005;87:351–360.PubMedCrossRef
26.
go back to reference Islam N, Haqqi TM, Jepsen KJ, Kraay M, Welter JF, Goldberg VM, Malemud CJ. Hydrostatic pressure induces apoptosis in human chondrocytes from osteoarthritic cartilage through up-regulation of tumor necrosis factor-alpha, inducible nitric oxide synthase, p53, c-myc, and bax-alpha, and suppression of bcl-2. J Cell Biochem. 2002;87:266–278.PubMedCrossRef Islam N, Haqqi TM, Jepsen KJ, Kraay M, Welter JF, Goldberg VM, Malemud CJ. Hydrostatic pressure induces apoptosis in human chondrocytes from osteoarthritic cartilage through up-regulation of tumor necrosis factor-alpha, inducible nitric oxide synthase, p53, c-myc, and bax-alpha, and suppression of bcl-2. J Cell Biochem. 2002;87:266–278.PubMedCrossRef
27.
go back to reference Jamali AA, Hatcher SL, You Z. Donor cell survival in a fresh osteochondral allograft at twenty-nine years. A case report. J Bone Joint Surg Am. 2007;89:166–169.PubMedCrossRef Jamali AA, Hatcher SL, You Z. Donor cell survival in a fresh osteochondral allograft at twenty-nine years. A case report. J Bone Joint Surg Am. 2007;89:166–169.PubMedCrossRef
28.
go back to reference Kim HA, Lee YJ, Seong SC, Choe KW, Song YW. Apoptotic chondrocyte death in human osteoarthritis. J Rheumatol. 2000;27:455–462.PubMed Kim HA, Lee YJ, Seong SC, Choe KW, Song YW. Apoptotic chondrocyte death in human osteoarthritis. J Rheumatol. 2000;27:455–462.PubMed
29.
go back to reference Kim HT, Lo M, Pillarisetty R. Chondrocyte apoptosis following intra-articular fracture in humans. Osteoarthritis Cartilage. 2002;10:747–749.PubMedCrossRef Kim HT, Lo M, Pillarisetty R. Chondrocyte apoptosis following intra-articular fracture in humans. Osteoarthritis Cartilage. 2002;10:747–749.PubMedCrossRef
30.
go back to reference Lee MS, Trindade MC, Ikenoue T, Goodman SB, Schurman DJ, Smith RL. Regulation of nitric oxide and bcl-2 expression by shear stress in human osteoarthritic chondrocytes in vitro. J Cell Biochem. 2003;90:80–86.PubMedCrossRef Lee MS, Trindade MC, Ikenoue T, Goodman SB, Schurman DJ, Smith RL. Regulation of nitric oxide and bcl-2 expression by shear stress in human osteoarthritic chondrocytes in vitro. J Cell Biochem. 2003;90:80–86.PubMedCrossRef
31.
go back to reference Lo MY, Kim HT. Chondrocyte apoptosis induced by collagen degradation: inhibition by caspase inhibitors and IGF-1. J Orthop Res. 2004;22:140–144.PubMedCrossRef Lo MY, Kim HT. Chondrocyte apoptosis induced by collagen degradation: inhibition by caspase inhibitors and IGF-1. J Orthop Res. 2004;22:140–144.PubMedCrossRef
32.
go back to reference Lo MY, Kim HT. Chondrocyte apoptosis induced by hydrogen peroxide requires caspase activation but not mitochondrial pore transition. J Orthop Res. 2004;22:1120–1125.PubMedCrossRef Lo MY, Kim HT. Chondrocyte apoptosis induced by hydrogen peroxide requires caspase activation but not mitochondrial pore transition. J Orthop Res. 2004;22:1120–1125.PubMedCrossRef
33.
go back to reference Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol. 1995;146:3–15.PubMed Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol. 1995;146:3–15.PubMed
34.
go back to reference Mankin HJ, Gebhardt MC, Jennings LC, Springfield DS, Tomford WW. Long-term results of allograft replacement in the management of bone tumors. Clin Orthop Relat Res. 1996;324:86–97.PubMedCrossRef Mankin HJ, Gebhardt MC, Jennings LC, Springfield DS, Tomford WW. Long-term results of allograft replacement in the management of bone tumors. Clin Orthop Relat Res. 1996;324:86–97.PubMedCrossRef
35.
go back to reference Matsuo M., Nishida K, Yoshida A, Murakami T, Inoue H. Expression of caspase-3 and -9 relevant to cartilage destruction and chondrocyte apoptosis in human osteoarthritic cartilage. Acta Med Okayama. 2001;55:333–340.PubMed Matsuo M., Nishida K, Yoshida A, Murakami T, Inoue H. Expression of caspase-3 and -9 relevant to cartilage destruction and chondrocyte apoptosis in human osteoarthritic cartilage. Acta Med Okayama. 2001;55:333–340.PubMed
36.
go back to reference Maury AC, Safir O, Heras FL, Pritzker KP, Gross AE. Twenty-five-year chondrocyte viability in fresh osteochondral allograft. A case report. J Bone Joint Surg Am. 2007;89:159–165.PubMedCrossRef Maury AC, Safir O, Heras FL, Pritzker KP, Gross AE. Twenty-five-year chondrocyte viability in fresh osteochondral allograft. A case report. J Bone Joint Surg Am. 2007;89:159–165.PubMedCrossRef
37.
go back to reference McCulloch PC, Kang RW, Sobhy MH, Hayden JK, Cole BJ. Prospective evaluation of prolonged fresh osteochondral allograft transplantation of the femoral condyle: minimum 2-year follow-up. Am J Sports Med. 2007;35:411–420.PubMedCrossRef McCulloch PC, Kang RW, Sobhy MH, Hayden JK, Cole BJ. Prospective evaluation of prolonged fresh osteochondral allograft transplantation of the femoral condyle: minimum 2-year follow-up. Am J Sports Med. 2007;35:411–420.PubMedCrossRef
38.
go back to reference Murray MM, Zurakowski D, Vrahas MS. The death of articular chondrocytes after intra-articular fracture in humans. J Trauma. 2004;56:128–131.PubMedCrossRef Murray MM, Zurakowski D, Vrahas MS. The death of articular chondrocytes after intra-articular fracture in humans. J Trauma. 2004;56:128–131.PubMedCrossRef
39.
go back to reference Nuttall ME, Nadeau DP, Fisher PW, Wang F, Keller PM, DeWolf WE Jr, Goldring MB, Badger AM, Lee D, Levy MA, Gowen M, Lark MW. Inhibition of caspase-3-like activity prevents apoptosis while retaining functionality of human chondrocytes in vitro. J Orthop Res. 2000;18:356–363.PubMedCrossRef Nuttall ME, Nadeau DP, Fisher PW, Wang F, Keller PM, DeWolf WE Jr, Goldring MB, Badger AM, Lee D, Levy MA, Gowen M, Lark MW. Inhibition of caspase-3-like activity prevents apoptosis while retaining functionality of human chondrocytes in vitro. J Orthop Res. 2000;18:356–363.PubMedCrossRef
40.
go back to reference Pelletier JP, Jovanovic DV, Lascau-Coman V, Fernandes JC, Manning PT, Connor JR, Currie MG, Martel-Pelletier J. Selective inhibition of inducible nitric oxide synthase reduces progression of experimental osteoarthritis in vivo: possible link with the reduction in chondrocyte apoptosis and caspase 3 level. Arthritis Rheum. 2000;43:1290–1299.PubMedCrossRef Pelletier JP, Jovanovic DV, Lascau-Coman V, Fernandes JC, Manning PT, Connor JR, Currie MG, Martel-Pelletier J. Selective inhibition of inducible nitric oxide synthase reduces progression of experimental osteoarthritis in vivo: possible link with the reduction in chondrocyte apoptosis and caspase 3 level. Arthritis Rheum. 2000;43:1290–1299.PubMedCrossRef
41.
go back to reference Pelletier JP, Fernandes JC, Jovanovic DV, Reboul P, Martel-Pelletier J. Chondrocyte death in experimental osteoarthritis is mediated by MEK 1/2 and p38 pathways: role of cyclooxygenase-2 and inducible nitric oxide synthase. J Rheumatol. 2001;28:2509–2519.PubMed Pelletier JP, Fernandes JC, Jovanovic DV, Reboul P, Martel-Pelletier J. Chondrocyte death in experimental osteoarthritis is mediated by MEK 1/2 and p38 pathways: role of cyclooxygenase-2 and inducible nitric oxide synthase. J Rheumatol. 2001;28:2509–2519.PubMed
42.
go back to reference Robertson CM, Allen RT, Pennock AT, Bugbee WD, Amiel D. Upregulation of apoptotic and matrix-related gene expression during fresh osteochondral allograft storage. Clin Orthop Relat Res. 2006;442:260–266.PubMedCrossRef Robertson CM, Allen RT, Pennock AT, Bugbee WD, Amiel D. Upregulation of apoptotic and matrix-related gene expression during fresh osteochondral allograft storage. Clin Orthop Relat Res. 2006;442:260–266.PubMedCrossRef
43.
go back to reference Serbest G, Horwitz J, Jost M, Barbee K. Mechanisms of cell death and neuroprotection by poloxamer 188 after mechanical trauma. FASEB J. 2006;20:308–310.PubMed Serbest G, Horwitz J, Jost M, Barbee K. Mechanisms of cell death and neuroprotection by poloxamer 188 after mechanical trauma. FASEB J. 2006;20:308–310.PubMed
44.
go back to reference Sharif M, Whitehouse A, Sharman P, Perry M, Adams M. Increased apoptosis in human osteoarthritic cartilage corresponds to reduced cell density and expression of caspase-3. Arthritis Rheum. 2004;50:507–515.PubMedCrossRef Sharif M, Whitehouse A, Sharman P, Perry M, Adams M. Increased apoptosis in human osteoarthritic cartilage corresponds to reduced cell density and expression of caspase-3. Arthritis Rheum. 2004;50:507–515.PubMedCrossRef
45.
go back to reference Stevenson S, Dannucci GA, Sharkey NA, Pool RR. The fate of articular cartilage after transplantation of fresh and cryopreserved tissue-antigen-matched and mismatched osteochondral allografts in dogs. J Bone Joint Surg Am. 1989;71:1297–1307.PubMed Stevenson S, Dannucci GA, Sharkey NA, Pool RR. The fate of articular cartilage after transplantation of fresh and cryopreserved tissue-antigen-matched and mismatched osteochondral allografts in dogs. J Bone Joint Surg Am. 1989;71:1297–1307.PubMed
46.
go back to reference Tew SR, Kwan AP, Hann A, Thomson BM, Arcerh CW. The reactions of articular cartilage to experimental wounding: role of apoptosis. Arthritis Rheum. 2000;43:215–225.PubMedCrossRef Tew SR, Kwan AP, Hann A, Thomson BM, Arcerh CW. The reactions of articular cartilage to experimental wounding: role of apoptosis. Arthritis Rheum. 2000;43:215–225.PubMedCrossRef
47.
go back to reference Wasiak J, Clar C, Villanueva E. Autologous cartilage implantation for full thickness articular cartilage defects of the knee. Cochrane Database Syst Rev. 2006;3:CD005489.PubMed Wasiak J, Clar C, Villanueva E. Autologous cartilage implantation for full thickness articular cartilage defects of the knee. Cochrane Database Syst Rev. 2006;3:CD005489.PubMed
48.
go back to reference Williams RJ 3rd, Ranawat AS, Potter HG, Carter T, Warren RF. Fresh stored allografts for the treatment of osteochondral defects of the knee. J Bone Joint Surg Am. 2007;89:718–726.PubMedCrossRef Williams RJ 3rd, Ranawat AS, Potter HG, Carter T, Warren RF. Fresh stored allografts for the treatment of osteochondral defects of the knee. J Bone Joint Surg Am. 2007;89:718–726.PubMedCrossRef
49.
go back to reference Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306.PubMedCrossRef Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306.PubMedCrossRef
50.
go back to reference Zhang Z, McCaffery JM, Spencer RGS, Francomano CA. Growth and integration of neocartilage with native cartilage in vitor. J Orthop Res. 2005;23:433–439.PubMedCrossRef Zhang Z, McCaffery JM, Spencer RGS, Francomano CA. Growth and integration of neocartilage with native cartilage in vitor. J Orthop Res. 2005;23:433–439.PubMedCrossRef
Metadata
Title
Chondrocyte Apoptosis: Implications for Osteochondral Allograft Transplantation
Authors
Hubert T. Kim, MD, PhD
Margie S. Teng, BS
Alexis C. Dang, MD
Publication date
01-08-2008
Publisher
Springer-Verlag
Published in
Clinical Orthopaedics and Related Research® / Issue 8/2008
Print ISSN: 0009-921X
Electronic ISSN: 1528-1132
DOI
https://doi.org/10.1007/s11999-008-0304-6

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