Bone grafts and bone graft substitutes in orthopaedic trauma surgery: A critical analysis

Journal of Bone and Joint Surgery

Volumn 89, Issue 3, 2007, Pages 649-658

  De Long, William G ^a   Einhorn, Thomas A ^b   Koval, Kenneth ^c   McKee, Michael ^d   Smith, Wade ^e   Sanders, Roy ^f   Watson, Tracy ^g  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^c DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^d ST MICHAEL'S HOSPITAL   (Canada)

^e DENVER HEALTH MEDICAL CENTER   (United States)

^f FLORIDA ORTHOPAEDIC INSTITUTE   (United States)

^g SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIAL; BONE CEMENT; BONE MORPHOGENETIC PROTEIN; CALCIUM PHOSPHATE; COLLAGEN DERIVATIVE; HYDROXYAPATITE; RECOMBINANT PROTEIN;

ALLOGRAFT; BONE CONDUCTION; BONE DEMINERALIZATION; BONE GRAFT; BONE MATRIX; CELL DIFFERENTIATION; CELL LINE; CERAMICS; COMPOSITE GRAFT; HUMAN; INJURY; MESENCHYME CELL; MITOGENESIS; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 33847651887     PISSN: 00219355     EISSN: None     Source Type: Journal    
DOI: 10.2106/00004623-200703000-00026     Document Type: Review

References (74)

1. Urist MR. Bone transplants and implants. In: Urist MR, editor. Fundamental and clinical bone physiology. Philadelphia: Lippincott Williams and Wilkins; 1980. p 331-68.
2. Urist MR. Bone: formation by autoinduction. Science. 1965;150:893-9.
3. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. Novel regulators of bone formation: molecular clones and activities. Science. 1988;242:1528-34.
4. Wright JG, Swiontkowski ME, Heckman JO. Introducing levels of evidence to the journal. J Bone Joint Surg Am. 2003;85:1-3.
5. Friedlaender GE. Immune responses to osteochondral allografts. Current knowledge and future directions. Clin Orthop Relat Res. 1983;174:58-68.
6. Bolander ME, Balian 6. The use of demineralized bone matrix in the repair of segmental defects. Augmentation with extracted matrix proteins and a comparison with autologous grafts. J Bone Joint Surg Am. 1986;68:1264-74.
7. Einhorn TA, Lane JM, Burstein AH, Kopman CR, Vigorita VJ. The healing of segmental bone defects induced by demineralized bone matrix. A radiographic and biomechanical study. J Bone Joint Surg Am. 1984;66:274-9.
8. Upton J, Boyajian M, Mulliken JB, Glowacki J. The use of demineralized xenogeneic bone implants to correct phalangeal defects: a case report. J Hand Surg [Am]. 1984;9:388-91.
9. Mulliken JB, Glowacki J, Kaban LB, Folkman J, Murray JE. Use of demineralized allogeneic bone implants for the correction of maxillocraniofacial deformities. Ann Surg. 1981;194:366-72.
10. Tiedeman JJ, Garvin KL, Kile TA, Connolly JF. The role of a composite, demineralized bone matrix and bone marrow in the treatment of osseous defects, Orthopedics. 1995;18:1153-8.
11. Cammisa FP Jr, Lowery G, Garfin SR, Geister FH, Klara PM, McGuire RA, Sassard WR, Stubbs H, Block JE. Two-year fusion rate equivalency between Grafton DBM gel and autograft in posterolateral spine fusion: a prospective controlled trial employing side-by-side comparison in the same patient. Spine. 2004;29:660-6.
12. Peterson B, Whang PG, Iglesias R, Wang JC, Lieberman JR. Osteoinductivity of commercially available demineralized bone matrix. Preparations in a spine fusion model. J Bone Joint Surg Am. 2004;86:2243-50.
13. Johnson EE, Urist MR, Finerman GA. Bone morphogenetic protein augmentation grafting of resistant femoral nonunions. A preliminary report. Clin Orthop Relat Res. 1988;230:257-65.
14. Friedlaender GE, Perry CR, Cole JD, Cook SD, Cierny G, Muschler GF, Zych GA, Calhoun JH, LaForte AJ, Yin S. Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J Bone Joint Surg Am. 2001;83 Suppl 1(Pt 2):S151-8.
15. Govender S, Csimma C, Genant HK, Valentin-Opran A, Amirt V, Arbel R, Aro H, Atar O, Bishay M, Borner MG, Chiron P Choong P Cinats J, Coutenay B, Feibel R, Geulette B, Gravel C, Haas N, Raschke M, Hammacher E, van der Velde D, Hardy P, Holt M, Josten C, Ketterl RL, Lindeque B, Lob G, Mathevon H, McCoy G, Marsh D, Miller R, Munting E, Oevre S, Nordsletten L, Patel A, Pohl A, Rennie W, Reynders P, Rommens PM, Rondia J, Rossouw WC, Daneel PJ, Ruff S, Ruter A, Santavirta S, Schildhauer TA, Gekle C, Schnettter R, Segal O, Seiler H, Snowdowne RB, Stapert J, Taglang G, Verdonk R, Vogels L, Weckbah A, Wentzensen A, Wisniewski T; BMP-2 Evaluation in Surgery for Tibial Trauma (BESTT) Study Group. Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients. J Bone Joint Surg Am. 2002;84:2123-34.
16. McKee MD, Schemitsch EH, Waddell JP, Kreder HJ, Stephen DJG, Leighton RK, Buckley RE, Powell JN, Wild LM, Blachut PA, O'Brien PJ, Pirani S, McCormack RG; the Canadian Orthopaedic Trauma Society. The effect of human recombinant bone morphogenic protein (rhBMP-7) on the healing of open tibial shaft fractures: results of a multi-center, prospective, randomized clinical trial. In: Proceedings of the 18th Annual Meeting of the Orthopaedic Trauma Association: 2002 Oct 11-13; Toronto, Ontario, Canada, p 157-8.
17. Boyce T, Edwards J, Scarborough N. Allograft bone. The influence of processing on safety and performance. Orthop Clin North Am. 1999;30:571-81.
18. Enneking WF, Campanacci DA. Retreived human allografts: a clinicopathological study. J Bone Joint Surg Am. 2001;83:971-86.
19. Enneking WF, Mindell ER. Observations on massive retrieved human allografts. J Bone Joint Surg Am. 1991;73:1123-42.
20. Hofer S, Leopold SS, Jacobs J. Clinical perspectives on the use of bone graft based on allografts. In: Laurencin CT, editor. Bone graft substitutes. West Conshohocken, PA: ASTM International; 2003. p 68-95.
21. Van Houwelingen AP, McKee MD. Treatment of osteopenic humeral shaft nonunion with compression plating, humeral cortical allograft struts, and bone grafting. J Orthop Trauma. 2005;19:36-42.
22. Hornicek FJ, Zych GA, Hutson JJ, Malinin TI. Salvage of humeral nonunions with onlay bone plate allograft augmentation. Clin Orthop Relat Res. 2001; 386:203-9.
23. Haddad FS, Duncan CP, Berry DJ, Lewallen DG, Gross AE, Chandler HP. Periprosthetic femoral fractures around welt-fixed implants: use of cortical onlay allografts with or without a plate. J Bone Joint Surg Am. 2002;84;945-50.
24. Wang JW, Weng LH. Treatment of distal femoral nonunion with internal fixation, cortical allograft struts, and autogenous bone-grafting. J Bone Joint Surg Am. 2003;85:436-40.
25. Herrera M, Chapman CB, Roh M, Strauch RJ, Rosenwasser MP. Treatment of unstable distal radius fractures with cancellous allograft and external fixation. J Hand Surg [Am]. 1999;24:1269-78.
26. Bauer TW, Smith ST. Bioactive materials in orthopaedic surgery: overview and regulatory considerations. Clin Orthop Relat Res. 2002;395:11-22.
27. Shors EC. The development of coralline porous ceramic bone graft substitutes. In: Laurencin CT, editor. Bone graft substitutes. West Conshohocken, PA: ASTM International; 2003. p 271-88.
28. Kuhne JH, Bartl R, Frisch B, Hammer C, Jansson V, Zimmer M. Bone formation in coralline hydroxyapatite. Effects of pore size studied in rabbits. Acta Orthop Scand. 1994;65:246-52.
29. Nakahara H, Goldberg VM, Caplan AI. Culture-expanded periosteal-derived cells exhibit osteochondrogenic potential in porous calcium phosphate ceramics in vivo. Clin Orthop Relat Res. 1992;276:291-8.
30. Ripamonti U. Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials. 1996;17:31-5.
31. Gosain AK, Song L, Riordan P, Amarante MT, Nagy PG, Wilson CR, Toth JM, Ricci JL. A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model: part I. Plast Reconstr Surg. 2002;109:619-30.
32. Knaack D, Goad ME, Aiolova M, Rey C, Tofighi A, Chakravarthy P Lee DD. Resorbable calcium phosphate bone substitute. J Biomed Mater Res. 1998;43:399-409.
33. Wiltfang J, Merten HA, Schlegel KA, Schultze-Mosgau S, Kloss FR, Rupprecht S, Kessler P. Degradation characteristics of alpha and beta tri-calcium-phosphate (TCP) in minipigs. J Biomed Mater Res. 2002;63:115-21.
34. Szpalski M, Gunzburg R. Applications of calcium phosphate-based cancellous bone void fillers in trauma surgery. Orthopedics. 2002;25(5 Suppl):s601-9.
35. Khan SN, Tomin E, Lane JM. Clinical applications of bone graft substitutes. Orthop Clin North Am. 2000;31:389-98.
36. Bucholz RW, Carlton A, Holmes R. Interporous hydroxyapatite as a bone graft substitute in tibial plateau fractures. Clin Orthop Relat Res. 1989;240:53-62.
37. Cameron HU. Tricalcium phosphate as a bone graft substitute. Contemp Orthop. 1992;25:506-8.
38. McAndrew MP, Gorman PW, Lange TA. Tricalcium phosphate as a bone graft substitute in trauma: preliminary report. J Orthop Trauma. 1988;2:333-9.
39. Bucholz RW, Carlton A, Holmes RE. Hydroxyapatite and tricalcium phosphate bone graft substitutes. Orthop Clin North Am. 1987;18:323-34.
40. Larsson S, Bauer TW. Use of injectable calcium phosphate cement for fracture fixation: a review. Clin Orthop Relat Res. 2002;395:23-32.
41. Kopylov P, Runnqvist K, Jonsson K, Aspenberg P. Norian SRS versus external fixation in redisplaced distal radial fractures. A randomized study in 40 patients. Acta Orthop Scand. 1999;70:1-5.
42. Zimmermann R, Gabl M, Lutz M, Angermann P, Gschwentner M, Pechlaner S. Injectable calcium phosphate bone cement Norian SRS for the treatment of intra-articular compression fractures of the distal radius in osteoporotic women. Arch Orthop Trauma Surg. 2003;123:22-7.
43. Cassidy C, Jupiter JS, Cohen M, Delli-Santi M, Fennell C, Leinberry C, Husband J, Ladd A, Seitz WR, Constanz B. Norian SRS cement compared with conventional fixation in distal radial fractures. A randomized study. J Bone Joint Surg Am. 2003;85:2127-37.
44. Lobenhoffer P, Gerich T, Witte F, Tscherne H. Use of an injectable calcium phosphate bone cement in the treatment of tibial plateau fractures: a prospective study of twenty-six cases with twenty-month mean follow-up. J Orthop Trauma. 2002;16:143-9.
45. Horstmann WG, Verheyen CC, Leemans R. An injectable calcium phosphate cement as a bone-graft substitute in the treatment of displaced lateral tibial plateau fractures. Injury. 2003;34:141-4.
46. Schildhauer TA, Bauer TW, Josten C, Muhr G. Open reduction and augmentation of internal fixation with an injectable skeletal cement for the treatment of complex calcaneal fractures. J Orthop Trauma. 2000;14:309-17.
47. Goodman SB, Bauer TW, Carter D, Casteleyn PP, Goldstein SA, Kyle RF, Larsson S, Stankewich CJ, Swiontkowski MF, Tencer AF, Yetkinler DN, Poser RD. Norian SRS cement augmentation in hip fracture treatment. Laboratory and initial clinical results. Clin Orthop Relat Res. 1998;348:42-50.
48. Mattsson P, Larsson S. Stability of internally fixed femoral neck fractures augmented with resorbable cement. A prospective randomized study using radiostereometry. Scand J Surg. 2003;92:215-9.
49. del Real RP, Ooms E, Wolke JG, Vallet-Regi M, Jansen JA. In vivo bone response to porous calcium phosphate cement. J Biomed Mater Res A. 2003;65:30-6.
50. Herron S, Thordarson OB, Winet H, Luk A, Bao JY. Ingrowth of bone into absorbable bone cement: an in vivo microscopic evaluation. Am J Orthop. 2003;32:581-4.
51. Chapman MW, Bucholz R, Cornell C. Treatment of acute fractures with a collagen-calcium phosphate graft material. A randomized clinical trial. J Bone Joint Surg Am. 1997;79:495-502.
52. Muschler GF, Midura RJ. Connective tissue progenitors: practical concepts for clinical applications. Clin Orthop Relat Res. 2002;395:66-80.
53. Muschler GF, Nakamoto C, Griffith LG. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am. 2004;86:1541-58.
54. Muschler GF, Boehm C, Easley K. Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume. J Bone Joint Surg Am. 1997;79:1699-709.
55. Fleming JE Jr, Cornell CN, Muschler GF. Bone cells and matrices in orthopedic tissue engineering. Orthop Clin North Am. 2000;31:357-74.
56. Lindholm TS, Urist MR. A quantitative analysis of new bone formation by in-duction in compositive grafts of bone marrow and bone matrix. Clin Orthop Relat Res. 1980;150:288-300.
57. Connolly JF, Shindell R. Percutaneous marrow injection for an ununited tibia. Nebr Med J. 1986;71:105-7.
58. Connolly JF, Guse R, Tiedeman J, Dehne R. Autologous marrow injection as a substitute for operative grafting of tibial nonunions. Clin Orthop Relat Res. 1991;266:259-70.
59. Connolly J, Guse R, Lippieilo L, Dehne R. Development of an osteogenic bone-marrow preparation. J Bone Joint Surg Am. 1989;71:684-91.
60. Tiedeman JJ, Connolly JF, Strates BS, Lippieilo L. Treatment of nonunion by percutaneous injection of bone marrow and demineralized bone matrix. An experimental study in dogs. Clin Orthop Relat Res. 1991;268:294-302.
61. Bruder SC Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am. 1998;80:985-96.
62. Lane JM, Yasko AW, Tomin E, Cole BJ, Waller S, Browne M, Turek T, Gross J. Bone marrow and recombinant human bone morphogenetic protein-2 in osseous repair. Clin Orthop Relat Res. 1999;361:216-27.
63. den Boer FC, Wippermann BW, Blokhuis TJ, Patka P, Bakker FC, Haarman HJ. Healing of segmental bone defects with granular porous hydroxyapatite augmented with recombinant human osteogenic protein-1 or autologous bone marrow. J Orthop Res. 2003;21:521-28.
64. Muschler GF, Nitto H, Matsukura Y, Boehm C, Valdevit A, Kambic H, Davros W, Powell K, Easley K. Spine fusion using cell matrix composites enriched in bone marrow-derived cells. Clin Orthop Relat Res. 2003;407:102-18.
65. Banwart JC, Asher MA, Hassanein RS. Iliac crest bone graft harvest donor site morbidity. A statistical evaluation. Spine. 1995;20:1055-60.
66. Connolly JF. Clinical use of marrow osteoprogenitor cells to stimulate osteogenesis. Clin Orthop Relat Res. 1998;355 Suppl:S257-66.
67. Garg NK, Gaur S, Sharma S. Percutaneous autogenous bone marrow grafting in 20 cases of ununited fracture. Acta Orthop Scand. 1993;64:671-2.
68. Healey JH, Zimmerman PA, McDonnell JM, Lane JM. Percutaneous bone marrow grafting of delayed union and nonunion in cancer patients. Clin Orthop Relat Res. 1990;256:280-5.
69. Wientroub S, Goodwin D, Khermosh O, Salama R. The clinical use of autologous marrow to improve osteogenic potential of bone grafts in pediatric orthopedics. J Pediatr Orthop, 1989;9:186-90.
70. Goel A, Sangwan SS, Siwach RC, Ali AM. Percutaneous bone marrow grafting for the treatment of tibial non-union. Injury. 2005;36:203-6.
71. Hernigou P, Poignard A, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Joint Surg Am. 2005;87:1430-7.
72. Slater M. Patava J, Kingham K, Mason RS. Involvement of platelets in stim lating osteogenic activity. J Orthop Res. 1995;13:655-63.
73. Marx RE, Carlson ER, Eichstaedt RM, Schimmele SR, Strauss JE, Georgeo KR. Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surf Oral Med Oral Pathol Oral Radiol Endod. 1998;85:638-46.
74. Bibbo C, Bono CM, Lin SS. Union rates using autologous platelet concent alone and with bone graft in high-risk foot and ankle surgery patients. J Surg thop Adv. 2005;14:17-22.