Seminars in Spine Surgery
Volume 20, Issue 4 , Pages 257-269 , December 2008

Alternatives to Autogenous Bone Graft in Revision Lumbar Spine Surgery

  • Anis O. Mekhail, MD, MS

      Affiliations

    • Department of Orthopaedic Surgery, University of Illinois at Chicago, Chicago, IL
    • Parkview Orthopaedic Group, Palos Heights, IL
  • ,
  • Gordon R. Bell, MD

      Affiliations

    • Department of Orthopaedic Surgery, Cleveland Clinic Foundation, Cleveland, OH
    • Corresponding Author InformationAddress reprint requests to Gordon R. Bell, MD, Head, Section of Spinal Surgery, Department of Orthopaedic Surgery, A-41, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195

References 

  1. Steinmann J, Herkowitz H. Pseudoarthrosis of the spine. Clin Orthop. 1992;284:80–90
  2. Cleveland M, Bosworth D, Thomson F. Pseudoarthrosis in the lumbosacral spine. J Bone Joint Surg Am. 1948;30:302–311
  3. Stauffer R, Coventry M. Posterolateral lumbar spine fusion. J Bone Joint Surg Am. 1972;54:1195–1204
  4. DePalma AF, Rothman RH. The nature of pseudoarthrosis. Clin Orthop. 1968;59:113–118
  5. West JL, Bradford DS, Oglivie JW. Results of spinal arthrodesis with pedicle screw plate fixation. J Bone Joint Surg Am. 1996;73:1179–1184
  6. Bridwell KH, Sedgewick TA, O'Brien MF, et al. The role of fusion and instrumentation in the treatment of degenerative spondylolisthesis with spinal stenosis. J Spinal Disord. 1993;6:461–472
  7. McGuire RA, Amundson GM. The use of primary internal fixation in spondylolisthesis. Spine. 1993;18:1662–1672
  8. Zdeblick TA. A prospective, randomized study of lumbar fusion: Preliminary results. Spine. 1993;18:983–991
  9. Deguchi M, Rapoff AJ, Zdeblick TA. Posterolateral fusion for isthmic spondylolisthesis in adults: analysis of fusion rate and clinical results. J Spinal Disord. 1998;11:459–464
  10. Meril AJ. Direct current stimulation of allograft in anterior and posterior lumbar interbody fusions. Spine. 1994;19:2393–2398
  11. Mooney V. A randomized double-blind prospective study of the efficacy of pulsed electromagnetic fields for interbody lumbar fusions. Spine. 1990;15:708–712
  12. Glazer PA, Heilmann MR, Lotz JC, et al. Use of electromagnetic fields in a spinal fusion: a rabbit model. Spine. 1997;22:2351–2356
  13. Banwart JC, Asher MA, Hassanein RS. Iliac crest bone graft harvest donor site morbidity (A statistical evaluation). Spine. 1995;20:1055–1060
  14. Betz RR. Limitations of autograft and allograft: new synthetic solutions. Orthopedics. 2002;25(suppl):561–570
  15. Robertson PA, Wray AC. Natural history of posterior iliac crest bone graft donation for spinal surgery: a prospective analysis of morbidity. Spine. 2001;26:1473–1476
  16. Summers BN, Eisenstein SM. Donor site pain from the ilium (A complication of lumbar spine fusion). J Bone Joint Surg Br. 1989;71:677–680
  17. Younger EM, Chapman MW. Morbidity of bone graft donor sites. J Orthop Trauma. 1989;3:192–195
  18. Boyce T, Edwards J, Scarborough N. Allograft bone (The influence of processing on safety and performance). Orthop Clin North Am. 1999;30:571–581
  19. Herron L, Newman M. The failure of ethylene oxide gas sterilized freeze-dried bone graft for thoracic and lumbar spine fusion. Spine. 1989;14:496–500
  20. Pelker R, Friedlaender G. Biomechanical aspects of bone autografts and allografts. Orthop Clin North Am. 1987;18:235–239
  21. Tomford WW. Transmission of disease through transplantation of musculoskeletal allografts. J Bone Joint Surg Am. 1995;77:1742–1754
  22. Conrad EU, Gretch DR, Obermeyer KR, et al. Transmission of the hepatitis-C virus by tissue transplantation. J Bone Joint Surg Am. 1995;77:214–224
  23. Simonds RJ, Holmberg SD, Hurwitz RL, et al. Transmission of human immunodeficiency virus type 1 from a seronegative organ and tissue donor. N Engl J Med. 1992;326:726–732
  24. Buck B, Malinin T, Brown M. Bone transplantation and human immunodeficiency virus. Clin Orthop. 1989;240:129–136
  25. Centers for Disease Control. Transmission of HIV through bone transplantation: case report and public health recommendations. JAMA. 1988;260:2487–2488
  26. Friedlaender GE. Bone allografts: the biological consequences of immunological events. J Bone Joint Surg Am. 1991;73:1119–1122
  27. Strong DM, Friedlaender GE, Tomford WW, et al. Immunologic responses in human recipients of osseous and osteochondral allografts. Clin Orthop. 1996;326:107–114
  28. Jorgenson S, Lowe T, France J, et al. A prospective analysis of autograft versus allograft in posterolateral lumbar fusion in the same patient. Spine. 1994;19:2048–2053
  29. Zdeblick T, Ducker T. The use of freeze-dried bone for anterior cervical fusions. Spine. 1991;16:726–732
  30. Martin GJ, Boden SD, Titus L, et al. New formulations of demineralized bone matrix as a more effective graft alternative in experimental posterolateral lumbar spine arthrodesis. Spine. 1999;24:637–645
  31. Lane JM, Sandhu HS. Current approaches to experimental bone grafting. Orthop Clin North Am. 1987;18:213–225
  32. Prolo DJ, Rodrigo JJ. Contemporary bone graft physiology and surgery. Clin Orthop. 1985;200:322–342
  33. Posner AS. The mineral of bone. Clin Orthop. 1985;200:87–99
  34. Ludwig SC, Boden SD. Osteoinductive bone graft substitutes for spinal fusion: a basic science summary. Orthop Clin North Am. 1999;30:635–645
  35. Aspenberg P, Wang E, Thorngren K-G. Bone morphogenetic protein induces bone in the squirrel monkey, but bone matrix does not. Acta Orthop Scand. 1992;63:619–622
  36. Martin GJ, Boden SD, Marone MA, et al. Posterolateral intertransverse process spinal arthrodesis with rhBMP-2 in a nonhuman primate: important lessons learned regarding dose, carrier, and safety. J Spinal Disord. 1999;12:179–186
  37. Boden SD, Zdeblick TA, Sandhu HS, et al. The use of rhBMP-2 in interbody fusion cages (Definitive evidence of osteoinduction in humans: a preliminary report). Spine. 2000;25:376–381
  38. Roufosse AH, Aue WP, Roberts JE, et al. Investigation of the mineral phases of bone by solid-state phosphorus-31 magic angle sample spinning nuclear magnetic resonance. Biochemistry. 1984;23:6115–6120
  39. Ohgushi H, Goldberg VM, Caplan AI. Heterotopic osteogenesis in porous ceramics induced by marrow cells. J Orthop Res. 1989;7:568–578
  40. Jarcho M. Calcium phosphate ceramics as hard tissue prosthetics. Clin Orthop. 1981;157:259–278
  41. Flattley T, Lynch K, Benson M. Tissue response to implants of calcium phosphate ceramic in the rabbit spine. Clin Orthop. 1983;179:246–252
  42. Hulbert SF, Young FA, Mathews RS, et al. Potential of ceramic materials as permanently implantable skeletal prostheses. J Biomed Mater Res. 1970;4:433–456
  43. White E, Shors EC. Biomaterial aspects of Interpore-200 porous hydroxyapatite. Dent Clin North Am. 1986;30:49–67
  44. Holmes RE, Bucholz RW, Mooney V. Porous hydroxyapatite as a bone graft substitute in diaphyseal defects: a histometric study. J Orthop Res. 1987;5:114–121
  45. Hoogendoorn HA, Renoooij W, Akkermans LMA, et al. Long-term study of large ceramic implants (porous hydroxyapatite) in dog femora. Clin Orthop. 1984;187:281–288
  46. Ferraro J. Experimental evaluation of ceramic calcium phosphate as a substitute for bone grafts. Plast Reconstr Surg. 1979;63:634–640
  47. Boden S, Martin G, Morone M, et al. Posterolateral lumbar intertransverse process spine arthrodesis with recombinant human bone morphogenetic protein-2/hydroxyapatite-tricalcium phosphate after laminectomy in the nonhuman primate. Spine. 1999;24:1179–1185
  48. Daculsi G, LeGeros R, Nery E, et al. Transformation of biphasic calcium phosphate ceramics in vivo: ultrastructural and physico-chemical characterization. J Biomed Mater Res. 1989;23:883–894
  49. Emery S, Fuller D, Stevenson S. Ceramic anterior spinal fusion (Biologic and biomechanical comparison in a canine model). Spine. 1996;21:2713–2719
  50. Guigui P, Plais P, Flautre B. Experimental model of posterolateral spinal arthrodesis in sheep (2. Application of the model: evaluation of vertebral fusion obtained with coral (Porites) or with a biphasic ceramic (Triosite)). Spine. 1994;19:2798–2803
  51. Zerwekh J, Kourosh S, Scheinberg R. Fibrillar collagen-biphasic calcium phosphate composite as a bone graft substitute for spinal fusion. J Orthop Res. 1992;10:562–572
  52. Chiroff RT, White EW, Weber KN, et al. Tissue ingrowth of Replamineform implants. J Biomed Mater Res. 1975;9:29–45
  53. Shors EC. Coralline bone graft substitutes. Orthop Clin North Am. 1999;30:599–613
  54. Bucholz R, Carlton A, Holmes R. Hydroxyapatite and tricalcium phosphate bone graft substitutes. Orthop Clin North Am. 1987;18:323–334
  55. Guillemin G, Meunier A, Dallant P. Comparison of coral resorption and bone apposition with two natural corals of different porosities. J Biomed Mater Res. 1989;23:765–779
  56. Holmes R. Bone regeneration within a coralline hydroxyapatite implant. Plast Reconstr Surg. 1979;63:626–633
  57. Holmes R, Bucholz R, Mooney V. Porous hydroxyapatite as a bone graft substitute in metaphyseal defects. J Bone Joint Surg Am. 1986;68:904–911
  58. Damien C, Christel P, Benedict J, et al. A composite of natural coral, collagen, bone protein, and basic fibroblast growth factor tested in a rat subcutaneous model. Ann Chir Gynecol. 1993;82:117–128
  59. Meadows GR. Adjunctive use of ultraporous beta-tricalcium phosphate bone void filler in spinal arthrodesis. Orthopedics. 2002;25(suppl):579–584
  60. Linovitz RJ, Peppers TA. Use of an advanced formulation of beta-tricalcium phosphate as a bone extender in interbody lumbar fusion. Orthopedics. 2002;25(suppl):485–589
  61. Gunzburg R, Szpalski M. Use of a novel beta-tricalcium phosphate-based bone void filler as a graft extender in spinal fusion surgeries. Orthopedics. 2002;25(suppl):591–595
  62. Steffen T, Marchesi D, Aebi M. Posterolateral and anterior interbody spinal fusion models in the sheep. Clin Orthop. 2000;371:28–37
  63. Spivak JM, Hasharoni A. Use of hydroxyapatite in spine surgery. Eur Spine J. 2001;10(suppl):197–204
  64. Delecrin J, Aguado E, NGuyen JM, et al. Influence of local environment on incorporation of ceramic for lumbar fusion (Comparison of laminar and intertransverse sites in a canine model). Spine. 1997;22:1683–1689
  65. Baramki H, Steffen T, Lander P, et al. The efficacy of interconnected porous hydroxyapatite in achieving posterior lumbar fusion in sheep. Spine. 2000;25:1053–1060
  66. Sidqui M, Collin P, Vitte C, et al. Osteoblast adherence and resorption activity of isolated osteoclasts on calcium sulphate hemihydrate. Biomaterials. 1995;16:1327–1332
  67. Hadjipavlou AG, Simmons JW, Tzermiadianos MN, et al. Plaster of Paris as bone substitute in spinal surgery. Eur Spine J. 2001;10(suppl 2):189–196
  68. Peltier LF. The use of plaster of Paris to fill defects in bone. Clin Orthop. 1961;21:1–31
  69. Peltier LR, Bickel EY, Lillo R, et al. The use of plaster of Paris to fill defects in bone. Ann Surg. 1957;146:61–69
  70. Cunningham BWO, Sefter JC, Buckley R, et al: An investigational study of calcium sulfate for posterolateral spinal arthrodesis—an in-vivo animal model. Presented at Scoliosis Research Society Meeting, New York, September 16-19, 1998
  71. McKee MSE, Wild L, Waddell JP. The use of antibiotic impregnated, bioabsorbable bone substitute in the treatment of infected long bone defects: results of a prospective trial. J Orthop Trauma. 2000;14:137–138
  72. Armstrong DG, Findlow AH, Oyibo SO, et al. The use of absorbable antibiotic impregnated calcium sulphate pellets in the management of diabetic foot infections. Diabet Med. 2001;18:942–943
  73. Turner TM, Urban RM, Gitelis S, et al. Radiographic and histologic assessment of calcium sulfate in experimental animal models and clinical use as a resorbable bone-graft substitute, a bone-graft expander, and a method for local antibiotic delivery (One institution's experience). J Bone Joint Surg Am. 2001;83(suppl):8–18
  74. Miclau T, Dahners LE, Lindesey RW. In vitro pharmacokinetics of antibiotic release from locally implantable materials. J Orthop Res. 1993;11:627–632
  75. Cornell CN. Osteoconductive materials and their role as substitutes for autogenous bone grafts. Orthop Clin North Am. 1999;30:591–598
  76. Parikh SN. Bone graft substitutes in modern orthopaedics. Orthopedics. 2002;25:1301–1309
  77. Cornell CN, Lane JM, Chapman M, et al. Multicenter trial of Collagraft as bone graft substitute. J Orthop Trauma. 1991;5:1–8
  78. Walsh WR, Harrison J, Loefler A, et al. Mechanical and histologic evaluation of Collagraft in an ovine lumbar fusion model. Clin Orthop. 2000;375:258–266
  79. Muschler GF, Negami S, Hyodo A, et al. Evaluation of collagen ceramic composite graft materials in a spinal fusion model. Clin Orthop. 1996;328:250–260
  80. Zerwekh JE, Kourosh S, Scheinberg R, et al. Fibrillar collagen-biphasic calcium phosphate composite as a bone graft substitute for spinal fusion. J Orthop Res. 1992;10:562–572
  81. Tay BK, Le AX, Heilman M, et al. Use of a collagen-hydroxyapatite matrix in spinal fusion (A rabbit model). Spine. 1998;23:2276–2281
  82. Kadiyala S, Lo H, Leong KW. Biodegradable polymers and synthetic bone graft in bone formation and repair. Park Ridge, IL: American Academy of Orthopaedic Surgeons Symposium; 1994;pp 317-324
  83. Urist M. Bone: formation by autoinduction. Science. 1965;150:839–899
  84. Urist M, Silverman B, Buring K, et al. The bone induction principle. Clin Orthop. 1967;53:243–283
  85. Chalmers J, Gray D, Rush J. Observations on the induction of bone in soft tissues. J Bone Joint Surg Br. 1975;57:29–45
  86. Van Der Putte K, Urist M. Osteogenesis of the interior of intramuscular implants of decalcified bone matrix. Clin Orthop. 1965;43:257–270
  87. Wang EA, Israel D, Kelly S, et al. Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors. 1993;9:57–71
  88. Boden SD. Overview of the biology of lumbar spine fusion and principles for selecting a bone graft substitute. Spine. 2002;27(16S):S26–S31
  89. Finkemeier CG. Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am. 2002;84:454–464
  90. Sandhu HS, Grewal HS, Parvataneni H. Bone grafting for spinal fusion. Orthop Clin North Am. 1999;30:685–698
  91. Fleming JE, Cornell CN, Muschler GF. Bone cells and matrices in orthopedic tissue engineering. Orthop Clin North Am. 2000;31:357–374
  92. Morone MA, Boden SD. Experimental posterolateral lumbar spinal fusion with demineralized bone matrix gel. Spine. 1998;23:159–167
  93. Buring K, Urist MR. Effects of ionizing radiation on the bone induction principle in the matrix of bone implants. Clin Orthop. 1967;55:225–234
  94. Aspenberg P, Johnson E, Thorngren KG. Dose-dependent reduction of bone inductive properties by ethylene oxide. J Bone Joint Surg Br. 1990;72:1036–1037
  95. Schwartz Z, Mellonin JT, Carnes DL, et al. Ability of commercial demineralized freeze-dried bone allograft to induce new bone formation. J Periodontol. 1996;67:918–926
  96. Schwartz Z, Somers A, Mellonig JT, et al. Ability of commercial demineralized freeze-dried bone allograft to induce new bone formation is dependent upon donor age but not gender. J Periodontol. 1998;69:470–478
  97. Peterson B, Whang PG, Iglesias R, et al. Osteoinductivity of commercially available demineralized bone matrix preparations in a spine fusion model. J Bone Joint Surg Am. 2004;86:2243–2250
  98. Bostrom MP, Yang X, Kennan M, et al. An unexpected outcome during testing of commercially available demineralized bone graft materials: how safe are the nonallograft components?. Spine. 2001;26:1425–1428
  99. Wang JC, Kanim LE, Nagakawa IS, et al. Dose-dependent toxicity of a commercially available demineralized bone matrix. Spine. 2001;26:1429–1436
  100. Edwards JT, Diegmann MH, Scarborough NL. Osteoinduction of human demineralized bone: characterization in a rat model. Clin Orthop. 1998;357:219–228
  101. Frenkel SR, Moskovich R, Spivak J, et al. Demineralized bone matrix: enhancement of spinal fusion. Spine. 1993;18:1634–1639
  102. Guizzardi S, Di Silvestre M, Scandroglio R, et al. Implants of heterologous demineralized bone matrix for induction of posterior spinal fusion in rats. Spine. 1992;17:701–707
  103. Lindholm TS, Ragni P, Lindholm TC. Response of bone marrow stroma cells to demineralized cortical bone matrix in experimental spinal fusion in rabbits. Clin Orthop. 1988;230:296–302
  104. Lindholm TS, Nilsson OS, Lindholm TC. Extraskeletal and intraskeletal new bone formation induced by demineralized bone matrix combined with bone marrow cells. Clin Orthop. 1982;171:251–255
  105. Ragni P, Lindholm TS. Interaction of allogeneic demineralized bone matrix and porous hydroxyapatite bioceramics in lumbar interbody fusion in rabbits. Clin Orthop. 1991;272:292–299
  106. Cammisa FP, Lowery G, Garfin SR, et al. Two-year rate equivalency between Grafton DBM gel and autograft in posterolateral spine fusion (A prospective controlled trial employing a side-by-side comparison in the same patient). Spine. 2004;29:660–666
  107. Louis-Ugbo J, Murakami H, Kim H, et al. Evidence of osteoinduction by Grafton demineralized bone matrix in nonhuman primate spinal fusion. Spine. 2004;29:360–366
  108. Hogan BL. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 1996;10:1580–1594
  109. Wozney JM. Overview of bone morphogenetic proteins. Spine. 2002;27(suppl):2–8
  110. Urist M, Strates B. Bone formation in implants of partially and wholly demineralized bone matrix. Clin Orthop. 1870;71:271–278
  111. Damien CJ, Grob D, Boden SD, et al. Purified bovine BMP extract and collagen for spine arthrodesis (Preclinical safety and efficacy). Spine. 2002;27(suppl):50–58
  112. Wozney JM, Rosen V, Celeste AJ, et al. Novel regulators of bone formation: molecular clones and activities. Science. 1988;242:1528–1534
  113. Wozney J. The bone morphogenetic protein family and osteogenesis. Mol Reprod Dev. 1992;32:160–167
  114. McKay B, Sandhu HS. Use of recombinant human bone morphogenetic protein-2 in spinal fusion application. Spine. 2002;27(suppl):66–85
  115. Vaccaro AR, Anderson DG, Toth CA. Recombinant human osteogenic protein-1 (Bone morphogenetic protein-7) as an osteoinductive agent in spinal fusion. Spine. 2002;2(suppl):59–65
  116. Seeherman H, Wozney J, Li R. Bone morphogenetic protein delivery systems. Spine. 2002;2(suppl):16–23
  117. Schimandle JH, Boden SD, Hutton WC. Experimental spinal fusion with recombinant human bone morphogenetic protein-2. Spine. 1995;20:1326–1337
  118. Boden SD, Martin GJ, Horton WC, et al. Laparoscopic anterior spinal arthrodesis with rhBMP-2 in a titanium interbody threaded cage. J Spinal Disord. 1998;11:95–101
  119. Boden SD, Schimandle JH, Hutton WC, et al. Volvo Award in basic sciences (The use of an osteoinductive growth factor for lumbar spinal fusion. Part I: Biology of spinal fusion). Spine. 1995;20:2626–2632
  120. Boden SD, Schimandle JH, Hutton WC. Volvo Award in basic sciences (The use of osteoinductive growth factor for lumbar spinal fusion, II: Study of dose, carrier, and species). Spine. 1995;20:2633–2644
  121. Sandhu HS, Kanim LE, Toth JM, et al. Experimental spinal fusion with recombinant human bone morphogenetic protein-2 without decortication of osseous elements. Spine. 1997;22:1171–1180
  122. Cook SD, Dalton JE, Tan EH, et al. In vivo evaluation of recombinant human osteogenic protein (rhOP-1) implant as a bone graft substitute for spinal fusions. Spine. 1994;19:1655–1663
  123. Muschler GF, Hyodo A, Manning T, et al. Evaluation of human bone morphogenetic protein 2 in a canine spinal fusion model. Clin Orthop. 1994;308:229–240
  124. Holliger EH, Trawick RH, Boden SD, et al. Morphology of the lumbar intertransverse process fusion mass in rabbit model: a comparison between two bone graft materials—rhBMP-2 and autograft. J Spinal Disord. 1996;9:125–128
  125. Grauer JN, Patel TC, Erulkar JS, et al. Evaluation of OP-1 as a graft substitute for intertransverse process lumbar fusion. Spine. 2000;26:127–133
  126. Sandhu HS, Kanim LE, Kabo JM, et al. Evaluation of rhBMP-2 with an OPLA carrier in a canine posterolateral (transverse process) spinal fusion model. Spine. 1995;20:2669–2682
  127. Silcox DH, Boden SD, Schimandle JH, et al. Reversing the inhibitory effect of nicotine on spinal fusion using an osteoinductive protein extract. Spine. 1998;23:291–296
  128. Martin GJ, Boden SD, Titus L. Recombinant human bone morphogenetic protein-2 overcomes the inhibitory effect of ketorolac, a nonsteroidal anti-inflammatory drug (NSAID), on posterolateral lumbar intertransverse process spine fusion. Spine. 1999;24:2188–2193
  129. Patel TC, Erulkar JS, Grauer JN, et al. Osteogenic protein-1 overcomes the inhibitory effect of nicotine on posterolateral lumbar fusion. Spine. 2001;26:1656–1661
  130. Vaccaro AR, Patel T, Fischgrund J, et al. A pilot study evaluating the safety and efficacy of OP-1 Putty (rhBMP-7) as a replacement for iliac crest autograft in posterolateral lumbar arthrodesis for degenerative spondylolisthesis. Spine. 2004;29(17):1885–1892
  131. Vaccaro AR, Patel T, Fischgrund J, et al. A 2-year follow-up pilot study evaluating the safety and efficacy of OP-1 Putty (rhBMP-7) as an adjunct to iliac crest autograft in posterolateral lumbar fusions. Eur Spine J. 2005;14(7):623–629
  132. Johnsson R, Stromqvist B, Aspenberg P. Randomized radiostereometric study comparing osteogenic protein-1 (BMP-7) and autograft bone in human noninstrumented posterolateral lumbar fusion: 2002 Volvo Award in clinical studies. Spine. 2002;27(23):2654–2661
  133. Kanayama M, Hashimoto T, Shigenobu K, et al. A prospective randomized study of posterolateral lumbar fusion using Osteogenic Protein-1 (OP-1) versus local autograft with ceramic bone substitute: emphasis of surgical exploration and histologic assessment. Spine. 2006;31(10):1067–1074
  134. Glassman SD, Carreon L, Djurasovic M, et al. Posterolateral lumbar spine fusion with INFUSE bone graft. Spine J. 2007;7(1):44–49
  135. Dimar JR, Glassman SD, Burkus KJ, et al. Clinical outcomes and fusion success at 2 years of single-level instrumented posterolateral fusions with recombinant human bone morphogenetic protein-2/compression resistant matrix versus iliac crest bone graft. Spine. 2006;31(22):2534–2539
  136. Slosar PJ, Reynolds JR. Accelerating lumbar fusions by combining rhBMP-2 with allograft bone: a prospective analysis of interbody fusion rates and clinical outcomes. Spine J. 2007;7(3):301–307
  137. Glassman SD, Dimar JR, Burkus , et al. The efficacy of rhBMP-2 for posterolateral lumbar fusion in smokers. Spine. 2007;32(15):1693–1698
  138. Lawerence JP, Waked W, Gillon TJ, et al. rhBMP-2 (ACS and CRM formulations) overcomes pseudoarthrosis in a New Zealand white rabbit posterolateral fusion model. Spine. 2007;32(11):1206–1213
  139. Poynton AR, Lane JM. Safety profile for the clinical use of bone morphogenetic proteins in the spine. Spine. 2002;2(suppl):40–48
  140. Paramore CG, Lauryssen C, Rauzzino MJ, et al. The safety of OP-1 for lumbar fusion with decompression—a canine study. Neurosurgery. 1999;44:1151–1155
  141. Kirsch T, Nickel J, Sebald W. BMP-2 antagonists emerge from alterations in the low-affinity binding epitope for receptor BMPR-II. EMBO J. 2000;19:3314–3324
  142. Kim DH, Jahng TA, Fu TS, et al. Evaluation of HEALOS/MP52 osteoinductive bone graft for instrumented lumbar intertransverse process fusion in sheep. Spine. 2004;29(24):2800–2808
  143. Jahng TA, Fu TS, Cunningham BW, et al. Endoscopic instrumented posterolateral lumbar fusion with HEALOS and recombinant human growth/differentiation factor-5. Neurosurgery. 2004;54(1):171–181
  144. Gupta MC, Turner SA, Seim HB, et al. Anterior interbody spine fusion in sheep using a PEEK cage and HEALOS/rhGDF-5 osteoinductive bone graft. Int Soc Study Lumbar Spine. 2005;132
  145. Ackerman SJ, Mafilios MS, Polly DW. Economic evaluation of bone morphogenetic protein versus autogenous iliac crest bone graft in single-level anterior lumbar fusion. Spine. 2002;27(suppl):94–99
  146. Glassman SD, Carreon LY, Campbell MJ, et al. The perioperative cost of infuse bone graft in posterolateral lumbar spine fusion. Spine J. 2008;8(3):443–448
  147. Baylink DJ, Finkelman RD, Mohan S. Growth factors to stimulate bone formation. J Bone Miner Res. 1993;8(suppl):565–572
  148. Slater M, Patava J, Kingham K, et al. Involvement of platelets in stimulating osteogenic activity. J Orthop Res. 1995;13:655–663
  149. Lowery GL, Kulkarni S, Pennisi AE. Use of autologous growth factors in lumbar spinal fusion. Bone. 1999;25(suppl):47–50
  150. Weiner B, Walker M. Efficacy of Autologous growth factors in lumbar intertransverse fusions (clinical cases series). Spine. 2003;28:1968–1970
  151. Muschler GF, Boehm C, Easley KA. Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume. J Bone Joint Surg Am. 1997;79:1699–1709
  152. Muschler GF, Nitto H, Boehm , et al. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res. 2001;19:117–125
  153. Connolly J, Guse R, Lippiello L, et al. Development of an osteogenic bone marrow preparation. J Bone Joint Surg Am. 1989;71:684–691
  154. Lane JM, Yasko AW, Tomin E, et al. Bone marrow and recombinant human bone morphogenetic protein-2 in osseous repair. Clin Orthop. 1999;361:216–227
  155. Kraiwattanapong C, Boden S, Louis-Ugbo J, et al. Comparison of Healos/bone marrow to INFUSE (rhBMP-2/ACS) with a collagen-ceramic sponge bulking agent as graft substitutes for lumbar spine fusion. Spine. 2005;30(9):1001–1007
  156. Curylo LJ, Johnstone G, Petersilge CA, et al. Augmentation of spinal arthrodesis with Autologous bone marrow in a rabbit posterolateral spine fusion model. Spine. 1999;24(5):434–438
  157. Muschler GF, Matsukura Y, Nitto H, et al. Selective retention of bone marrow-derived cells to enhance spinal fusion. Clin Orthop Relat Res. 2005;432:242–251
  158. Price CT, Connolly JF, Carantzas AC, et al. Comparison of bone grafts for posterior spinal fusion in adolescent idiopathic scoliosis. Spine. 2003;28(8):793–798
  159. Kitchel SH. A preliminary comparative study of radiographic results using mineralized collagen and bone marrow aspirate versus autologous bone in the same patients undergoing posterior lumbar interbody fusion with instrumented posterolateral lumbar fusion. Spine J. 2006;6(4):405–411
  160. Kai T, Shao-qing G, Geng-ting D. In vivo evaluation of bone marrow stromal-derived osteoblasts-porous calcium phosphate ceramic composites as bone graft substitute for lumbar intervertebral spinal fusion. Spine. 2003;28(15):1653–1658
  161. Jaiswal N, Haynesworth SE, Caplan AI, et al. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem. 1997;64:295–312
  162. Kadiyala S, Young RG, Thiede MA, et al. Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro. Cell Transplant. 1997;6:125–134
  163. Lieberman JR, Daluiski A, Stevenson S, et al. The effect of regional gene therapy with bone morphogenetic protein-2-producing bone-marrow cells on the repair of segmental femoral defects in rats. J Bone Joint Surg Am. 1999;81:905–917
  164. Alden TD, Pittman DD, Beres EJ, et al. Percutaneous spinal fusion using bone morphogenetic protein-2 gene therapy. J Neurosurg. 1999;90(suppl):109–114
  165. Wang JC, Kanim LE, Yoo S, et al. Effect of regional gene therapy with bone morphogenetic protein-2-producing bone marrow cells on spinal fusion in rats. J Bone Joint Surg Am. 2003;85:905–901
  166. Boden SD, Titus L, Hair G, et al. Lumbar spine fusion by local gene therapy with a cDNA encoding a novel osteoinductive protein (LMP-1). Spine. 1998;23:2486–2492
  167. Toribatake Y, Hutton C, Boden SD, et al. Revascularization of the fusion mass in a posterolateral intertransverse process fusion. Spine. 1998;23:1149–1154

PII: S1040-7383(08)00072-5

doi: 10.1053/j.semss.2008.08.003

Seminars in Spine Surgery
Volume 20, Issue 4 , Pages 257-269 , December 2008