Bone graft materials for posterolateral fusion made simple: a systematic review

  • Matthew T. Morris
  • Sandip P. Tarpada
  • Woojin Cho
Review
  • 58 Downloads

Abstract

Background

Iliac crest has long been the gold standard for lumbar fusion, but concerns over donor site morbidity have led to a wide variety of bone graft substitutes. Despite prolific research, a general consensus is yet to be reached on bone graft materials that lead to optimal fusion.

Purpose

The purpose of this review is to evaluate the current literature for bone graft material options that maximize fusion rate in posterolateral lumbar fusion surgery.

Design

Systematic Review.

Methods

A PRISMA—compliant systematic review of PubMed, EMBASE, and the Web of Science was conducted. Included studies were published from January 2000 to July 2015, were clinical human research studies involving available autograft, allograft, or synthetic bone graft options in posterolateral lumbar spine fusion, and reported radiographic fusion rate as a primary end outcome. This research had no funding source and the authors have no conflicts to declare.

Results

81 articles underwent full-text review, and 48 were included in this study. 18 studies assessed fusion rate by plain radiographs alone (37.5%), while 6 used CT scan (12.5%), and 24 used both (50.0%). 45 studies looked at ICBG in conjunction with LAG (29), BCP(1), APC (2), BMPs (6), or DBM (1). Aggregate mean fusion rates among these ranged from 68.0 to 91.5%. 22 studies evaluated fusion rates of LAG, either isolated (3) or combined with ceramic extenders (8), DBM (4), BMP (1), BMA (4), APC (1), or ICBG(1). Aggregate mean fusion rate ranged from 75 to 95.5%. With the exception of studies involving allograft (mean fusion rate 40.0%), the mean fusion rate for all other graft combinations exceeded 70.0%.

Conclusions

While our results find that LAG+BMA provided highest fusion rate, most material options analyzed in this study provide comparable fusion outcomes. The ideal graft option must incorporate a combination of materials with osteoconductive, osteoinductive, and osteogenic properties. Our results represent the robust and dynamic nature of the current state of lumbar graft technology.

Graphical abstract

These slides can be retrieved under Electronic Supplementary Material.

Keywords

Posterolateral lumbar fusion Bone graft Graft materials Allograft Autograft Bone marrow Growth factors Collagen Ceramics 

Notes

Acknowledgements

We would like to thank our librarian Karen Sorensen M.L.S, B.A, for her contributions to this systematic review.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

586_2018_5511_MOESM1_ESM.pptx (208 kb)
Supplementary material 1 (PPTX 207 kb)

References

  1. 1.
    Carreon LY, Glassman SD, Djurasovic M et al (2009) RhBMP-2 versus iliac crest bone graft for lumbar spine fusion in patients over 60 years of age: a cost-utility study. Spine 34(3):238–243.  https://doi.org/10.1097/BRS.0b013e31818ffabe CrossRefPubMedGoogle Scholar
  2. 2.
    Korovessis P, Koureas G, Zacharatos S, Papazisis Z, Lambiris E (2005) Correlative radiological, self-assessment and clinical analysis of evolution in instrumented dorsal and lateral fusion for degenerative lumbar spine disease. Autograft versus coralline hydroxyapatite. Eur Spine J 14(7):630–638.  https://doi.org/10.1007/s00586-004-0855-5 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Lee K-B, Taghavi CE, Hsu MS et al (2010) The efficacy of rhBMP-2 versus autograft for posterolateral lumbar spine fusion in elderly patients. Eur Spine J 19(6):924–930.  https://doi.org/10.1007/s00586-009-1248-6 CrossRefPubMedGoogle Scholar
  4. 4.
    Vaccaro AR, Stubbs HA, Block JE (2007) Demineralized bone matrix composite grafting for posterolateral spinal fusion. Orthopedics 30(7):567–570PubMedGoogle Scholar
  5. 5.
    Sassard WR, Eidman DK, Gray PM et al (2000) Augmenting local bone with Grafton demineralized bone matrix for posterolateral lumbar spine fusion: avoiding second site autologous bone harvest. Orthopedics 23(10):1059–1064 (discussion 1064–1065) PubMedGoogle Scholar
  6. 6.
    Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700.  https://doi.org/10.1136/bmj.b2700 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Wright JG, Swiontkowski MF, Heckman JD (2003) Introducing levels of evidence to the journal. J Bone Joint Surg Am 85(1):1–3CrossRefPubMedGoogle Scholar
  8. 8.
    Dimar JR, Glassman SD, Burkus JK, Pryor PW, Hardacker JW, Carreon LY (2009) Two-year fusion and clinical outcomes in 224 patients treated with a single-level instrumented posterolateral fusion with iliac crest bone graft. Spine J 9(11):880–885.  https://doi.org/10.1016/j.spinee.2009.03.013 CrossRefPubMedGoogle Scholar
  9. 9.
    Dai L-Y, Jiang L-S (2008) Single-level instrumented posterolateral fusion of lumbar spine with beta-tricalcium phosphate versus autograft: a prospective, randomized study with 3-year follow-up. Spine 33(12):1299–1304.  https://doi.org/10.1097/BRS.0b013e3181732a8e CrossRefPubMedGoogle Scholar
  10. 10.
    Fischgrund JS, Mackay M, Herkowitz HN, Brower R, Montgomery DM, Kurz LT (1997) 1997 Volvo Award winner in clinical studies. Degenerative lumbar spondylolisthesis with spinal stenosis: a prospective, randomized study comparing decompressive laminectomy and arthrodesis with and without spinal instrumentation. Spine 22(24):2807–2812CrossRefPubMedGoogle Scholar
  11. 11.
    Kimura I, Shingu H, Murata M, Hashiguchi H (2001) Lumbar posterolateral fusion alone or with transpedicular instrumentation in L4–L5 degenerative spondylolisthesis. J Spin Disord 14(4):301–310CrossRefGoogle Scholar
  12. 12.
    Dimar JR, Glassman SD, Burkus KJ, Carreon LY (2006) 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 31(22):2534–2539.  https://doi.org/10.1097/01.brs.0000240715.78657.81 (discussion 2540) CrossRefPubMedGoogle Scholar
  13. 13.
    Epstein NE (2006) A preliminary study of the efficacy of Beta Tricalcium Phosphate as a bone expander for instrumented posterolateral lumbar fusions. J Spinal Disord Tech 19(6):424–429CrossRefPubMedGoogle Scholar
  14. 14.
    Vaccaro AR, Whang PG, Patel T et al (2008) The safety and efficacy of OP-1 (rhBMP-7) as a replacement for iliac crest autograft for posterolateral lumbar arthrodesis: minimum 4-year follow-up of a pilot study. Spine J 8(3):457–465.  https://doi.org/10.1016/j.spinee.2007.03.012 CrossRefPubMedGoogle Scholar
  15. 15.
    Jorgenson SS, Lowe TG, France J, Sabin J (1994) A prospective analysis of autograft versus allograft in posterolateral lumbar fusion in the same patient. A minimum of 1-year follow-up in 144 patients. Spine 19(18):2048–2053CrossRefPubMedGoogle Scholar
  16. 16.
    Sengupta DK, Truumees E, Patel CK et al (2006) Outcome of local bone versus autogenous iliac crest bone graft in the instrumented posterolateral fusion of the lumbar spine. Spine 31(9):985–991.  https://doi.org/10.1097/01.brs.0000215048.51237.3c CrossRefPubMedGoogle Scholar
  17. 17.
    Acebal-Cortina G, Suárez-Suárez MA, García-Menéndez C, Moro-Barrero L, Iglesias-Colao R, Torres-Pérez A (2011) Evaluation of autologous platelet concentrate for intertransverse lumbar fusion. Eur Spine J 20(Suppl 3):361–366.  https://doi.org/10.1007/s00586-011-1904-5 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Alexander DI, Manson NA, Mitchell MJ (2001) Efficacy of calcium sulfate plus decompression bone in lumbar and lumbosacral spinal fusion: preliminary results in 40 patients. Can J Surg 44(4):262–266PubMedPubMedCentralGoogle Scholar
  19. 19.
    Chen W-J, Tsai T-T, Chen L-H et al (2005) The fusion rate of calcium sulfate with local autograft bone compared with autologous iliac bone graft for instrumented short-segment spinal fusion. Spine 30(20):2293–2297CrossRefPubMedGoogle Scholar
  20. 20.
    Kanayama M, Hashimoto T, Shigenobu K, Yamane S, Bauer TW, Togawa D (2006) 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 31(10):1067–1074.  https://doi.org/10.1097/01.brs.0000216444.01888.21 CrossRefPubMedGoogle Scholar
  21. 21.
    Odri GA, Hami A, Pomero V et al (2012) Development of a per-operative procedure for concentrated bone marrow adjunction in postero–lateral lumbar fusion: radiological, biological and clinical assessment. Eur Spine J 21(12):2665–2672.  https://doi.org/10.1007/s00586-012-2375-z CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hart R, Komzák M, Okál F, Náhlík D, Jajtner P, Puskeiler M (2014) Allograft alone versus allograft with bone marrow concentrate for the healing of the instrumented posterolateral lumbar fusion. Spine J 14(7):1318–1324.  https://doi.org/10.1016/j.spinee.2013.12.014 CrossRefPubMedGoogle Scholar
  23. 23.
    Acharya NK, Kumar RJ, Varma HK, Menon VK (2008) Hydroxyapatite-bioactive glass ceramic composite as stand-alone graft substitute for posterolateral fusion of lumbar spine: a prospective matched, and controlled study. J Spin Disord Tech 21(2):106–111.  https://doi.org/10.1097/BSD.0b013e31805fea1f CrossRefGoogle Scholar
  24. 24.
    Jenis LG, Banco RJ (2010) Efficacy of silicate-substituted calcium phosphate ceramic in posterolateral instrumented lumbar fusion. Spine 35(20):E1058–E1063.  https://doi.org/10.1097/BRS.0b013e3181df196f CrossRefPubMedGoogle Scholar
  25. 25.
    Moro-Barrero L, Acebal-Cortina G, Suárez-Suárez M, Pérez-Redondo J, Murcia-Mazón A, López-Muñiz A (2007) Radiographic analysis of fusion mass using fresh autologous bone marrow with ceramic composites as an alternative to autologous bone graft. J Spin Disord Tech 20(6):409–415CrossRefGoogle Scholar
  26. 26.
    Ploumis A, Albert TJ, Brown Z, Mehbod AA, Transfeldt EE (2010) Healos graft carrier with bone marrow aspirate instead of allograft as adjunct to local autograft for posterolateral fusion in degenerative lumbar scoliosis: a minimum 2-year follow-up study. J Neurosurg Spine 13(2):211–215.  https://doi.org/10.3171/2010.3.SPINE09603 CrossRefPubMedGoogle Scholar
  27. 27.
    Carreon LY, Glassman SD, Anekstein Y, Puno RM (2005) Platelet gel (AGF) fails to increase fusion rates in instrumented posterolateral fusions. Spine 30(9):E243–E246 (discussion E247) CrossRefPubMedGoogle Scholar
  28. 28.
    Boden SD, Kang J, Sandhu H, Heller JG (2002) Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies. Spine 27(23):2662–2673.  https://doi.org/10.1097/01.BRS.0000035320.82533.06 CrossRefPubMedGoogle Scholar
  29. 29.
    Kang J, An H, Hilibrand A, Yoon ST, Kavanagh E, Boden S (2012) Grafton and local bone have comparable outcomes to iliac crest bone in instrumented single-level lumbar fusions. Spine 37(12):1083–1091.  https://doi.org/10.1097/BRS.0b013e31823ed817 CrossRefPubMedGoogle Scholar
  30. 30.
    Vaccaro AR, Patel T, Fischgrund J et al (2004) 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 29(17):1885–1892CrossRefPubMedGoogle Scholar
  31. 31.
    Singh K, Smucker JD, Gill S, Boden SD (2006) Use of recombinant human bone morphogenetic protein-2 as an adjunct in posterolateral lumbar spine fusion: a prospective CT-scan analysis at one and two years. J Spin Disord Tech 19(6):416–423CrossRefGoogle Scholar
  32. 32.
    Epstein NE (2008) An analysis of non-instrumented posterolateral lumbar fusions performed in predominantly geriatric patients using lamina autograft and beta tricalcium phosphate. Spine J 8(6):882–887.  https://doi.org/10.1016/j.spinee.2007.11.005 CrossRefPubMedGoogle Scholar
  33. 33.
    Park DK, Kim SS, Thakur N, Boden SD (2013) Use of recombinant human bone morphogenetic protein-2 with local bone graft instead of iliac crest bone graft in posterolateral lumbar spine arthrodesis. Spine 38(12):E738–E747.  https://doi.org/10.1097/BRS.0b013e31828fd23c CrossRefPubMedGoogle Scholar
  34. 34.
    Coetzee AS (1988) Regeneration of bone in the presence of calcium sulfate. Arch Otolaryngol 106(7):405–409CrossRefGoogle Scholar
  35. 35.
    Hadjipavlou AG, Simmons JW, Yang J, Nicodemus CL, Esch O, Simmons DJ (2000) Plaster of Paris as an osteoconductive material for interbody vertebral fusion in mature sheep. Spine 25(1):10–15 (discussion 16) CrossRefPubMedGoogle Scholar
  36. 36.
    Turner TM, Urban RM, Gitelis S, Haggard WO, Richelsoph K (2003) Resorption evaluation of a large bolus of calcium sulfate in a canine medullary defect. Orthopedics 26(5 Suppl):s577–s579PubMedGoogle Scholar
  37. 37.
    Sidqui M, Collin P, Vitte C, Forest N (1995) Osteoblast adherence and resorption activity of isolated osteoclasts on calcium sulphate hemihydrate. Biomaterials 16(17):1327–1332CrossRefPubMedGoogle Scholar
  38. 38.
    Blom AW, Cunningham JL, Hughes G et al (2005) The compatibility of ceramic bone graft substitutes as allograft extenders for use in impaction grafting of the femur. J Bone Joint Surg Br 87(3):421–425CrossRefPubMedGoogle Scholar
  39. 39.
    Hurlbert RJ, Alexander D, Bailey S et al (2013) rhBMP-2 for posterolateral instrumented lumbar fusion: a multicenter prospective randomized controlled trial. Spine 38(25):2139–2148.  https://doi.org/10.1097/BRS.0000000000000007 CrossRefPubMedGoogle Scholar
  40. 40.
    Johnsson R, Strömqvist B, Aspenberg P (2002) Randomized radiostereometric study comparing osteogenic protein-1 (BMP-7) and autograft bone in human non-instrumented posterolateral lumbar fusion: 2002 Volvo Award in clinical studies. Spine 27(23):2654–2661.  https://doi.org/10.1097/01.BRS.0000035339.83704.60 CrossRefPubMedGoogle Scholar
  41. 41.
    Gupta A, Kukkar N, Sharif K, Main BJ, Albers CE, El-Amin SF III (2015) Bone graft substitutes for spine fusion: a brief review. World J Orthop 6(6):449–456.  https://doi.org/10.5312/wjo.v6.i6.449 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Epstein NE (2009) Beta tricalcium phosphate: observation of use in 100 posterolateral lumbar instrumented fusions. Spine J 9(8):630–638.  https://doi.org/10.1016/j.spinee.2009.04.007 CrossRefPubMedGoogle Scholar
  43. 43.
    Glassman SD, Dimar JR, Carreon LY, Campbell MJ, Puno RM, Johnson JR (2005) Initial fusion rates with recombinant human bone morphogenetic protein-2/compression resistant matrix and a hydroxyapatite and tricalcium phosphate/collagen carrier in posterolateral spinal fusion. Spine 30(15):1694–1698CrossRefPubMedGoogle Scholar
  44. 44.
    Glassman SD, Dimar JR, Burkus K et al (2007) The efficacy of rhBMP-2 for posterolateral lumbar fusion in smokers. Spine 32(15):1693–1698.  https://doi.org/10.1097/BRS.0b013e318074c366 CrossRefPubMedGoogle Scholar
  45. 45.
    Bae HW, Stambough J, Glassman SD, Burkus JK (2007) 18. Level-1 data comparing rhBMP-2/ACS combined with an osteoconductive bulking agent with iliac crest bone graft in posterolateral lumbar fusion. Spine J 7(5):9S.  https://doi.org/10.1016/j.spinee.2007.07.024 CrossRefGoogle Scholar
  46. 46.
    Dawson E, Bae HW, Burkus JK, Stambough JL, Glassman SD (2009) Recombinant human bone morphogenetic protein-2 on an absorbable collagen sponge with an osteoconductive bulking agent in posterolateral arthrodesis with instrumentation. A prospective randomized trial. J Bone Joint Surg Am 91(7):1604–1613.  https://doi.org/10.2106/JBJS.G.01157 CrossRefPubMedGoogle Scholar
  47. 47.
    Burkus JK, Dorchak JD, Sanders DL (2003) Radiographic assessment of interbody fusion using recombinant human bone morphogenetic protein type 2. Spine 28(4):372–377.  https://doi.org/10.1097/01.BRS.0000048469.45035.B9 PubMedGoogle Scholar
  48. 48.
    Burkus JK, Transfeldt EE, Kitchel SH, Watkins RG, Balderston RA (2002) Clinical and radiographic outcomes of anterior lumbar interbody fusion using recombinant human bone morphogenetic protein-2. Spine 27(21):2396–2408.  https://doi.org/10.1097/01.BRS.0000030193.26290.DD CrossRefPubMedGoogle Scholar
  49. 49.
    Slosar PJ, Josey R, Reynolds J (2007) Accelerating lumbar fusions by combining rhBMP-2 with allograft bone: a prospective analysis of interbody fusion rates and clinical outcomes. Spine J 7(3):301–307.  https://doi.org/10.1016/j.spinee.2006.10.015 CrossRefPubMedGoogle Scholar
  50. 50.
    Kasai Y, Takegami K, Uchida A (2003) Mixture ratios of local bone to artificial bone in lumbar posterolateral fusion. J Spinal Disord Tech 16(1):31–37CrossRefPubMedGoogle Scholar
  51. 51.
    Frantzén J, Rantakokko J, Aro HT et al (2011) Instrumented spondylodesis in degenerative spondylolisthesis with bioactive glass and autologous bone: a prospective 11-year follow-up. J Spinal Disord Tech 24(7):455–461.  https://doi.org/10.1097/BSD.0b013e31822a20c6 CrossRefPubMedGoogle Scholar
  52. 52.
    Vaccaro AR, Anderson DG, Patel T et al (2005) Comparison of OP-1 Putty (rhBMP-7) to iliac crest autograft for posterolateral lumbar arthrodesis: a minimum 2-year follow-up pilot study. Spine 30(24):2709–2716CrossRefPubMedGoogle Scholar
  53. 53.
    Buser Z, Brodke DS, Youssef JA, Meisel HJ, Myhre SL, Hashimoto R, Park JB, Tim Yoon S, Wang JC (2016) Synthetic bone graft versus autograft or allograft for spinal fusion: a systematic review. J Neurosurg Spine 25(4):509–516CrossRefPubMedGoogle Scholar
  54. 54.
    Tuchman A, Brodke DS, Youssef JA, Meisel HJ, Dettori JR, Park JB, Yoon ST, Wang JC (2016) Iliac crest bone graft versus local autograft or allograft for lumbar spinal fusion: a systematic review. Glob spine J 6(06):592–606CrossRefGoogle Scholar
  55. 55.
    Bhakta G, Ekaputra AK, Rai B, Abbah SA, Tan TC, Le BQ, Chatterjea A, Hu T, Lin T, Arafat MT, van Wijnen AJ, Goh J, Nurcombe V, Bhakoo K, Birch W, Xu L, Gibson I, Wong HK, Cool SM (2017) Fabrication of polycaprolactone-silanated β-tricalcium phosphate-heparan sulfate scaffolds for spinal fusion applications. Spine J. S1529-9430(17):31199–31203Google Scholar
  56. 56.
    Geurts J, Ramp D, Schären S, Netzer C (2017) Comparison of in vitro osteogenic potential of iliac crest and degenerative facet joint bone autografts for intervertebral fusion in lumbar spinal stenosis. Eur Spine J 26(5):1408–1415CrossRefPubMedGoogle Scholar
  57. 57.
    Ajiboye RM, Eckardt MA, Hamamoto JT, Sharma A, Khan AZ, Wang JC (2018) Does age influence the efficacy of demineralized bone matrix enriched with concentrated bone marrow aspirate in lumbar fusions? Clin Spine Surg 31(1):E30–E35PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Matthew T. Morris
    • 1
  • Sandip P. Tarpada
    • 1
  • Woojin Cho
    • 1
    • 2
  1. 1.Department of Orthopaedic SurgeryAlbert Einstein College of MedicineBronxUSA
  2. 2.Department of Orthopaedic SurgeryMontefiore Medical CenterBronxUSA

Personalised recommendations