Top

European Spine Journal

Published in:

01-06-2013 | Review Article

A systematic review of comparative studies on bone graft alternatives for common spine fusion procedures

Authors: Charla R. Fischer, Ryan Cassilly, Winifred Cantor, Emmanuel Edusei, Qusai Hammouri, Thomas Errico

Published in: European Spine Journal | Issue 6/2013

Abstract

Background

The increased prevalence of spinal fusion surgery has created an industry focus on bone graft alternatives. While autologous bone graft remains the gold standard, the complications and morbidity from harvesting autologous bone drives the search for reliable and safe bone graft substitutes. With the recent information about the adverse events related to bone morhogenetic protein use, it is appropriate to review the literature about the numerous products that are not solely bone morphogenetic protein.

Purpose

The purpose of this literature review is to determine the recommendations for use of non-bone morphogenetic protein bone graft alternatives in the most common spine procedures based on a quantifiable grading system.

Study design

Systematic literature review.

Methods

A literature search of MEDLINE (1946–2012), CINAHL (1937–2012), and the Cochrane Central Register of Controlled Trials (1940–April 2012) was performed, and this was supplemented by a hand search. The studies were then evaluated based on the Guyatt criteria for quality of the research to determine the strength of the recommendation.

Results

In this review, more than one hundred various studies on the ability of bone graft substitutes to create solid fusions and good patient outcomes are detailed.

Conclusion

The recommendations for use of bone graft substitutes and bone graft extenders are based on the strength of the studies and given a grade.

Weinstein JN, Lurie JD, Olson PR, Bronner KK, Fisher ES (2006) United States’ trends and regional variations in lumbar spine surgery: 1992–2003. Spine (Phila Pa 1976) 31(23):2707–2714. doi:10.1097/01.brs.0000248132.15231.fe

Bono CM, Lee CK (2004) Critical analysis of trends in fusion for degenerative disc disease over the past 20 years: influence of technique on fusion rate and clinical outcome. Spine (Phila Pa 1976) 29(4):455–463; discussion Z455. pii:00007632-200402150-00019

Burkus JK, Schuler TC, Gornet MF, Zdeblick TA (2004) Anterior lumbar interbody fusion for the management of chronic lower back pain: current strategies and concepts. Orthop Clin North Am 35(1):25–32. doi:10.1016/S0030-5898(03)00053-1 PubMedCrossRef

Dawson EG, Lotysch M 3rd, Urist MR (1981) Intertransverse process lumbar arthrodesis with autogenous bone graft. Clin Orthop Relat Res 154:90–96PubMed

Dodd CA, Fergusson CM, Freedman L, Houghton GR, Thomas D (1988) Allograft versus autograft bone in scoliosis surgery. J Bone Joint Surg Br 70(3):431–434PubMed

Kho VK, Chen WC (2004) The results of posterolateral lumbar fusion with bone chips from laminectomy in patients with lumbar spondylolisthesis. J Chin Med Assoc 67(11):575–578PubMed

Dai LY, Jiang LS, Jiang SD (2008) Conservative treatment of thoracolumbar burst fractures: a long-term follow-up results with special reference to the load sharing classification. Spine (Phila Pa 1976) 33(23):2536–2544. doi:10.1097/BRS.0b013e3181851bc2 CrossRef

Dimar JR, Glassman SD (2007) The art of bone grafting. Curr Opin Orthop 18(3):8CrossRef

Dimar JR 2nd, 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. doi:S1529-9430(09)00147-8 PubMedCrossRef

10.

Ahlmann E, Patzakis M, Roidis N, Shepherd L, Holtom P (2002) Comparison of anterior and posterior iliac crest bone grafts in terms of harvest-site morbidity and functional outcomes. J Bone Joint Surg Am 84-A(5):716–720PubMed

11.

Arrington ED, Smith WJ, Chambers HG, Bucknell AL, Davino NA (1996) Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res 329:300–309PubMedCrossRef

12.

Banwart JC, Asher MA, Hassanein RS (1995) Iliac crest bone graft harvest donor site morbidity. A statistical evaluation. Spine (Phila Pa 1976) 20(9):1055–1060CrossRef

13.

Delawi D, Dhert WJ, Castelein RM, Verbout AJ, Oner FC (2007) The incidence of donor site pain after bone graft harvesting from the posterior iliac crest may be overestimated: a study on spine fracture patients. Spine (Phila Pa 1976) 32(17):1865–1868. doi:10.1097/BRS.0b013e318107674e CrossRef

14.

Younger EM, Chapman MW (1989) Morbidity at bone graft donor sites. J Orthop Trauma 3(3):192–195PubMedCrossRef

15.

Niu CC, Tsai TT, Fu TS, Lai PL, Chen LH, Chen WJ (2009) A comparison of posterolateral lumbar fusion comparing autograft, autogenous laminectomy bone with bone marrow aspirate, and calcium sulphate with bone marrow aspirate: a prospective randomized study. Spine (Phila Pa 1976) 34(25):2715–2719. doi:10.1097/BRS.0b013e3181b47232 CrossRef

16.

Hsu CJ, Chou WY, Teng HP, Chang WN, Chou YJ (2005) Coralline hydroxyapatite and laminectomy-derived bone as adjuvant graft material for lumbar posterolateral fusion. J Neurosurg Spine 3(4):271–275. doi:10.3171/spi.2005.3.4.0271 PubMedCrossRef

17.

Miyazaki M, Tsumura H, Wang JC, Alanay A (2009) An update on bone substitutes for spinal fusion. Eur Spine J 18(6):783–799. doi:10.1007/s00586-009-0924-x PubMedCrossRef

18.

Ransford AO, Morley T, Edgar MA, Webb P, Passuti N, Chopin D, Morin C, Michel F, Garin C, Pries D (1998) Synthetic porous ceramic compared with autograft in scoliosis surgery. A prospective, randomized study of 341 patients. J Bone Joint Surg Br 80(1):13–18PubMedCrossRef

19.

Rihn JA, Kirkpatrick K, Albert TJ (2010) Graft options in posterolateral and posterior interbody lumbar fusion. Spine (Phila Pa 1976) 35(17):1629–1639. doi:10.1097/BRS.0b013e3181d25803 CrossRef

20.

Guyatt G, Schunemann H, Cook D, Jaeschke R, Pauker S, Bucher H (2001) Grades of recommendation for antithrombotic agents. Chest 119(1 Suppl):3S–7SPubMedCrossRef

21.

Guyatt G, Gutterman D, Baumann MH, Addrizzo-Harris D, Hylek EM, Phillips B, Raskob G, Lewis SZ, Schunemann H (2006) Grading strength of recommendations and quality of evidence in clinical guidelines: report from an american college of chest physicians task force. Chest 129(1):174–181. doi:10.1378/chest.129.1.174 PubMedCrossRef

22.

Fisher CG, Wood KB (2007) Introduction to and techniques of evidence-based medicine. Spine (Phila Pa 1976) 32(19 Suppl):S66–S72. doi:10.1097/BRS.0b013e318145308d CrossRef

23.

Samartzis D, Shen FH, Goldberg EJ, An HS (2005) Is autograft the gold standard in achieving radiographic fusion in one-level anterior cervical discectomy and fusion with rigid anterior plate fixation? Spine (Phila Pa 1976) 30(15):1756–1761CrossRef

24.

Sassard WR, Eidman DK, Gray PM, Block JE, Russo R, Russell JL, Taboada EM (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 1064-1055PubMed

25.

Christensen FB, Laursen M, Gelineck J, Eiskjaer SP, Thomsen K, Bunger CE (2001) Interobserver and intraobserver agreement of radiograph interpretation with and without pedicle screw implants: the need for a detailed classification system in posterolateral spinal fusion. Spine 26(5):538–543 discussion 543-534PubMedCrossRef

26.

Sugiyama S, Wullschleger M, Wilson K, Williams R, Goss B (2012) Reliability of clinical measurement for assessing spinal fusion: an experimental sheep study. Spine 37(9):763–768. doi:10.1097/BRS.0b013e31822ffa05 PubMedCrossRef

27.

Mikhael MM, Huddleston PM, Nassr A (2009) Postoperative culture positive surgical site infections after the use of irradiated allograft, nonirradiated allograft, or autograft for spinal fusion. Spine (Phila Pa 1976) 34(22):2466–2468. doi:10.1097/BRS.0b013e3181b1fef5 CrossRef

28.

Buck BE, Malinin TI, Brown MD (1989) Bone transplantation and human immunodeficiency virus. An estimate of risk of acquired immunodeficiency syndrome (AIDS). Clin Orthop Relat Res 240:129–136PubMed

29.

Nasca RJ, Whelchel JD (1987) Use of cryopreserved bone in spinal surgery. Spine (Phila Pa 1976) 12(3):222–227CrossRef

30.

Glassman SD, Howard JM, Sweet A, Carreon LY (2010) Complications and concerns with osteobiologics for spine fusion in clinical practice. Spine (Phila Pa 1976) 35(17):1621–1628. doi:10.1097/BRS.0b013e3181ce11cc CrossRef

31.

Chau AM, Mobbs RJ (2009) Bone graft substitutes in anterior cervical discectomy and fusion. Eur Spine J 18(4):449–464. doi:10.1007/s00586-008-0878-4 PubMedCrossRef

32.

Suchomel P, Barsa P, Buchvald P, Svobodnik A, Vanickova E (2004) Autologous versus allogenic bone grafts in instrumented anterior cervical discectomy and fusion: a prospective study with respect to bone union pattern. Eur Spine J 13(6):510–515. doi:10.1007/s00586-003-0667-z PubMedCrossRef

33.

Ryu SI, Mitchell M, Kim DH (2006) A prospective randomized study comparing a cervical carbon fiber cage to the Smith-Robinson technique with allograft and plating: up to 24 months follow-up. Eur Spine J 15(2):157–164. doi:10.1007/s00586-005-0951-1 PubMedCrossRef

34.

Yue WM, Brodner W, Highland TR (2005) Long-term results after anterior cervical discectomy and fusion with allograft and plating: a 5- to 11-year radiologic and clinical follow-up study. Spine (Phila Pa 1976) 30(19):2138–2144CrossRef

35.

Gibson S, McLeod I, Wardlaw D, Urbaniak S (2002) Allograft versus autograft in instrumented posterolateral lumbar spinal fusion: a randomized control trial. Spine (Phila Pa 1976) 27(15):1599–1603CrossRef

36.

An HS, Lynch K, Toth J (1995) Prospective comparison of autograft vs. allograft for adult posterolateral lumbar spine fusion: differences among freeze-dried, frozen, and mixed grafts. J Spinal Disord 8(2):131–135PubMedCrossRef

37.

Thalgott JS, Fogarty ME, Giuffre JM, Christenson SD, Epstein AK, Aprill C (2009) A prospective, randomized, blinded, single-site study to evaluate the clinical and radiographic differences between frozen and freeze-dried allograft when used as part of a circumferential anterior lumbar interbody fusion procedure. Spine (Phila Pa 1976) 34(12):1251–1256. doi:10.1097/BRS.0b013e3181a005d7 CrossRef

38.

Winters HA, van Engeland AE, Jiya TU, van Royen BJ (2010) The use of free vascularised bone grafts in spinal reconstruction. J plast reconst aesthet surg JPRAS 63(3):516–523. doi:10.1016/j.bjps.2008.11.037 CrossRef

39.

Aurori BF, Weierman RJ, Lowell HA, Nadel CI, Parsons JR (1985) Pseudarthrosis after spinal fusion for scoliosis. A comparison of autogeneic and allogeneic bone grafts. Clin Orthop Relat Res 199:153–158PubMed

40.

Emovon OE, King JA, Holt CO, Singleton B, Howell D, Browne BJ (2003) Effect of cyclosporin pharmacokinetics on renal allograft outcome in African-Americans. Clin Transplant 17(3):206–211 (pii:029)PubMedCrossRef

41.

Knapp DR Jr, Jones ET, Blanco JS, Flynn JC, Price CT (2005) Allograft bone in spinal fusion for adolescent idiopathic scoliosis. J Spinal Disord Tech 18(Suppl):S73–S76PubMedCrossRef

42.

An HS, Simpson JM, Glover JM, Stephany J (1995) Comparison between allograft plus demineralized bone matrix versus autograft in anterior cervical fusion. A prospective multicenter study. Spine (Phila Pa 1976) 20(20):2211–2216CrossRef

43.

Thalgott JS, Giuffre JM, Klezl Z, Timlin M (2002) Anterior lumbar interbody fusion with titanium mesh cages, coralline hydroxyapatite, and demineralized bone matrix as part of a circumferential fusion. Spine J 2(1):63–69. doi:S1529943001001553 PubMedCrossRef

44.

Kang JD, An H, Hilibrand AS (2008) Grafton and local bone has comparable outcomes to iliac crest bone in single level lumbar fusions. Paper presented at the American Academy of Orthopaedic Surgeons 75th Annual Meeting, San Francisco, CA, March 5–9, 2008

45.

Schizas C, Triantafyllopoulos D, Kosmopoulos V, Tzinieris N, Stafylas K (2008) Posterolateral lumbar spine fusion using a novel demineralized bone matrix: a controlled case pilot study. Arch Orthop Trauma Surg 128(6):621–625. doi:10.1007/s00402-007-0495-4 PubMedCrossRef

46.

Cammisa FP Jr, Lowery G, Garfin SR, Geisler FH, Klara PM, McGuire RA, Sassard WR, Stubbs H, Block JE (2004) Two-year fusion 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 (Phila Pa 1976) 29(6):660–666 (pii:00007632-200403150-00010)CrossRef

47.

Price CT, Connolly JF, Carantzas AC, Ilyas I (2003) Comparison of bone grafts for posterior spinal fusion in adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 28(8):793–798 (pii:00007632-200304150-00012)

48.

Weinzapfel B, Son-Hing JP, Armstrong DG, Blakemore LC, Poe-Kochert C, Thompson GH (2008) Fusion rates after thoracoscopic release and bone graft substitutes in idiopathic scoliosis. Spine (Phila Pa 1976) 33(10):1079–1083. doi:10.1097/BRS.0b013e31816f69b3 CrossRef

49.

Feiz-Erfan I, Harrigan M, Sonntag VK, Harrington TR (2007) Effect of autologous platelet gel on early and late graft fusion in anterior cervical spine surgery. J Neurosurg Spine 7(5):496–502. doi:10.3171/SPI-07/11/496 PubMedCrossRef

50.

Jenis LG, Banco RJ, Kwon B (2006) A prospective study of Autologous Growth Factors (AGF) in lumbar interbody fusion. Spine J 6(1):14–20. doi:10.1016/j.spinee.2005.08.014 PubMedCrossRef

51.

Weiner BK, Walker M (2003) Efficacy of autologous growth factors in lumbar intertransverse fusions. Spine (Phila Pa 1976) 28 (17):1968–1970; discussion 1971. doi:10.1097/01.BRS.0000083141.02027.48

52.

Carreon LY, Glassman SD, Anekstein Y, Puno RM (2005) Platelet gel (AGF) fails to increase fusion rates in instrumented posterolateral fusions. Spine (Phila Pa 1976) 30(9):E243–246; discussion E247. pii:00007632-200505010-00026

53.

Tsai CH, Hsu HC, Chen YJ, Lin MJ, Chen HT (2009) Using the growth factors-enriched platelet glue in spinal fusion and its efficiency. J Spinal Disord Tech 22(4):246–250. doi:10.1097/BSD.0b013e3181753ae2 PubMedCrossRef

54.

Castro FP Jr (2004) Role of activated growth factors in lumbar spinal fusions. J Spinal Disord Tech 17(5):380–384. doi:00024720-200410000-00005 PubMedCrossRef

55.

Hee HT, Majd ME, Holt RT, Myers L (2003) Do autologous growth factors enhance transforaminal lumbar interbody fusion? Eur Spine J 12(4):400–407. doi:10.1007/s00586-003-0548-5 PubMedCrossRef

56.

Cho DY, Lee WY, Sheu PC, Chen CC (2005) Cage containing a biphasic calcium phosphate ceramic (Triosite) for the treatment of cervical spondylosis. Surg Neurol 63(6):497–503; discussion 503–494. doi:10.1016/j.surneu.2004.10.016

57.

McConnell JR, Freeman BJ, Debnath UK, Grevitt MP, Prince HG, Webb JK (2003) A prospective randomized comparison of coralline hydroxyapatite with autograft in cervical interbody fusion. Spine (Phila Pa 1976) 28(4):317–323. doi:10.1097/01.BRS.0000048503.51956.E1

58.

Iseda T, Nakano S, Suzuki Y, Miyahara D, Uchinokura S, Moriyama T, Sameshima T, Goya T, Wakisaka S (2000) Radiographic and scintigraphic courses of union in cervical interbody fusion: hydroxyapatite grafts versus iliac bone autografts. J Nucl Med 41(10):1642–1645PubMed

59.

Neen D, Noyes D, Shaw M, Gwilym S, Fairlie N, Birch N (2006) Healos and bone marrow aspirate used for lumbar spine fusion: a case controlled study comparing healos with autograft. Spine (Phila Pa 1976) 31(18):E636–E640. doi:10.1097/01.brs.0000232028.97590.12 CrossRef

60.

Chen WJ, Tsai TT, Chen LH, Niu CC, Lai PL, Fu TS, McCarthy K (2005) The fusion rate of calcium sulfate with local autograft bone compared with autologous iliac bone graft for instrumented short-segment spinal fusion. Spine (Phila Pa 1976) 30(20):2293–2297 (pii:00007632-200510150-00010)CrossRef

61.

Chang CH, Lin MZ, Chen YJ, Hsu HC, Chen HT (2008) Local autogenous bone mixed with bone expander: an optimal option of bone graft in single-segment posterolateral lumbar fusion. Surg Neurol 70 Suppl 1:S1:47–49; discussion S41:49. doi:10.1016/j.surneu.2008.05.022

62.

Dai LY, Jiang LS (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 (Phila Pa 1976) 33(12):1299–1304. doi:10.1097/BRS.0b013e3181732a8e CrossRef

63.

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 Spinal Disord Tech 21(2):106–111. doi:10.1097/BSD.0b013e31805fea1f PubMedCrossRef

64.

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. doi:10.1007/s00586-004-0855-5 PubMedCrossRef

65.

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. doi:10.3171/2010.3.SPINE09603 PubMedCrossRef

66.

Le Huec JC, Lesprit E, Delavigne C, Clement D, Chauveaux D, Le Rebeller A (1997) Tri-calcium phosphate ceramics and allografts as bone substitutes for spinal fusion in idiopathic scoliosis as bone substitutes for spinal fusion in idiopathic scoliosis: comparative clinical results at four years. Acta Orthop Belg 63(3):202–211PubMed

67.

Muschik M, Ludwig R, Halbhubner S, Bursche K, Stoll T (2001) Beta-tricalcium phosphate as a bone substitute for dorsal spinal fusion in adolescent idiopathic scoliosis: preliminary results of a prospective clinical study. Eur Spine J 10(Suppl 2):S178–S184. doi:10.1007/s005860100271 PubMedCrossRef

68.

Delecrin J, Takahashi S, Gouin F, Passuti N (2000) A synthetic porous ceramic as a bone graft substitute in the surgical management of scoliosis: a prospective, randomized study. Spine (Phila Pa 1976) 25(5):563–569CrossRef

69.

Lerner T, Bullmann V, Schulte TL, Schneider M, Liljenqvist U (2009) A level-1 pilot study to evaluate of ultraporous beta-tricalcium phosphate as a graft extender in the posterior correction of adolescent idiopathic scoliosis. Eur Spine J 18(2):170–179. doi:10.1007/s00586-008-0844-1 PubMedCrossRef

70.

Ilharreborde B, Morel E, Fitoussi F, Presedo A, Souchet P, Pennecot GF, Mazda K (2008) Bioactive glass as a bone substitute for spinal fusion in adolescent idiopathic scoliosis: a comparative study with iliac crest autograft. J Pediatr Orthop 28(3):347–351. doi:10.1097/BPO.0b013e318168d1d4 PubMedCrossRef

Title: A systematic review of comparative studies on bone graft alternatives for common spine fusion procedures
Authors: Charla R. Fischer
Ryan Cassilly
Winifred Cantor
Emmanuel Edusei
Qusai Hammouri
Thomas Errico
Publication date: 01-06-2013
Publisher: Springer-Verlag
Published in: European Spine Journal / Issue 6/2013
Print ISSN: 0940-6719
Electronic ISSN: 1432-0932
DOI: https://doi.org/10.1007/s00586-013-2718-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

A systematic review of comparative studies on bone graft alternatives for common spine fusion procedures

Abstract

Background

Purpose

Study design

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Purpose

Study design

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 6/2013

Asymmetry of the cross-sectional area of paravertebral and psoas muscle in patients with degenerative scoliosis

Degenerative lumbar scoliosis in Chinese Han population: prevalence and relationship to age, gender, bone mineral density, and body mass index

Expert’s Comment concerning Grand Rounds Case entitled “Congenital C1 arch deficiency: Grand Round Presentation” (by M. Elmalky, S. Elsayed, G. Arealis, H. Mehdian doi:10.1007/s00586-013-2682-z)

Congenital C1 arch deficiency: Grand Round presentation

The impact of fluorescence guidance on spinal intradural tumour surgery

Association of surgical resection and survival in patients with malignant primary osseous spinal neoplasms from the Surveillance, Epidemiology, and End Results (SEER) database