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The effect of supercritical carbon dioxide sterilization on the anisotropy of bovine cortical bone

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Abstract

Bone allografts are used to replace bone that has been removed or to augment bone tissue in a number of clinical scenarios. In order to minimize the risk of infection and immune response, the bone is delipidated and terminally sterilized prior to implantation. The optimal method for bone graft sterilization has been the topic of considerable research and debate. Recently, supercritical carbon dioxide (SCCO2) treatments have been shown to terminally sterilize bone against a range of bacteria and viruses. This study aimed to evaluate the effect of these SCCO2 treatments on the anisotropic mechanical properties of cortical bone. Adult bovine cortical cubes were prepared and treated using SCCO2 and a range of common processing additives (ethanol, peracetic acid and hydrogen peroxide). The bone was mechanically tested in uniaxial compression in the axial, radial and tangential orientations. Ultimate stress, strain, elastic modulus, energy and stiffness were evaluated. This study found that SCCO2 treatment without additive did not alter the ultimate stress, stiffness or energy to failure depreciably in any orientation. The addition of sterilants peracetic acid and hydrogen peroxide also preserved mechanical function, with no deleterious effect on stress or stiffness. This study highlights the expediency of SCCO2 treatment for bone allograft processing as terminal sterilization can be achieved while maintaining the intrinsic mechanical properties of the graft.

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References

  • 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):716–720

    PubMed  Google Scholar 

  • Akkus O, Belaney RM (2005) Sterilization by gamma radiation impairs the tensile fatigue life of cortical bone by two orders of magnitude. J Orthop Res 23(5):1054–1058. doi:10.1016/j.orthres.2005.03.003

    Article  PubMed  Google Scholar 

  • Akkus O, Rimnac CM (2001) Fracture resistance of gamma radiation sterilized cortical bone allografts. J Orthop Res 19(5):927–934. doi:10.1016/S0736-0266(01)00004-3

    Article  CAS  PubMed  Google Scholar 

  • Anderson MJ, Keyak JH, Skinner HB (1992) Compressive mechanical properties of human cancellous bone after gamma irradiation. J Bone Joint Surg Am 74(5):747–752

    CAS  PubMed  Google Scholar 

  • Barth HD, Zimmermann EA, Schaible E, Tang SY, Alliston T, Ritchie RO (2011) Characterization of the effects of X-ray irradiation on the hierarchical structure and mechanical properties of human cortical bone. Biomaterials 32(34):8892–8904. doi:10.1016/j.biomaterials.2011.08.013

    Article  CAS  PubMed  Google Scholar 

  • Beaupied H, Dupuis A, Arlettaz A, Brunet-Imbault B, Bonnet N, Jaffr C, Benhamou C-L, Courteix D (2006) The mode of bone conservation does not affect the architecture and the tensile properties of rat femurs. Bio Med Mater Eng 16(4):253–259

    Google Scholar 

  • Campbell DG, Li P, Stephenson AJ, Oakeshott RD (1994) Sterilization of HIV by gamma irradiation: a bone allograft model. Int Orthop 18(3):172–176

    Article  CAS  PubMed  Google Scholar 

  • Checinska A, Fruth IA, Green TL, Crawford RL, Paszczynski AJ (2011) Sterilization of biological pathogens using supercritical fluid carbon dioxide containing water and hydrogen peroxide. J Microbiol Methods 87(1):70–75. doi:10.1016/j.mimet.2011.07.008

    Article  CAS  PubMed  Google Scholar 

  • Cornu O, Banse X, Docquier PL, Luyckx S, Delloye C (2000) Effect of freeze-drying and gamma irradiation on the mechanical properties of human cancellous bone. J Orthop Res 18(3):426–431. doi:10.1002/jor.1100180314

    Article  CAS  PubMed  Google Scholar 

  • Currey JD, Foreman J, Laketic I, Mitchell J, Pegg DE, Reilly GC (1997) Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res 15(1):111–117. doi:10.1002/jor.1100150116

    Article  CAS  PubMed  Google Scholar 

  • DePaula CA, Truncale KG, Gertzman AA, Sunwoo MH, Dunn MG (2005) Effects of hydrogen peroxide cleaning procedures on bone graft osteoinductivity and mechanical properties. Cell Tissue Bank 6(4):287–298. doi:10.1007/s10561-005-3148-2

    Article  CAS  PubMed  Google Scholar 

  • Dillow AK, Dehghani F, Hrkach JS, Foster NR, Langer R (1999) Bacterial inactivation by using near- and supercritical carbon dioxide. Proc Natl Acad Sci USA 96(18):10344–10348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dul’neva LV, Moskvin AV (2005) Kinetics of formation of peroxyacetic acid. Rus J Gen Chem 75(7):1125–1130. doi:10.1007/s11176-005-0378-8

    Article  Google Scholar 

  • Evans FG (1969) The mechanical properties of bone. Artif Limb 13(1):37–48

    CAS  Google Scholar 

  • Fages J, Marty A, Delga C, Condoret JS, Combes D, Frayssinet P (1994) Use of supercritical CO2 for bone delipidation. Biomaterials 15(9):650–656

    Article  CAS  PubMed  Google Scholar 

  • Fages J, Poirier B, Barbier Y, Frayssinet P, Joffret ML, Majewski W, Bonel G, Larzul D (1998) Viral inactivation of human bone tissue using supercritical fluid extraction. ASAIO J 44(4):289–293

    Article  CAS  PubMed  Google Scholar 

  • Frayssinet P, Rouquet N, Mathon D, Autefage A, Fages J (1998) Histological integration of allogeneic cancellous bone tissue treated by supercritical CO2 implanted in sheep bones. Biomaterials 19(24):2247–2253

    Article  CAS  PubMed  Google Scholar 

  • Gerd B (2005) Supercritical fluids: technology and application to food processing. J Food Eng 67(1–2):21–33. doi:10.1016/j.jfoodeng.2004.05.060

    Google Scholar 

  • Hamer AJ, Strachan JR, Black MM, Ibbotson CJ, Stockley I, Elson RA (1996) Biochemical properties of cortical allograft bone using a new method of bone strength measurement: a comparison of fresh, fresh-frozen and irradiated bone. J Bone Joint Surg Br 78(3):363–368

    CAS  PubMed  Google Scholar 

  • Hamer AJ, Stockley I, Elson RA (1999) Changes in allograft bone irradiated at different temperatures. J Bone Joint Surg Br 81(2):342–344

    Article  CAS  PubMed  Google Scholar 

  • Hemmer JD, Drews MJ, LaBerge M, Matthews MA (2007) Sterilization of bacterial spores by using supercritical carbon dioxide and hydrogen peroxide. J Biomed Mater Res B 80(2):511–518. doi:10.1002/jbm.b.30625

    Article  Google Scholar 

  • Lietman SA, Tomford WW, Gebhardt MC, Springfield DS, Mankin HJ (2000) Complications of irradiated allografts in orthopaedic tumor surgery. Clin Orthop Relat Res 375:214–217

    Article  PubMed  Google Scholar 

  • Linde F, Sørensen HCF (1993) The effect of different storage methods on the mechanical properties of trabecular bone. J Biomech 26(10):1249–1252. doi:10.1016/0021-9290(93)90072-M

    Article  CAS  PubMed  Google Scholar 

  • Mitchell EJ, Stawarz AM, Kayacan R, Rimnac CM (2004) The effect of gamma radiation sterilization on the fatigue crack propagation resistance of human cortical bone. J Bone Joint Surg Am 86(12):2648–2657

    PubMed  Google Scholar 

  • Mitton D, Rappeneau J, Bardonnet R (2005) Effect of a supercritical CO2 based treatment on mechanical properties of human cancellous bone. Eur J Orthop Surg Traumatol 15(4):264–269. doi:10.1007/s00590-005-0250-x

    Article  Google Scholar 

  • Nguyen H, Morgan DA, Forwood MR (2007a) Sterilization of allograft bone: effects of gamma irradiation on allograft biology and biomechanics. Cell Tissue Bank 8(2):93–105. doi:10.1007/s10561-006-9020-1

    Article  PubMed  Google Scholar 

  • Nguyen H, Morgan DA, Forwood MR (2007b) Sterilization of allograft bone: is 25 kGy the gold standard for gamma irradiation? Cell Tissue Bank 8(2):81–91. doi:10.1007/s10561-006-9019-7

    Article  PubMed  Google Scholar 

  • Nguyen H, Gineyts E, Wu A, Cassady A, Bennett M, Morgan DAF, Delmas P, Forwood M (2012) Degradation of allograft bone mechanical and biological properties by gamma irradiation can be explained by alteration to the collagen triple helix, rather than collagen cross-links. J Bone Joint Surg Br 94-B(SUPP XXIII):125

    Google Scholar 

  • Nguyen H, Cassady AI, Bennett MB, Gineyts E, Wu A, Morgan DAF, Forwood MR (2013) Reducing the radiation sterilization dose improves mechanical and biological quality while retaining sterility assurance levels of bone allografts. Bone 57(1):194–200. doi:10.1016/j.bone.2013.07.036

    Article  CAS  PubMed  Google Scholar 

  • Nichols A, Burns D, Christopher R (2009) Studies on the sterilization of human bone and tendon musculoskeletal allograft tissue using supercritical carbon dioxide. J Orthop 6(2):e9

    Google Scholar 

  • Novitskaya E, Chen P-Y, Lee S, Castro-Ceseña A, Hirata G, Lubarda VA, McKittrick J (2011) Anisotropy in the compressive mechanical properties of bovine cortical bone and the mineral and protein constituents. Acta Biomater 7(8):3170–3177. doi:10.1016/j.actbio.2011.04.025

    Article  CAS  PubMed  Google Scholar 

  • Pietrzak WS, Woodell-May J (2005) The composition of human cortical allograft bone derived from FDA/AATB-screened donors. J Craniofac Surg 16(4):579–585

    Article  PubMed  Google Scholar 

  • Qiu Q–Q, Leamy P, Brittingham J, Pomerleau J, Kabaria N, Connor J (2009) Inactivation of bacterial spores and viruses in biological material using supercritical carbon dioxide with sterilant. J Biomed Mater Res B 91B(2):572–578. doi:10.1002/jbm.b.31431

    Article  CAS  Google Scholar 

  • Reilly DT, Burstein AH (1974) Review article: the mechanical properties of cortical bone. J Bone Joint Surg Am 56(5):1001–1022

    CAS  PubMed  Google Scholar 

  • Reilly DT, Burstein AH (1975) The elastic and ultimate properties of compact bone tissue. J Biomech 8(6):393–405

    Article  CAS  PubMed  Google Scholar 

  • Russell NA, Pelletier MH, Bruce WJ, Walsh WR (2012) The effect of gamma irradiation on the anisotropy of bovine cortical bone. Med Eng Phys 34(8):1117–1122. doi:10.1016/j.medengphy.2011.11.021

    Article  PubMed  Google Scholar 

  • Russell N, Rives A, Bertollo N, Pelletier MH, Walsh WR (2013a) The effect of sterilization on the dynamic mechanical properties of paired rabbit cortical bone. J Biomech 46(10):1670–1675. doi:10.1016/j.jbiomech.2013.04.006

    Article  PubMed  Google Scholar 

  • Russell N, Rives A, Pelletier M, Bruce W, Walsh W (2013b) The effect of sterilization on the mechanical properties of intact rabbit humeri in three-point bending, four-point bending and torsion. Cell Tissue Bank 14(2):231–242. doi:10.1007/s10561-012-9318-0

    Article  PubMed  Google Scholar 

  • Seiler JG 3rd, Johnson J (2000) Iliac crest autogenous bone grafting: donor site complications. J South Orthop Assoc 9(2):91–97

    PubMed  Google Scholar 

  • Shieh E, Paszczynski A, Wai CM, Lang Q, Crawford RL (2009) Sterilization of Bacillus pumilus spores using supercritical fluid carbon dioxide containing various modifier solutions. J Microbial Methods 76(3):247–252

    Article  CAS  Google Scholar 

  • Spilimbergo S, Dehghani F, Bertucco A, Foster NR (2003) Inactivation of bacteria and spores by pulse electric field and high pressure CO2 at low temperature. Biotechnol Bioeng 82(1):118–125. doi:10.1002/bit.10554

    Article  CAS  PubMed  Google Scholar 

  • Thoren K, Aspenberg P (1995) Ethylene oxide sterilization impairs allograft incorporation in a conduction chamber. Clin Orthop Relat Res 318:259–264

    PubMed  Google Scholar 

  • Thoren K, Aspenberg P, Thorngren KG (1995) Lipid extracted bank bone: bone conductive and mechanical properties. Clin Orthop Relat Res 311:232–246

    PubMed  Google Scholar 

  • Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14(4):595–608

    Article  CAS  PubMed  Google Scholar 

  • Unger S, Blauth M, Schmoelz W (2010) Effects of three different preservation methods on the mechanical properties of human and bovine cortical bone. Bone 47(6):1048–1053. doi:10.1016/j.bone.2010.08.012

    Article  PubMed  Google Scholar 

  • Vaccaro AR, Chiba K, Heller JG, Patel TC, Thalgott JS, Truumees E, Fischgrund JS, Craig MR, Berta SC, Wang JC (2002) Bone grafting alternatives in spinal surgery. Spine J 2(3):206–215. doi:10.1016/s1529-9430(02)00180-8

    Article  PubMed  Google Scholar 

  • Wang T, Feng Z (2005) Dynamic mechanical properties of cortical bone: the effect of mineral content. Mater Lett 59(18):2277–2280. doi:10.1016/j.matlet.2004.08.048

    Article  CAS  Google Scholar 

  • Watanabe T, Furukawa S, Hirata J, Koyama T, Ogihara H, Yamasaki M (2003) Inactivation of Geobacillus stearothermophilus spores by high-pressure carbon dioxide treatment. Appl Environ Microb 69(12):7124–7129

    Article  CAS  Google Scholar 

  • White A, Burns D, Christensen TW (2006) Effective terminal sterilization using supercritical carbon dioxide. J Biotechnol 123(4):504–515. doi:10.1016/j.jbiotec.2005.12.033

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Burrows S, Gleason C, Matthews MA, Drews MJ, Laberge M, An YH (2006) Sterilizing Bacillus pumilus spores using supercritical carbon dioxide. J Microbial Meth 66(3):479–485. doi:10.1016/j.mimet.2006.01.012

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to acknowledge funding support for this research was provided by a grant from the Australian Orthopaedic Association.

Conflict of interest

The authors declare there are no conflicts of interest in the preparation of this manuscript.

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Authors and Affiliations

  1. Surgical and Orthopaedic Research Laboratories, Prince of Wales Clinical School, University of New South Wales, Sydney, Australia

    Nicholas Russell, Alain Rives, Matthew H. Pelletier, Tian Wang & William R. Walsh

  2. Surgical and Orthopaedic Research Laboratories, Prince of Wales Hospital, Level 1 Clinical Sciences Building, Avoca St Randwick, Sydney, NSW, 2031, Australia

    William R. Walsh

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  1. Nicholas Russell
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  2. Alain Rives
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  3. Matthew H. Pelletier
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  4. Tian Wang
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Correspondence to William R. Walsh.

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Russell, N., Rives, A., Pelletier, M.H. et al. The effect of supercritical carbon dioxide sterilization on the anisotropy of bovine cortical bone. Cell Tissue Bank 16, 109–121 (2015). https://doi.org/10.1007/s10561-014-9447-8

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  • DOI: https://doi.org/10.1007/s10561-014-9447-8

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