Skip to main content

Advertisement

SpringerLink
Log in

Sterilization of allograft bone: effects of gamma irradiation on allograft biology and biomechanics

  • Review Paper
  • Published:
Cell and Tissue Banking Aims and scope Submit manuscript

Abstract

Gamma irradiation from Cobalt 60 sources has been used to terminally sterilize bone allografts for many years. Gamma radiation adversely affects the mechanical and biological properties of bone allografts by degrading the collagen in bone matrix. Specifically, gamma rays split polypeptide chains. In wet specimens irradiation causes release of free radicals via radiolysis of water molecules that induces cross-linking reactions in collagen molecules. These effects are dose dependent and give rise to a dose-dependent decrease in mechanical properties of allograft bone when gamma dose is increased above 25 kGy for cortical bone or 60 kGy for cancellous bone. But at doses between 0 and 25 kGy (standard dose), a clear relationship between gamma dose and mechanical properties has yet to be established. In addition, the effects of gamma radiation on graft remodelling have not been intensively investigated. There is evidence that the activity of osteoclasts is reduced when they are cultured onto irradiated bone slices, that peroxidation of marrow fat increases apoptosis of osteoblasts; and that bacterial products remain after irradiation and induce inflammatory bone resorption following macrophage activation. These effects need considerably more investigation to establish their relevance to clinical outcomes. International consensus on an optimum dose of radiation has not been achieved due to a wide range of confounding variables and individual decisions by tissue banks. This has resulted in the application of doses ranging from 15 to 35 kGy. Here, we provide a critical review on the effects of gamma irradiation on the mechanical and biological properties of allograft bone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • AATB (ed) (2002) Standards for tissue banking, American Association of Tissue Banking, MD

  • 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 23:1054-058

    Article  PubMed  Google Scholar 

  • Akkus O, Belaney RM, Das P (2005) Free radical scavenging alleviates the biomechanical impairment of gamma radiation sterilized bone tissue. J Orthop Res 23:838-45

    Article  PubMed  Google Scholar 

  • Akkus O, Rimnac CM (2001) Fracture resistance of gamma radiation sterilized cortical bone allografts. J Orthop Res 19:927-34

    Article  CAS  PubMed  Google Scholar 

  • An HY (2000) Mechanical properties of bone. In: An HY, Draughn AR (eds) Mechanical testing of bone and bone-implant interface. CRC Press, Boca Raton, pp 41-3

  • Anderson MJ, Keyak JH, Skinner HB (1992) Compressive mechanical-properties of human cancellous bone after gamma-irradiation. J Bone Joint Surg-Am 74A:747-52

    Google Scholar 

  • Andre LP, Liz AG-ER (2000) Proposed donor screening questionnaire. Cell Tissue Bank 1:149-53

    Article  Google Scholar 

  • Angermann P, Jepsen OB (1991) Procurement, banking and decontamination of bone and collagenous tissue allografts: guidelines for infection control. J Hosp Infect 17:159-69

    Article  CAS  PubMed  Google Scholar 

  • Arora M, Shah N, Meghji S, et al (1998) Effect of Staphylococcus aureus extracellular proteinaceous fraction in an isolated osteoclastic resorption assay. J Bone Miner Metab 16:158-61

    Article  CAS  Google Scholar 

  • Aspenberg P, Tagil M, Kristensson C, Lidin S (1996) Bone graft proteins influence osteoconduction—a titanium chamber study in rats. Acta Orthop Scand 76:377-82

    Google Scholar 

  • Bailey DA, Martin AD, McKay HA, Whiting S, Mirwald R (2000) Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 15:2245-0

    Article  CAS  PubMed  Google Scholar 

  • Boyce T, Edwards J, Scarborough N (1999) Allograft bone—the influence of processing on safety and performance. Orthop Clin North Am 30:571-81

    Article  CAS  PubMed  Google Scholar 

  • Buring K, Urist RM (1967) Effects of ionizing radiation on the bone induction principle in the matrix of bone implants. Clin Orthop 55:225-34

    CAS  PubMed  Google Scholar 

  • Campbell DG, Li P. (1999) Sterilization of HIV with irradiation: relevance to infected bone allografts. Aust NZ J Surg 69:517-21

    Article  CAS  Google Scholar 

  • Chapman PG, Villar RN (1992) The bacteriology of bone allografts. J Bone Joint Surg Br 74:398-99

    CAS  PubMed  Google Scholar 

  • Colwell A, Hamer A, Blumsohn A, Eastell R (1996) To determine the effects of ultraviolet light, natural light and ionizing radiation on pyridinium cross-links in bone and urine using high-performance liquid chromatography. Eur J Clin Invest 26:1107-114

    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 18:426-31

    Article  CAS  PubMed  Google Scholar 

  • Cornu O, Bavadekar A, Godts B, et al (2003) Impaction bone grafting with freeze-dried irradiated bone. Part II Changes in stiffness and compactness of morselized grafts—experiments in cadavers. Acta Orthop Scand 74:553-58

    PubMed  Google Scholar 

  • Currey JD, Foreman J, Laketic I, et al (1997) Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res 15:111-17

    Article  CAS  PubMed  Google Scholar 

  • Davy DT (1999) Biomechanical issues in bone transplantation. Orthop Clin N Am 30:553-63

    Article  CAS  Google Scholar 

  • Diab T, Condon KW, Burr DB, Vashishth D (2005) Age-related change in the damage morphology of human cortical bone and its role in bone fragility bone

  • Dziedzic-Goclawska A, Kaminski A, Uhrynowska-Tyszkiewicz I, Stachowicz W (2005) Irradiation as a safety procedure in tissue banking. Cell Tissue Bank 6:201-19

    Article  CAS  PubMed  Google Scholar 

  • Dziedzic-Goclawska A, Ostrowski K, Stachowicz W, Michalik J, Grzesik W (1991) Effect of radiation sterilization on the osteoinductive properties and the rate of remodeling of bone implants preserved by lyophilization and deep-freezing. Clin Orthop 30-7

  • Eastlund DT, Strong DM (2003) Infectious disease transmission through tissue transplantation. In: Phillips GO (ed) Advances in tissue banking. World Scientific Publishing, Singapore, pp 51-31

    Google Scholar 

  • Enneking WE, Campanacci DA (2001) Retrieved human allografts—a clinicopathological study. J Bone Joint Surg Am 83A:971-86

    Google Scholar 

  • Enneking WF, Mindell ER (1991) Observations on massive retrieved human allografts. J Bone Joint Surg Am 73A:1123-142

    Google Scholar 

  • Fideler BM, Vangsness CT Jr, Lu B, Orlando C, Moore T (1995) Gamma irradiation: effects on biomechanical properties of human bone-patellar tendon-bone allografts. Am J Sports Med 23:643-46

    Article  CAS  PubMed  Google Scholar 

  • Forwood MR, Bailey DA, Beck TJ, et al (2004) Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone 35:973-81

    Article  PubMed  Google Scholar 

  • Gibbons MJ, Butler DL, Grood ES, et al (1991) Effects of gamma-irradiation on the initial mechanical and material properties of goat bone-patellar tendon-bone allografts. J Orthop Res 9:209-18

    Article  CAS  PubMed  Google Scholar 

  • Godette GA, Kopta JA, Egle DM (1996) Biomechanical effects of gamma irradiation on fresh frozen allografts in vivo. Orthopedics 19:649-53

    CAS  PubMed  Google Scholar 

  • Grieb TA, Forng R-Y, Stafford RE, et al (2005) Effective use of optimized, high-dose (50 kGy) gamma irradiation for pathogen inactivation of human bone allografts. Biomaterials 26:2033-042

    Article  CAS  PubMed  Google Scholar 

  • Hallfeldt KKJ, Stutzle H, Puhlmann M, Kessler S, Schweiberer L (1995) Sterilization of partially demineralized bone-matrix—the effects of different sterilization techniques on osteogenetic properties. J Surg Res 59:614-20

    Article  PubMed  Google Scholar 

  • Hamer AJ, Stockley I, Elson RA (1999) Changes in allograft bone irradiated at different temperatures. J Bone Joint Surg Br 81:342-44

    Article  CAS  PubMed  Google Scholar 

  • Hamer AJ, Strachan JR, Black MM, et al. (1996) Biomechanical 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 78B:363-68

    Google Scholar 

  • Heiple KG, Goldberg VM, Powell AE, Bos GD, Zika JM (1987) Biology of cancellous bone-grafts. Orthop Clin N Am 18:179-85

    CAS  Google Scholar 

  • Hernigou P, Delepine G, Goutallier D, Julieron A (1993) Massive allografts sterilised by irradiation. Clinical results J Bone Joint Surg Br 75:904-13

    CAS  Google Scholar 

  • Hernigou P, Gras G, Marinello G, Dormont D (2000) Inactivation of HIV by application of heat and radiation: implication in bone banking with irradiated allograft bone. Acta Orthop Scand 71:508-12

    Article  CAS  PubMed  Google Scholar 

  • Heyligers IC, Klein-Nulend J (2005) Detection of living cells in non-processed but deep-frozen bone allografts. Cell Tissue Bank 6:25-1

    Article  PubMed  Google Scholar 

  • Hong CY, Lin SK, Kok SH, et al (2004) The role of lipopolysaccharide in infectious bone resorption of periapical lesion. J Oral Pathol Med 33:162-69

    Article  CAS  PubMed  Google Scholar 

  • Hornicek FJ, Gebhardt MC, Tomford WW, et al (2001) Factors affecting nonunion of the allograft-host junction. Clin Orthop 87-8

  • IAEA (2002) International standards on tissue banking—first meeting of the IAEA technical advisory committee. In: Committee ITA (ed) The IAEA programme in radiation and tissue banking. IAEA, Boston, USA, pp 44

    Google Scholar 

  • Ijiri S, Yamamuro T, Nakamura T, Kotani S, Notoya K (1994) Effect of sterilization on bone morphogenetic protein. J Orthop Res 12:628-36

    Article  CAS  PubMed  Google Scholar 

  • James LA, Gower A. (2002) The clinical significance of femoral head culture results in donors after hip arthroplasty—a preliminary report. J Arthroplasty 17:355-58

    Article  CAS  PubMed  Google Scholar 

  • Jiang YL, Mehta CK, Hsu TY, Alsulaimani FFH (2002) Bacteria induce osteoclastogenesis via an osteoblast-independent pathway. Infect Immun 70:3143-148

    Article  CAS  PubMed  Google Scholar 

  • Jinno T, Miric A, Kirk S, Davy D, Stevenson S (2000) The effects of processing and low dose irradiation on cortical bone grafts. J Clin Orthopa Relat Res 375:275-85

    Article  Google Scholar 

  • Kalfas I (2001) Principles of bone healing Neurosurg. Focus 10:1-

    Article  Google Scholar 

  • Kennedy JF, Phillips GO, Williams PA (2005) Sterilisation of tissues using ionising radiation. CRC Press LLC, Boca Raton, Florida

    Google Scholar 

  • Khan SN, Cammisa FP, Sandha HS, et al (2005) The biology of bone grafting. J Am Acad Orthop Surg 13:77-6

    PubMed  Google Scholar 

  • Kingsmill VJ, Boyde A, Jones SJ (1999) The resorption of vital and devitalized bone in vitro: significance for bone grafts. Calcif Tissue Int 64:252-56

    Article  CAS  PubMed  Google Scholar 

  • Kluger R, Bouhon W, Freudenberger H, et al (2003) Removal of the surface layers of human cortical bone allografts restores in vitro osteoclast function reduced by processing and frozen storage. Bone 32:291-96

    Article  CAS  PubMed  Google Scholar 

  • Lee FYI, Hazan EJ, Gebhardt MC, Mankin HJ (2000) Experimental model for allograft incorporation and allograft fracture repair. J Orthop Res 18:303-06

    Article  CAS  PubMed  Google Scholar 

  • Lietman AS, Tomford WW, Gebhardt CM, Springfield SD, Mankin JM (2000) Complications os irradiated allografts in orthopaedic tumor surgery. J Clin Orthopaedic Relat Res 375:214-17

    Article  Google Scholar 

  • Liu JW, Chao LH, Su LH, Wang JW, Wang CJ (2002) Experience with a bone bank operation and allograft bone infection in recipients at a medical centre in southern Taiwan. J Hosp Infect 50:293-97

    Article  CAS  PubMed  Google Scholar 

  • Loty B, Courpied JP, Tomeno B, et al. (1990) Bone allografts sterilised by irradiation. Biological properties, procurement and results of 150 massive allografts. Int Orthop 14:237-42

    CAS  PubMed  Google Scholar 

  • Meghji S, Crean SJ, Hill PA, et al. (1998) Surface-associated protein from Staphylococcus aureus stimulates osteoclastogenesis: possible role in S-aureus-induced bone pathology. Br J Rheumatol 37:1095-101

    Article  CAS  PubMed  Google Scholar 

  • Meghji S, Crean SJ, Nair S, et al. (1997a) Staphylococcus epidermidis produces a cell-associated proteinaceous fraction which causes bone resorption by a prostanoid-independent mechanism: Relevance to the treatment of infected orthopaedic implants. Br J Rheumatol 36:957-63

    Article  CAS  Google Scholar 

  • Meghji S, Henderson B, Nair SP, Tufano MA (1997b) Bacterial porins stimulate bone resorption. Infect Immun 65:1313-316

    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. Bone Joint Sur 86-A:2648-657

    Google Scholar 

  • Moreau MF, Gallois Y, Basle MF, Chappard D (2000) Gamma irradiation of human bone allografts alters medullary lipids and releases toxic compounds for osteoblast-like cells. Biomaterials 21:369-76

    Article  CAS  PubMed  Google Scholar 

  • Mosekilde L (1986) Normal vertebral body size and compressive strength: relations to age and to vertebral and iliac trabecular bone compressive strength. Bone 7:207-12

    Article  CAS  PubMed  Google Scholar 

  • Muldashev ER, Muslimov SA, Musina LA, Nigmatulin RT, Lebedeva AI (2005) The role of macrophage in the tissue regeneration stimulated by the biomaterials. Cell Tissue Bank 6:99-07

    Article  CAS  PubMed  Google Scholar 

  • Munting E, Wilmart JF, Wijne A, Hennebert P, Delloye C (1988) Effect of sterilization on osteoinduction—comparison of 5 methods in demineralized rat bone. Acta Orthop Scand 59:34-8

    CAS  PubMed  Google Scholar 

  • Nair S, Song Y, Meghji S, et al (1995) Surface-associated proteins from Staphylococcus-aureus demonstrate potent bone-resorbing activity. J Bone Miner Res 10:726-34

    Article  CAS  PubMed  Google Scholar 

  • Nair SP, Meghji S, Wilson M, et al. (1996) Bacterially induced bone destruction: mechanisms and misconceptions. Infect Immun 64:2371-380

    CAS  PubMed  Google Scholar 

  • Pelker RR, McKay J, Troiano N, Panjabi MM, Friedlaender GE (1989) Allograft incorporation—a biomechanical evaluation in a rat model. J Orthop Res 7:585-89

    Article  CAS  PubMed  Google Scholar 

  • Puolakkainen PA, Ranchalis JE, Strong DM, Twardzik DR (1993) The effect of sterilization on transforming growth-factor-beta isolated from demineralized human bone transfusion (Paris). 33:679-85

  • Rasmussen TJ, Feder SM, Butler DL, Noyes FR (1994) The effects of 4 mrad of gamma-irradiation on the initial mechanical-properties of bone patellar tendon bone-grafts arthroscopy, 10:188-97

  • Salehpour A, Butler DL, Proch E, et al. (1995) Dose-dependent response of gamma irradiation on mechanical properties and related biochemical composition of coat bone-patellar tendon-bone allografts. J Orthop Res 13:898-06

    Article  CAS  PubMed  Google Scholar 

  • Schachar N, Fennel C, Otsuka T, Ladd A (2002) Bone grafts and bone subtitutes. In: R., F. H., H., K. and A., M. L. (eds) Orthopaedics. St. Louis, Mosby, pp 186-94

  • Schuster JM, Avellino AM, Mann FA, et al (2000) Use of structural allografts in spinal osteomyelitis: a review of 47 cases. J Neurosurg 93:8-4

    CAS  PubMed  Google Scholar 

  • Simonian PT, Conrad EU, Chapman JR, Harrington RM, Chansky HA (1994) Effect of sterilization and storage treatments on screw pullout strength in human allograft bone. Clin Orthop 290-96

  • Smith CW, Young IS, Kearney JN (1996) Mechanical properties of tendons: changes with sterilization and preservation. J Biomech Eng-Trans Asme 118:56-1

    Article  CAS  Google Scholar 

  • Sommerville SMM, Johnson N, Bryce SL, Journeaux SF, Morgan DAF (2000) Contamination of banked femoral head allograft: incidence, bacteriology and donor follow up. Aust N Z J Surg 70:480-84

    Article  CAS  PubMed  Google Scholar 

  • Triantafyllou E, Sotiropoulos E, Triantafyllou JN (1975) The mechanical properties of the lymphylized and Irradiated bone grafts. Acta Orthopeadica Belgica 41:35-4

    Google Scholar 

  • Urist, MR, Hernandez, A. (1974) Excitation transfer in bone. Deleterious effects of cobalt 60 radiation-sterilization of bank bone. Arch Surg 109:586-93

    CAS  PubMed  Google Scholar 

  • Vastel L, Meunier A, Siney H, Sedel L, Courpied JP (2004) Effect of different sterilization processing methods on the mechanical properties of human cancellous bone allografts. Biomaterials 25:2105-110

    Article  CAS  PubMed  Google Scholar 

  • Voggenreiter G, Ascherl R, Blumel G, SchmitNeuerburg KP (1996) Extracorporeal irradiation and incorporation of bone grafts- autogeneic cortical grafts studied in rats. Acta Orthop Scand 67:583-88

    Article  CAS  PubMed  Google Scholar 

  • Wientroub S, Reddi HA (1988) Influence of irradiation on the osteoindictive potential of demineralized bone matrix calcif. Tissue Int 42:255-60

    Article  CAS  Google Scholar 

  • Zhang YX, Homsi D, Gates K, et al. (1994) A comprehensive study of physical parameters, biomechanical properties, and statistical correlations of iliac crest bone wedges used in spinal-fusion surgery 4. Effect of gamma-irradiation on mechanical and material properties Spine 19:304-08

    CAS  Google Scholar 

  • Zioupos P, Smith WC, An HY (2000) Factors effecting mechanical properties of bone. In: An HY, Draughn AR (eds) Mechanical testing of bone and bone-implant interface. pp 65-5

  • Zubillaga G, Von Hagen S, Simon BI, Deasy MJ (2003). Changes in alveolar bone height and width following post-extraction ridge augmentation using a fixed bioabsorbable membrane and demineralized freeze-dried bone osteoinductive graft. J Periodontol 74:965-75

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Developmental Biology, The University of Queensland, School of Biomedical Sciences, Brisbane, Qld, 4072, Australia

    Huynh Nguyen & Mark R. Forwood

  2. The University of Queensland, Brisbane Private Hospital, Brisbane, Australia, 4000

    David A. F. Morgan

  3. Queensland Bone Bank, Brisbane, Australia

    Huynh Nguyen & David A. F. Morgan

Authors
  1. Huynh Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. F. Morgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark R. Forwood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark R. Forwood.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nguyen, H., Morgan, D.A.F. & Forwood, M.R. Sterilization of allograft bone: effects of gamma irradiation on allograft biology and biomechanics. Cell Tissue Banking 8, 93–105 (2007). https://doi.org/10.1007/s10561-006-9020-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10561-006-9020-1

Keywords

Search

Navigation