Irradiation sterilization used for allogenetic tendon: a literature review of current concept

Abstract

Tendon injury is a very common type of sports trauma, and its incidence has increased over the past decades. Surgical reconstruction with tendon allograft has been increasingly used to restore the motor function and stability of the injured site. However, the risk of disease transmission caused by allogeneic tendon transplantation has been a major problem for tissue bank researchers and clinicians. In order to eliminate the risk of disease transmission, a process of terminal sterilization is necessary. Ionizing irradiation, including gamma irradiation and electron beam irradiation is the most commonly used method for the terminal sterilization, which has been widely proved to be able to effectively inactivate the contained pathogens. Nevertheless, some accompanying damage to the mechanical and histological properties of collagen fibers in tendons will be caused. Therefore, more and more studies have begun to pay attention to the protective effect of radiation protection agents, including the radical scavengers and cross-linking agents, in the irradiation sterilization of allogeneic tendons.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Akkus O, Belaney RM, Das P (2005) Free radical scavenging alleviates the biomechanical impairment of gamma radiation sterilized bone tissue. J Orthop Res 23:838–845

    Article  Google Scholar 

  2. Amiel D, Kuiper S (1990) Experimental studies on anterior cruciate ligament grafts: histology and biochemistry. In: Daniel DM, Akeson WH, O’Connor JJ (eds) Knee ligaments: structure, function, injury, and repair. Raven Press, New York, pp 319–388

    Google Scholar 

  3. Azar FM (2009) Tissue processing: role of secondary sterilization techniques. Clin Sports Med 28:191–201

    Article  Google Scholar 

  4. Bailey AJ (1968) Effect of ionizing radiation on connective tissue components. In: Hall DA (ed) International review of connective tissue research, vol 4. Academic Press, New York, pp 233–281

    Google Scholar 

  5. Bailey AJ, Rhodes DN, Cater CW (1964) Irradiation-induced crosslinking of collagen. Radiat Res 22:606–621

    CAS  Article  Google Scholar 

  6. Bernier J, Hall EJ, Giaccia A (2004) Radiation oncology: a century of achievements. Nat Rev Cancer 4:737–747

    CAS  Article  Google Scholar 

  7. Busch MP, Dodd RY (2000) NAT and blood safety: what is the paradigm? Transfusion 40:1157–1160

    CAS  Article  Google Scholar 

  8. Centers for Disease Control and Prevention (CDC) (2003) Hepatitis C virus transmission from an antibody-negative organ and tissue donor-United States, 2000–2002. MMWR Morb Mortal Wkly Rep 52(13):273-4–276

    Google Scholar 

  9. Cerulli G, Placella G, Sebastiani E et al (2013) ACL reconstruction: choosing the graft. Joints 1(1):18–24

    PubMed  PubMed Central  Google Scholar 

  10. 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

    CAS  Article  Google Scholar 

  11. Cornu O, Boquet J, Nonclercq O, Docquier PL, Van Tomme J, Delloye C, Banse X (2011) Synergetic effect of freeze-drying and gamma irradiation on the mechanical properties of human cancellous bone. Cell Tissue Bank 12(4):281–288

    CAS  Article  Google Scholar 

  12. Cusinato R, Pacenti M, Martello T, Fattori P, Morroni M, Palù G (2016) Effectiveness of hydrogen peroxide and electron-beam irradiation treatment for removal and inactivation of viruses in equine-derived xenografts. J Virol Methods 232:39–46

    CAS  Article  Google Scholar 

  13. De Deyne P, Haut RC (1991) Some effects of gamma irradiation on patellar tendon allografts. Connect Tissue Res 27:51–62

    Article  Google Scholar 

  14. Desobry GE, Boyer AL (1991) Bremsstrahlung review: an analysis of the Schiff spectrum. Med Phys 18(3):497–505

    CAS  Article  Google Scholar 

  15. Dodd RY, Notari EP, Stramer SL (2002) Current prevalence and incidence of infectious disease markers and estimated window-period risk in the American Red Cross blood donor population. Transfusion 42:975–979

    CAS  Article  Google Scholar 

  16. Dziedzic-Goclawska A, Kaminski A, Uhrynowska-Tyszkiewicz I, Stachowicz W (2005) Irradiation as a safety procedure in tissue banking. Cell Tissue Bank 6:201–219

    CAS  Article  Google Scholar 

  17. Elenes EY, Hunter SA (2014) Soft-tissue allografts terminally sterilized with an electron beam are biomechanically equivalent to aseptic, nonsterilized tendons. J Bone Joint Surg Am 96(16):1321–1326

    Article  Google Scholar 

  18. Eyre DR (1990) The collagens of musculoskeletal soft tissues. In: Leadbetter WB, Buckwalter JA, Gordon SL (eds) Sports-induced inflammation. American Academy of Orthopaedic Surgeons, Park Ridge, pp 161–170

    Google Scholar 

  19. Eyre DR, Koob TJ, van Ness KP (1984) Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. Anal Biochem 137:380–388

    CAS  Article  Google Scholar 

  20. Fertey J, Bayer L, Grunwald T, Pohl A, Beckmann J, Gotzmann G, Casado JP, Schönfelder J, Rögner FH, Wetzel C, Thoma M, Bailer SM, Hiller E, Rupp S, Ulbert S (2016) Pathogens Inactivated by low-energy-electron irradiation maintain antigenic properties and induce protective immune responses. Viruses 8(11):pii: E319

    Article  Google Scholar 

  21. Fideler BM, Vangsness CT Jr, Moore T, Li Z, Rasheed S (1994) Effects of gamma irradiation on the human immunodeficiency virus. A study in frozen human bone-patellar ligament-bone grafts obtained from infected cadavera. J Bone Joint Surg Am 76(7):1032–1035

    CAS  Article  Google Scholar 

  22. 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(5):643–646

    CAS  Article  Google Scholar 

  23. Fujimoto D, Akiba K-Y, Nakamura N (1977) Isolation and characterization of a fluorescent material in bovine tendon and dentin. Biochem Biophys Res Commnun 76:1124–1129

    CAS  Article  Google Scholar 

  24. Ganestam A, Kallemose T, Troelsen A et al (2016) Increasing incidence of acute Achilles tendon rupture and a noticeable decline in surgical treatment from 1994 to 2013. A nationwide registry study of 33,160 patients. Knee Surg Sports Traumatol Arthrosc 24(12):3730–3737

    Article  Google Scholar 

  25. Gelberman R, Goldberg V, An KN, Banes A (1988) Tendon. In: Woo SL-Y, Buckwalter JA (eds) Injury and repair of the musculoskeletal soft tissues. American Academy of Orthopaedic Surgeons, Park Ridge, pp 5–40

    Google Scholar 

  26. Gerbi BJ, Antolak JA, Deibel FC, Followill DS, Herman MG, Higgins PD, Huq MS, Mihailidis DN, Yorke ED, Hogstrom KR, Khan FM (2009) Recommendations for clinical electron beam dosimetry: supplement to the recommendations of task group 25. Med Phys 36:3239–3279

    Article  Google Scholar 

  27. Gibbons MJ, Butler DL, Grood ES, Bylski-Austrow DI, Levy MS, Noyes FR (1991) Effects of gamma irradiation on the initial mechanical and material properties of goat bone-patellar tendon-bone allografts. J Orthop Res 9(2):209–218

    CAS  Article  Google Scholar 

  28. Greaves L, Poole N (2008) Bringing sex and gender into women’s substance use treatment programs. Subst Use Misuse 43(8–9):1271–1273

    Article  Google Scholar 

  29. Grieb TA, Forng RY, Bogdansky S, Ronholdt C, Parks B, Drohan WN, Burgess WH, Lin J (2006) High-dose gamma irradiation for soft tissue allografts: high margin of safety with biomechanical integrity. J Orthop Res 24(5):1011–1018

    Article  Google Scholar 

  30. Hafeez YM, Zuki AB, Yusof N, Asnah H, Loqman MY, Noordin MM, Ainul-Yuzairi MY (2005) Effect of freeze-drying and gamma irradiation on biomechanical properties of bovine pericardium. Cell Tissue Bank 6(2):85–89

    CAS  Article  Google Scholar 

  31. Hall EJ (1985) Radiation biology. Cancer 55:2051–2057

    CAS  Article  Google Scholar 

  32. Hawkins CL, Davies MJ (1997) Oxidative damage to collagen and related substrates by metal ion/hydrogen peroxide systems: random attack or site-specific damage? Biochim Biophys Acta 1360:84–96

    CAS  Article  Google Scholar 

  33. Hedbom E, Heinegard D (1993) Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J Biol Chem 268:27307–27312

    CAS  Google Scholar 

  34. Hiemstra H, Tersmette M, Vos AHV, Over J, van Burkel MP, de Bree H (1991) Inactivation of human immunodeficiency virus by gamma irradiation and its effects on plasma and coagulation factors. Transfusion 31(2):32–39

    CAS  Article  Google Scholar 

  35. Hoburg AT, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C, Pruss A, Scheffler S (2010) Effect of electron beam irradiation on biomechanical properties of patellar tendon allografts in anterior cruciate ligament reconstruction. Am J Sports Med 38:1134–1140

    Article  Google Scholar 

  36. Hoburg A, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C, Pruss A, Scheffler S (2011) Fractionation of high-dose electron beam irradiation of BPTB grafts provides significantly improved viscoelastic and structural properties compared to standard gamma irradiation. Knee Surg Sports Traumatol Arthrosc 19(11):1955–1961

    CAS  Article  Google Scholar 

  37. Hoburg A, Keshlaf S, Schmidt T, Smith M, Gohs U, Perka C, Pruss A, Scheffler S (2015) High-dose electron beam sterilization of soft-tissue grafts maintains significantly improved biomechanical properties compared to standard gamma treatment. Cell Tissue Bank 16(2):219–226

    CAS  Article  Google Scholar 

  38. Jones D, Huddleston P, Zobitz M, Stuart MJ (2007) Mechanical properties of patellar tendon allografts subjected to chemical sterilization. Arthroscopy 23:400–404

    Article  Google Scholar 

  39. Kamiński A, Gut G, Marowska J, Lada-Kozłowska M, Biwejnis W, Zasacka M (2009) Mechanical properties of radiation-sterilised human Bone-Tendon-Bone grafts preserved by different methods. Cell Tissue Bank 10(3):215–219

    Article  Google Scholar 

  40. Manjunatha HC (2014) A dosimetric study of Beta induced bremsstrahlung in bone. Appl Radiat Isot 94:282–293

    CAS  Article  Google Scholar 

  41. McAllister DR, Joyce MJ, Mann BJ, Vangsness CT Jr (2007) Allograft update: the current status of tissue regulation, procurement, processing, and sterilization. Am J Sports Med 35(12):2148–2158

    Article  Google Scholar 

  42. McGuire D, Hendricks S (2009) Allograft tissue in ACL reconstruction. Sports Med Arthrosc 17:224–233

    Article  Google Scholar 

  43. Monboisse JC, Borel JP (1992) Oxidative damage to collagen. EXS 62:323–327

    CAS  PubMed  Google Scholar 

  44. Monboisse JC, Gardes-Albert M, Randoux A, Borel JP, Ferradini C (1988) Collagen degradation by superoxide anion in pulse and gamma radiolysis. Biochim Biophys Acta 965:29–35

    CAS  Article  Google Scholar 

  45. Prub A, Katthagen BD (2008) Musculoskeletal tissue banks. Legal foundations and graft safety. Orthopade 37(8):749–755 (in German)

    CAS  Article  Google Scholar 

  46. Pruss A, Caspari G, Krüger DH, Blümel J, Nübling CM, Gürtler L et al (2010) Tissue donation and virus safety: more nucleic acid amplification testing is needed. Transpl Infect Dis 12:375–386

    CAS  Article  Google Scholar 

  47. Rasmussen TJ, Feder SM, Butler DL, Noyes FR (1994) The effects of 4 Mrad of γ irradiation on the initial mechanical properties of bone-patellar tendon-bone grafts. Arthroscopy 10(2):188–197

    CAS  Article  Google Scholar 

  48. Rigney PR (2004) AATB Bulletin No. 04-42 - Implementation of nucleic acid testing (NAT). http://www.aatb.org/files/2004bulletin42.pdf. Accessed 25 Sep 2007

  49. Salehpour A, Butler DL, Proch FS et al (1995) Dose-dependent response of gamma irradiation on mechanical properties and related biochemical composition of goat bone-patellar tendon-bone allografts. J Orthop Res 13(6):898–906

    CAS  Article  Google Scholar 

  50. Schmidt T, Hoburg A, Broziat C, Smith MD, Gohs U, Pruss A, Scheffler S (2012a) Sterilization with electron beam irradiation influences the biomechanical properties and the early remodeling of tendon allografts for reconstruction of the anterior cruciate ligament (ACL). Cell Tissue Bank 13(3):387–400

    CAS  Article  Google Scholar 

  51. Schmidt T, Hoburg AT, Gohs U, Schumann W, Sim-Brandenburg JW, Nitsche A, Scheffler S, Pruss A (2012b) inactivation effect of standard and fractionated electron beam irradiation on enveloped and non-enveloped viruses in a tendon transplant model. Transfus Med Hemother 39(1):29–35

    Article  Google Scholar 

  52. Schmidt T, Grabau D, Grotewohl JH, Gohs U, Pruß A, Smith M, Scheffler S, Hoburg A (2017) Does sterilization with fractionated electron beam irradiation prevent ACL tendon allograft from tissue damage? Knee Surg Sports Traumatol Arthrosc 25(2):584–594

    CAS  Article  Google Scholar 

  53. Schwartz HE, Matava MJ, Proch FS, Butler CA, Ratcliffe A, Levy M, Butler DL (2006) The effect of gamma irradiation on anterior cruciate ligament allograft biomechanical and biochemical properties in the caprine model at time zero and at 6 months after surgery. Am J Sports Med 34(11):1747–1755

    Article  Google Scholar 

  54. Seto A, Gatt CJ Jr, Dunn MG (2008) Radioprotection of tendon tissue via crosslinking and free radical scavenging. Clin Orthop Relat Res 466(8):1788–1795

    Article  Google Scholar 

  55. Seto A, Gatt CJ Jr, Dunn MG (2009) Improved tendon radioprotection by combined cross-linking and free radical scavenging. Clin Orthop Relat Res 467(11):2994–3001

    Article  Google Scholar 

  56. Sheng Z, Sentoku Y, Mima K, Zhang J, Yu W, Meyer-ter-Vehn J (2000) Angular distributions of fast electrons, ions, and Bremsstrahlung x/gamma-rays in intense laser interaction with solid targets. Phys Rev Lett 85(25):5340–5343

    CAS  Article  Google Scholar 

  57. Sikka RS, Narvy SJ, Vangsness CT Jr (2011) Anterior cruciate ligament allograft surgery: underreporting of graft source, graft processing, and donor age. Am J Sports Med 39(3):649–655

    Article  Google Scholar 

  58. Simonds RJ, Holmberg SD, Hurwitz RL, Coleman TR, Bottenfield S, Conley LJ, Kohlenberg SH, Castro KG, Dahan BA, Schable CA et al (1992) Transmission of human immunodeficiency virus type 1 from a seronegative organ and tissue donor. N Engl J Med 326(11):726–732

    CAS  Article  Google Scholar 

  59. Smith RA, Ingels J, Lochemes JJ, Dutkowsky JP, Pifer LL (2001) Gamma irradiation of HIV-1. J Orthop Res 19(5):815–819

    CAS  Article  Google Scholar 

  60. Spire B, Dormont D, Barre-Sinoussi F, Montagnier L, Chermann JC (1985) Inactivation of lympliadenopathy-associated virus by heat, gamma rays, and ultraviolet light. Lancet 1:188–189

    CAS  Article  Google Scholar 

  61. Stramer SL, Glynn SA, Kleinman SH, Strong DM, Caglioti S, Wright DJ, Dodd RY, Busch MP, National Heart, Lung, and Blood Institute Nucleic Acid Test Study Group (2004) Detection of HIV-I and HCV infections among antibodynegative blood donors by nucleic acid-amplification testing. N Eng J Med 351(8):760–768

    CAS  Article  Google Scholar 

  62. Tomford WW, Doppelt SH, Mankin HJ, Friedlaender GE (1983) Bone bank procedures. Clin Orthop Relat Res 174:15–21

    Google Scholar 

  63. Toritsuka Y, Shino K, Horibe S, Nakamura N, Matsumoto N, Ochi T (1997) Effect of freeze-drying or gamma-irradiation on remodeling of tendon allograft in a rat model. J Orthop Res 15(2):294–300

    CAS  Article  Google Scholar 

  64. Vogel KG, Ordog A, Pogany G, Olah J (1993) Proteoglycans in the compressed region of human tibialis posterior tendon and in ligaments. J Orthop Res 11:68–77

    CAS  Article  Google Scholar 

  65. West RV, Harner CD (2005) Graft selection in anterior cruciate ligament reconstruction. J Am Acad Orthop Surg 13(3):197–207

    Article  Google Scholar 

  66. Yusof N (2000) Irradiation for sterilising tissue grafts for viral inactivation. Malays J Nucl Sci 18(1):23–35

    Google Scholar 

  67. Yusof N (2006) Radiation in tissue banking: basic science and clinical applications of irradiated tissue allografts. World Scientific Publishing Co., Ptc. Ltd, Singapore

    Google Scholar 

  68. Zbrojkiewicz D, Vertullo C, Grayson JE (2018) Increasing rates of anterior cruciate ligament reconstruction in young Australians, 2000–2015. Med J Aust 208(8):354–358

    Article  Google Scholar 

Download references

Acknowledgements

I would like to express my special thanks to my partners for the encouragement and support they gave me during my study.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yongcheng Hu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, X., Feng, J., Wang, F. et al. Irradiation sterilization used for allogenetic tendon: a literature review of current concept. Cell Tissue Bank 20, 129–139 (2019). https://doi.org/10.1007/s10561-019-09756-9

Download citation

Keywords

  • Tendon allograft
  • Irradiation sterilization
  • Biomechanics
  • Histological property
  • Radiation protectant