Skip to main content
SpringerLink
Log in

Bone tissue formation in sheep muscles induced by a biphasic calcium phosphate ceramic and fibrin glue composite

  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Some biomaterials are able to induce ectopic bone formation in muscles of large animals. The osteoinductive potential of macro- micro-porous biphasic calcium phosphate (MBCP) ceramic granules with fibrin glue was evaluated by intramuscular implantation for 6 months in six adult female sheep. The MBCP granules were 1–2 mm in size and were composed of hydroxyapatite (HA) and beta-tricalcium phosphate (β-TCP) in a 60/40 ratio. The fibrin glue was composed of fibrinogen, thrombin and other biological factors. After 6 months of implantation in the dorsal muscles of sheep, the explants were rigid. Histology, back-scattered electron microscopy and micro-computed tomography of the implants indicated that approximately 12% of mineralized bone had formed in between the MBCP granules. The ectopic bone appeared well-mineralized with mature osteocytes and Haversian structures. In addition, the number and thickness of bone trabeculae formed in between the MBCP particles were similar to those measured in trabecular bone in sheep. The overall results therefore confirmed the formation of well-mineralized ectopic bone tissue after intramuscular implantation of MBCP/fibrin glue composites. These bone substitutes exhibiting osteoinductive properties could be used for the reconstruction of large bone defects.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. H. BURCHARDT, Orthop. Clin. North Am. 18 (1987) 187

    CAS  Google Scholar 

  2. T. BOYCE, J. EDWARDS and N. SCARBOROUGH, Orthop. Clin. North Am. 30 (1999) 571

    Article  CAS  Google Scholar 

  3. G. DACULSI, O. LABOUX, O. MALARD and P. WEISS, J. Mater. Sci. Mater. Med. 14 (2003) 195

    Article  CAS  Google Scholar 

  4. U. RIPAMONTI, J. CROOKS and A. KIRBRIDE, South Africa J. Sci. 95 (1999) 335

    CAS  Google Scholar 

  5. H. YUAN, M. VAN DEN DOEL, S. LI, C. A. VAN BLITTERSWIJK, K. DE GROOT and J. D. DE BRUIJN, J. Mater. Sci. Mater. Med. 13 (2002) 1271

    Article  CAS  Google Scholar 

  6. P. HABIBOVIC, H. YUAN, C. M. VAN DER VALK, G. MEIJER, C. A. VAN BLITTERSWIJK and K. DE GROOT, Biomaterials 26 (2005) 3565

  7. U. RIPAMONTI, Clin. Orthop. 269 (1991) 284

  8. U. RIPAMONTI, Biomaterials 17 (1996) 31

    Article  CAS  Google Scholar 

  9. H. YUAN, Y. LI, J. D. DE BRUIJN, K. DE GROOT and X. ZHANG, Biomaterials 21 (2000) 1283

    Article  CAS  Google Scholar 

  10. H. YUAN, Z. YANG, J. D. DE BRUIJ, K. DE GROOT and X. ZHANG, Biomaterials 22 (2001) 2617

    Article  CAS  Google Scholar 

  11. F. BARRERE, C. M. VAN DER VALK, R. A. DALMEIJER, G. MEIJER, C. A. VAN BLITTERSWIJK, K. DE GROOT and P. LAYROLLE, J. Biomed. Mater. Res. 66A (2003) 779

    Article  CAS  Google Scholar 

  12. D. M. ALBALA, Cardiovasc. Surg. 11(Suppl 1) (2003) 5

    Article  Google Scholar 

  13. J. M. KARP, F. SARRAF, M. S. SHOICHET and J. E. DAVIES, J. Biomed. Mater. Res. A 71 (2004) 162

    Article  CAS  Google Scholar 

  14. L. LE GUEHENNEC, P. LAYROLLE and G. DACULSI, Eur. Cell. Mater. 8 (2004) 1; discussion 1

  15. E. SOFFER, J. P. OUHAYOUN and F. ANAGNOSTOU, Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 95 (2003) 521

    Article  Google Scholar 

  16. S. ABIRAMAN, H. K. VARMA, P. R. UMASHANKAR and A. JOHN, Biomaterials 23 (2002) 3023

    Article  CAS  Google Scholar 

  17. N. SCHWARZ, Ann. Chir. Gynaecol. Suppl. 207 (1993) 63

    CAS  Google Scholar 

  18. A. R. WITTKAMPF, J. Craniomaxillofac. Surg. 17 (1989) 179

    CAS  Google Scholar 

  19. G. DACULSI, M. BAGOT D’ARC, P. CORLIEU and M. GERSDORFF, Ann. Otol. Rhinol. Laryngol. 101 (1992) 669

    CAS  Google Scholar 

  20. R. E. KANIA, A. MEUNIER, M. HAMADOUCHE, L. SEDEL and H. PETITE, J. Biomed. Mater. Res. 43 (1998) 38

    Article  CAS  Google Scholar 

  21. G. CUNIN, H. BOISSONNET, H. PETITE, C. BLANCHAT and G. GUILLEMIN, Spine 25 (2000) 1070

    Article  CAS  Google Scholar 

  22. M. HALLMAN, A. CEDERLUND, S. LINDSKOG, S. LUNDGREN and L. SENNERBY, Clin. Oral Implants Res. 12 (2001) 135

    Article  CAS  Google Scholar 

  23. D. CARMAGNOLA, T. BERGLUNDH and J. LINDHE, J. Clin. Periodontol. 29 (2002) 377

    Article  CAS  Google Scholar 

  24. M. BAGOT D’ARC and G. DACULSI, J. Mater. Sci. Mater. Med. 14 (2003) 229

    Article  CAS  Google Scholar 

  25. L. LE GUEHENNEC, E. GOYENVALLE, E. AGUADO, P. PILET, M. BAGOT D’Arc, M. BILBAN, R. SPAETHE and G. DACULSI, J. Mater. Sci. Mater. Med. 16 (2005) 29

    Article  CAS  Google Scholar 

  26. R. S. SPITZER, C. PERKA, K. LINDENHAYN and H. ZIPPEL, J. Biomed. Mater. Res. 59 (2002) 690

    Article  CAS  Google Scholar 

  27. O. GUREVICH, A. VEXLER, G. MARX, T. PRIGOZHINA, L. LEVDANSKY, S. SLAVIN, I. SHIMELIOVICH and R. GORODETSKY, Tissue Eng. 8 (2002) 661

    Article  CAS  Google Scholar 

  28. Y. YAMADA, J. S. BOO, R. OZAWA, T. NAGASAKA, Y. OKAZAKI, K. HATA and M. UEDA, J. Craniomaxillofac. Surg. 31 (2003) 27

    Google Scholar 

  29. W. BENSAID, J. T. TRIFFITT, C. BLANCHAT, K. OUDINA, L. SEDEL and H. PETITE, Biomaterials 24 (2003) 2497

    Article  CAS  Google Scholar 

  30. F. JEGOUX, E. GOYENVALLE, M. BAGOT D’ARC, E. AGUADO and G. DACULSI, Arch. Orthop. Trauma Surg. 125 (2005) 153

    Article  Google Scholar 

  31. H. YAMASAKI and H. SAKAI, Biomaterials 13 (1992) 308

    Article  CAS  Google Scholar 

  32. J. M. TOTH, K. L. LYNCH and D. A. HACKBARTH, Bioceramics 6 (1993) 9

    CAS  Google Scholar 

  33. C. KLEIN, K. DE GROOT, W. CHEN, Y. LI and X. Zhang, Biomaterials 15 (1994) 31

    Article  CAS  Google Scholar 

  34. Z. YANG, H. YUAN, W. TONG, P. ZOU, W. CHEN and X. ZHANG, Biomaterials 17 (1996) 2131

    Article  CAS  Google Scholar 

  35. H. YUAN, Z. YANG, Y. LI, X. ZHANG, J. D. DE BRUIJN and K. DE GROOT, J. Mater. Sci. Mater. Med. 9 (1998) 723

    Article  CAS  Google Scholar 

  36. D. LE NIHOUANNEN, G. DACULSI, A. SAFFARZADEH, O. GAUTHIER, S. DELPLACE, P. PILET and P. LAYROLLE, Bone 36 (2005) 1086

    Article  CAS  Google Scholar 

  37. P. HABIBOVIC, J. LI, C. M. VAN DER VALK, G. MEIJER, P. LAYROLLE, C. A. VAN BLITTERSWIJK and K. DE GROOT, Biomaterials 26 (2005) 23

    Article  CAS  Google Scholar 

  38. D. J. GEER, D. D. SWARTZ and S. T. ANDREADIS, Tissue Eng. 8 (2002) 787

    Article  CAS  Google Scholar 

  39. J. W. WEISEL, Biophys. Chem. 112 (2004) 267

    Article  CAS  Google Scholar 

  40. R. R. PFISTER and C. I. SOMMERS, Cornea 24 (2005) 593

    Article  Google Scholar 

  41. N. SCHWARZ, H. REDL, L. ZENG, G. SCHLAG, H. P. DINGES and J. ESCHBERGER, Clin. Orthop. Relat. Res. 293 (1993) 353

  42. H. YUAN, J. D. DE BRUIJN, Y. LI, J. FENG, Z. YANG, K. DE GROOT and X. ZHANG, J. Mater. Sci. Mater. Med. 12 (2001) 7

    Article  CAS  Google Scholar 

  43. G. LI, J. T. RYABY, D. H. CARNEY and H. WANG, J. Orthop. Res. 23 (2005) 196

    Article  CAS  Google Scholar 

  44. M. GEIGER, R. H. LI and W. FRIESS, Adv. Drug Deliv. Rev. 55 (2003) 1613

    Article  CAS  Google Scholar 

  45. M. YAMAMOTO, Y. TAKAHASHI and Y. TABATA, Biomaterials 24 (2003) 4375

    Article  CAS  Google Scholar 

  46. H. YUAN, P. ZOU, Z. YANG, X. ZHANG, J. D. DE BRUIJN and K. DE GROOT, J. Mater. Sci. Mater. Med. 9 (1998) 717

    Article  CAS  Google Scholar 

  47. G. DACULSI, R. Z. LEGEROS, M. HEUGHEBAERT and I. BARBIEUX, Calcif. Tissue Int. 46 (1990) 20

    Article  CAS  Google Scholar 

  48. J. DE GROOT, Tissue Eng. 4 (1998) 337

    Article  Google Scholar 

  49. S. A. KUZNETSOV, M. H. MANKANI, S. GRONTHOS, K. SATOMURA, P. BIANCO and P. G. ROBEY, J. Cell. Biol. 153 (2001) 1133

    Article  CAS  Google Scholar 

  50. P. LAQUERRIERE, A. GRANDJEAN-LAQUERRIERE, E. JALLOT, G. BALOSSIER, P. FRAYSSINET and M. GUENOUNOU, Biomaterials 24 (2003) 2739

    Article  CAS  Google Scholar 

  51. J. LU, M. C. BLARY, S. VAVASSEUR, M. DESCAMPS, K. ANSELME and P. HARDOUIN, J. Mater. Sci. Mater. Med. 15 (2004) 361

    Article  CAS  Google Scholar 

  52. T. R. SANTHOSH KUMAR and L. K.KRISHNAN, Biomaterials 22 (2001) 2769

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported financially by both the “Réseau National des Technologies pour la Santé” (RNTS 2002) and the “Contrat Etat Région” (CER Biomaterials). The authors would like to thank Baxter Bioscience for providing the fibrin glue (Tissucol) and Biomatlante for the biphasic calcium phosphate (TricOs®, Baxter BioSciences BioSurgery, Vienna Austria). We thank Stéphane Grolleau from the Institut des Matériaux de Nantes for measuring specific surface area and François Dulieu, Doctor in Veterinary Medicine, for collecting the μCT of vertebrae.

Author information

Authors and Affiliations

  1. Inserm, U791, Laboratoire d’ingénierie ostéoarticulaire et dentaire, Univ Nantes, Faculté de chirurgie dentaire, 1 place Alexis Ricordeau, Nantes, 44042, France

    Damien Le Nihouannen, Afchine Saffarzadeh, Olivier Gauthier, Françoise Moreau, Paul Pilet, Pierre Layrolle & Guy Daculsi

  2. Ecole Nationale Vétérinaire de Nantes, Service de chirurgie, route de Gachet, Nantes, 44307, France

    Olivier Gauthier

  3. Inserm RIO IFR 26 – 1, place Alexis Ricordeau, Nantes, 44042, France

    Paul Pilet

  4. Baxter BioSciences BioSurgery, Vienna, Austria

    Reiner Spaethe

Authors
  1. Damien Le Nihouannen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Afchine Saffarzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olivier Gauthier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Françoise Moreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paul Pilet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reiner Spaethe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pierre Layrolle
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guy Daculsi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre Layrolle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Nihouannen, D., Saffarzadeh, A., Gauthier, O. et al. Bone tissue formation in sheep muscles induced by a biphasic calcium phosphate ceramic and fibrin glue composite. J Mater Sci: Mater Med 19, 667–675 (2008). https://doi.org/10.1007/s10856-007-3206-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10856-007-3206-3

Keywords

Search

Navigation