Human platelet rich plasma plus Persian Gulf coral effects on experimental bone healing in rabbit model: radiological, histological, macroscopical and biomechanical evaluation

  • A. Meimandi Parizi
  • A. Oryan
  • Z. Shafiei-Sarvestani
  • A. S. Bigham
Article

Abstract

Coral is an osteoconductive material used as a bone graft extender and human platelet rich plasma has been used as a source of osteoinductive factor. A combination of human platelet rich plasma and coral is expected to create a composite with both osteoconductive and osteoinductive properties. This study examined the effect of a combination of human platelet rich plasma and coral on osteogenesis in vivo using rabbit model of bone healing. A critical size defect of 10 mm elongation was created in the radial diaphysis of 36 rabbit and either supplied with coral-human PRP, or coral alone or left empty (control group). The platelets in the PRP were about 10.1 fold compared to normal blood. Radiographs of each forelimb was taken postoperatively on 1st day and then at the 2nd, 4th, 6th and 8th weeks post injury to evaluate bone formation, union and remodeling of the defect. The operated radiuses were removed on 56th postoperative day and were grossly and histopathologically evaluated. In addition, biomechanical test was conducted on the operated and normal forearms of the rabbits. This study demonstrated that coral-human PRP (hPRP), could promote bone regeneration in critical size defects with a high regenerative capacity. The results of the present study demonstrated that coral-hPRP could be an attractive alternative for reconstruction of the major diaphyseal defects of the long bones in animal models.

References

  1. 1.
    Arrington ED, Smith WJ, Chambers HG, Bucknell AL, Davino NA. Complications of iliac crest bone graft harvesting. Clin Orthop. 1996;329:300–9.CrossRefGoogle Scholar
  2. 2.
    Damien C, Parsons R. Bone graft and bone graft substitutes: review of current technology and applications. J Appl Biomater. 1991;2:187–208.CrossRefGoogle Scholar
  3. 3.
    Van heest A, Swiontkowski M. Bone-graft substitutes. Lancet. 1999;353:28–9.CrossRefGoogle Scholar
  4. 4.
    Friedlaender GE. Bone grafts: the basic science rationale for clinical applications. J Bone Joint Surg Am. 1987;69:786–90.Google Scholar
  5. 5.
    Inoue K, Ohgushi H, Yoshikawa T, Okumura M, Sempuku T, Tamai S, et al. The effect of aging on bone formation in porous hydroxyapatite: biochemical and histologic analysis. J Bone Miner Res. 1997;12:989–94.CrossRefGoogle Scholar
  6. 6.
    Albrek T, Johansson C. Osteoinduction, osteoconduction and osteointegration. Eur Spine J. 2001;10:S96–101.CrossRefGoogle Scholar
  7. 7.
    Alexander JW. Leonard’s orthopedic surgery of the dog and cat. 3rd ed. Florida: WB Sounders Company; 1985.Google Scholar
  8. 8.
    Alexander JW. Bone grafting. Vet Clin of North Am Small Anim Pract. 1987;17(4):811–9.Google Scholar
  9. 9.
    Brinker WO, Piermattei DL, Flo GL. Bone grafting. Small animal orthopedics and fracture repair. 3rd ed. Florida: WB Saunders Company; 1997. p. 147–53.Google Scholar
  10. 10.
    Fitch R, Kerwin S, Newman-Gage H, Sinibaldi KR. Bone autografts and allografts in dogs. Comp Vet Cont Ed. 1997;19(5):558–75.Google Scholar
  11. 11.
    Fox SM. Cancellous bone grafting in the dog: an overview. J Am Anim Hosp Assoc. 1984;20:840–8.Google Scholar
  12. 12.
    McLaughlin RM, Roush JK. Autogenous cancellous and cortico-cancellous bone grafting. Vet Med. 1998;93(12):1071–4.Google Scholar
  13. 13.
    Lohmann CH, Andreacchio D, Koster G, Carnes DL, Dean BD, Schwartz Z. Tissue response and osteoinduction of human bone grafts in vivo. Arch Orthop Trauma Surg. 2001;121:583–90.CrossRefGoogle Scholar
  14. 14.
    Pokorny JJ, Davids H, Moneim M. Vascularized bone graft for scaphoid nonunion. Tech Hand Up Extrem Surg. 2003;7:32–6.CrossRefGoogle Scholar
  15. 15.
    Bauer TW, Muschler GF. Bone graft materials: an overview of the basic science. Clin Orthop Rel Res. 2000;371:10–27.CrossRefGoogle Scholar
  16. 16.
    Keating JF, McQueen MM. Substitutes for autologous bone graft in orthopaedic trauma. J Bone Joint Surg Am. 2001;83-B:3–8.Google Scholar
  17. 17.
    Kim DH, Jenis L, Berta SC, Vaccaro AR. Bone graft alternatives in spinal fusion surgery. Cur Opin in Orthop. 2003;14:127–37.CrossRefGoogle Scholar
  18. 18.
    Emami MJ, Oryan A, Saeidinasab H, Meimandi Parizi A. The effect of bone marrow graft on bone healing: a radiological and biomechanical study. Iran J Med Sci. 2002;27:63–6.Google Scholar
  19. 19.
    Meimandi Parizi A, Jelodar G, Moslemi H, KT A, Emami MJ. Influence of hydroxyapatite on fracture healing in diabetic rats: biomechanical and radiographic studies. Veterinarski Arhiv. 2010;80:113–20.Google Scholar
  20. 20.
    Meimandi Parizi A, Zeidabadi nejad GR. Biomechanical and radiographical evaluation of the effects of constant direct current on the fracture healing of the radius in the rabbits. J Fac Vet Med Univ Tehran. 1997;52:1–10.Google Scholar
  21. 21.
    Hollinger JO, Brekke J, Gruskin E, Lee D. Role of bone substitutes. Clin Orthop Relat Res. 1996;324:55–65.CrossRefGoogle Scholar
  22. 22.
    Bostrom MP, Saleh KJ, Einhorn TA. Osteoinductive growth factors in preclinical fracture and long bone defects models. Orthop Clin North Am. 1999;30:647–58.CrossRefGoogle Scholar
  23. 23.
    Weibrich G, Kleis WK, Hafner G, Hitzler WE. Growth factor levels in platelet-rich plasma and correlations with donor age, sex, and platelet count. J Craniomaxillofac Surg. 2002;30:97–102.CrossRefGoogle Scholar
  24. 24.
    Marx RE, Carlson ER, Eichstaedt RM, Schimmele SR, Strauss JE, Georgeff KR. Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1998;85:638–46.CrossRefGoogle Scholar
  25. 25.
    McClain SA, Simon M, Jones E, Nandi A, Gailit JO, Tonnesen MG. Mesenchymal cell activation is the rate-limiting step of granulation tissue induction. Am J Pathol. 1996;149:1257–70.Google Scholar
  26. 26.
    Mustoe TA, Pierce GF, Morishima C, Deuel TF. Growth factorinduced acceleration of tissue repair through direct and inductive activities in a rabbit dermal ulcer model. J Clin Invest. 1991;87:694–703.CrossRefGoogle Scholar
  27. 27.
    Saba AA, Freedman BM, Gaffield JW, Mackay DR, Ehrlich HP. Topical platelet-derived growth factor enhances wound closure in the absence of wound contraction: an experimental and clinical study. Ann Plast Surg. 2002;49:62–6.CrossRefGoogle Scholar
  28. 28.
    Aghaloo TL, Moy PK, Freymiller EG. Investigation of platelet-rich plasma in rabbit cranial defects: a pilot study. J Oral Maxillofac Surg. 2002;60:1176–81.CrossRefGoogle Scholar
  29. 29.
    Anitua E. Plasma rich in growth factors: preliminary results of use in the preparation of future sites for implants. Int J Oral Maxillofac Implants. 1999;14:529–35.Google Scholar
  30. 30.
    Kassolis JD, Rosen PS, Reynolds MA. Alveolar ridge and sinus augmentation utilizing platelet-rich plasma in combination with freeze-dried bone allograft: case series. J Periodontol. 2000;71:1654–61.CrossRefGoogle Scholar
  31. 31.
    Nash TJ, Howlett CR, Martin C, Steele J, Johnson KA, Hicklin DJ. Effect of platelet-derived growth factor on tibial osteotomies in rabbits. Bone. 1994;15:203–8.CrossRefGoogle Scholar
  32. 32.
    Robiony M, Polini F, Costa F, Politi M. Osteogenesis distraction and platelet-rich plasma for bone restoration of the severely atrophic mandible: preliminary results. J Oral Maxillofac Surg. 2002;60:630–5.CrossRefGoogle Scholar
  33. 33.
    Rodriguez A, Anastassov GE, Lee H, Buchbinder D, Wettan H. Maxillary sinus augmentation with deproteinated bovine bone and platelet rich plasma with simultaneous insertion of endosseous implants. J Oral Maxillofac Surg. 2003;61:157–63.CrossRefGoogle Scholar
  34. 34.
    Schlegel KA, Donath K, Rupprecht S, Falk S, Zimmermann R, Felszeghy E. De novo bone formation using bovine collagen and platelet-rich plasma. Biomaterials. 2004;25:5387–93.CrossRefGoogle Scholar
  35. 35.
    Froum SJ, Wallace SS, Tarnow DP, Cho SC. Effect of platelet-rich plasma on bone growth and osseointegration in human maxillary sinus grafts: three bilateral case reports. Int J Periodont Restor Dent. 2002;22:45–53.Google Scholar
  36. 36.
    Kim SG, Kim WK, Park JC, Kim HJ. A comparative study of osseointegration of Avana implants in a demineralized freeze-dried bone alone or with platelet-rich plasma. J Oral Maxillofac Surg. 2002;60:1018–25.CrossRefGoogle Scholar
  37. 37.
    Bouchon C, Lebrun T, Rouvillain JL, Roudier M. The Caribbean Scleractinian corals used for surgical implants. Bull Inst Océanogr. 1995;14(3):111–22.Google Scholar
  38. 38.
    Kavousi J, Seyfabadi J, Rezai H, Fenner D. Coral reefs and communities of Qeshm Island, the Persian Gulf. Zool Stud. 2011;50(3):276–83.Google Scholar
  39. 39.
    Ghavam Mostafavi P, Fatemi SMR, Shahhosseiny MH, Hoegh-Guldberg O, WLW K. Predominance of clade D Symbiodinium in shallow-water reef-building corals of Kish and Larak Islands (Persian Gulf, Iran). Mar Biol. 2007;153:25–34.CrossRefGoogle Scholar
  40. 40.
    Guillemin G, Patat JL, Fournie J, Chetail M. The use of coral as a bone graft substitute. J Biomed Mater Res. 1987;21(5):557–67.CrossRefGoogle Scholar
  41. 41.
    Guillemin G, Meunier A, Dallant P, Christel P, Pouliquen J. Comparison of coral resorption and bone apposition with two natural corals of different porosities. J Biomed Mater Res. 1989;23(7):765–79.CrossRefGoogle Scholar
  42. 42.
    Irigaray JL, Oudadesse H, El FH. Effet de la température sur la structure cristalline d’un Biocorail. J Therm Anal. 1993;39:3–14.CrossRefGoogle Scholar
  43. 43.
    Lane JM, Sandhu HS. Current approach to experimental bone grafting. Orthop Clin North Am. 1987;18:213–25.Google Scholar
  44. 44.
    Emery SE, Brazinski MS, Koka A, Bensusan JS, Stevenson S. The biological and biomechanical effects of irradiation on anterior spinal bone grafts in a canine model. J Bone Jt Surg. 1994;76(4):540.Google Scholar
  45. 45.
    An YH, Friedman RJ. Animal models in orthopedic research. 1st ed. Boca Raton: CRC Press Inc.; 1999.Google Scholar
  46. 46.
    Bolander ME, Galian G. The use of demineralize bone matrix in the repair of segmental defect. J Bone Jt Surg. 1983;68A:1264–74.Google Scholar
  47. 47.
    Thorwarth M, Rupprecht S, Falk S, Felszeghy E, Wiltfang J, Schlegel KA. Expression of bone matrix proteins during de novo bone formation using a bovine collagen and platelet-rich plasma (prp)-an immunohistochemical analysis. Biomaterials. 2005;26:2575–84.CrossRefGoogle Scholar
  48. 48.
    Shanaman R, Filstein MR, Danesh-Meyer MJ. Localized ridge augmentation using GBR and platelet-rich plasma: case reports. Int J Oral Maxillofac Implants Periodont Restor Dent. 2001;21:345–55.Google Scholar
  49. 49.
    Raghoebar GM, Schortinghuis J, Liem RS, Ruben JL, van der Wal JE, Vissink A. Does platelet-rich plasma promote remodeling of autologous bone grafts used for augmentation of the maxillary sinus floor? Clin Oral Implants Res. 2005;16:349–56.CrossRefGoogle Scholar
  50. 50.
    Grageda E. Platelet-rich plasma and bone graft materials:a review and a standardized research protocol. Implant Dent. 2004;13(4):301–9.Google Scholar
  51. 51.
    Papa F, Cortese A, Sagliocco R, Farella M, Banzi C, Maltarello MC, et al. Outcome of 47 consecutive sinus lift operations using aragonitic calcium carbonate associated with autologous platelet-rich plasma: clinical, histologic, and histomorphometrical evaluations. J Craniofac Surg. 2009;20(6):2067.CrossRefGoogle Scholar
  52. 52.
    Zhang Y, Wang Y, Shi B, Cheng X. A platelet-derived growth factor releasing chitosan/coral composite scaffold for periodontal tissue engineering. Biomaterials. 2007;28(8):1515–22.CrossRefGoogle Scholar
  53. 53.
    Marx RE. Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg. 2004;62(4):489–96.CrossRefGoogle Scholar
  54. 54.
    Pouliquen JC, Noat M, Verneret C, Guillemin G, Patat J. Coral as a substitute for bone graft in posterior spine fusion in childhood. Fr J Orthop Surg. 1989;3:272–80.Google Scholar
  55. 55.
    Zajour W, Dehoux E, Deprey F, Segal P. Use of coral as a bone graft substitute for anterior fusion of lower spine. Orthop Prod News. 1992:38–9.Google Scholar
  56. 56.
    Roux FX, Brasnu D, Loty B, George B, Guillemin G. Madreporic coral: a new bone graft substitute for cranial surgery. J Neurosurg. 1988;69(4):510–3.CrossRefGoogle Scholar
  57. 57.
    Yukna RA. Clinical evaluation of coralline calcium carbonate as a bone replacement graft material in human periodontal osseous defects. J Periodontol. 1994;65:177–85.Google Scholar
  58. 58.
    Ohgushi H, Goldberg VM, Caplan AI. Repair of bone defects with marrow cells and porous ceramic: experiments in rats. Acta Orthop Scand. 1989;60:334–9.CrossRefGoogle Scholar
  59. 59.
    Ohgushi H, Okumura M, Yoshikawa T, Inboue K, Senpuku N, Tamai S, et al. Bone formation processin porous calcium carbonate and hydroxyapatite. J Biomed Mater Res. 1992;26(7):885–95.CrossRefGoogle Scholar
  60. 60.
    Vuola J, Goransson H, Bohling T, Asko-Seljavaara S. Bone marrow induced osteogenesis in hydroxyapatite and calcium carbonate implants. Biomaterials. 1996;17(18):1761–6.CrossRefGoogle Scholar
  61. 61.
    Petite H, Kacem K, Triffitt JT. Adhesion, growth and differentiation of human bone marrow stromal cells on non-porous calcium carbonate and plastic substrata: effects of dexamethasone and 1, 25 dihydroxyvitamin D3. J Mater Sci Mater in Med. 1996;7:665–71.CrossRefGoogle Scholar
  62. 62.
    Assoian RK, Grotendorst GR, Miller DM, Sporn MB. Cellular transformation by coordinated action of three peptide growth factors from human platelets. Nature. 1984;309:804–6.CrossRefGoogle Scholar
  63. 63.
    Fiedler J, Roderer G, Gunther KP, Brenner RE. BMP-2, BMP-4, and PDGF-bb stimulate chemotactic migration of primary human mesenchymal progenitor cells. J Cell Biochem. 2002;87:305–12.CrossRefGoogle Scholar
  64. 64.
    Baylink DJ, Finkelman RD, Mohan S. Growth factors to stimulate bone formation. J Bone Miner Res. 1993;8:565–72.CrossRefGoogle Scholar
  65. 65.
    Spencer EM, Liu CC, Si EC, Howard GA. In vivo actions of insulinlike growth factor-I (IGF-I) on bone formation and resorption in rats. Bone. 1991;12:21–6.CrossRefGoogle Scholar
  66. 66.
    Street J, Bao M, deGuzman L, Bunting S, Peale JF, Ferrara N. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA. 2002;99:9656–61.CrossRefGoogle Scholar
  67. 67.
    Cook SD. Preclinical and clinical evaluation of osteogenic protein-1 (BMP-7) in bony sites. Orthopedics. 1999;22:669–71.Google Scholar
  68. 68.
    Plachokova AS, van den Dolder J, van den Beucken JJJP, Jansen JA. Bone regenerative properties of rat, goat and human platelet-rich plasma. Int J Oral Maxillofac Implants. 2009;38(8):861–9.CrossRefGoogle Scholar
  69. 69.
    Nash TJ, Howlett CR, Martin C, Steele J, Johnson KA, Hicklin DJ. Effect of platelet-derived growth factor on tibial osteotomies in rabbits. Bone. 1994;15(2):203–8.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • A. Meimandi Parizi
    • 1
  • A. Oryan
    • 2
  • Z. Shafiei-Sarvestani
    • 3
  • A. S. Bigham
    • 4
  1. 1.Department of Veterinary Surgery and Radiology, School of Veterinary MedicineShiraz UniversityShirazIran
  2. 2.Department of Veterinary Pathobiology, School of Veterinary MedicineShiraz UniversityShirazIran
  3. 3.Department of Veterinary Surgery and Radiology, School of Veterinary MedicineShiraz UniversityShirazIran
  4. 4.Department of Veterinary Surgery and Radiology, School of Veterinary MedicineShahrekord UniversityShahrekordIran

Personalised recommendations