Archives of Oral Biology
Volume 55, Issue 3 , Pages 185-194 , March 2010

Choukroun's platelet-rich fibrin (PRF) stimulates in vitro proliferation and differentiation of human oral bone mesenchymal stem cell in a dose-dependent way

  • David M. Dohan Ehrenfest

      Affiliations

    • Department of Biomaterials, Institute for Clinical Sciences, The Sahlgrenska Academy at University of Gothenburg, Sweden
    • The LoB5 Foundation for Research, Paris, France
    • Corresponding Author InformationCorresponding author at: Department of Biomaterials, Institute for Clinical Sciences, The Sahlgrenska Academy at University of Gothenburg, Medicinaregatan 8B, 41390 Gothenburg, Sweden. Tel.: +33 6 64 72 95 40.
    • ,
  • Pierre Doglioli

      Affiliations

    • Cell Culture Laboratory, Jules Ferry Institute, Cannes, France
    • ,
  • Giuseppe M. de Peppo

      Affiliations

    • Department of Biomaterials, Institute for Clinical Sciences, The Sahlgrenska Academy at University of Gothenburg, Sweden
    • ,
  • Marco Del Corso

      Affiliations

    • The LoB5 Foundation for Research, Paris, France
    • ,
  • Jean-Baptiste Charrier

      Affiliations

    • The LoB5 Foundation for Research, Paris, France
    • Department of ENT, Head and Neck Surgery, Paris Sud University, AP-HP Bicêtre Hospital, Le Kremlin Bicêtre, France

,Accepted 15 January 2010.

References 

  1. Dohan Ehrenfest DM, Rasmusson L, Albrektsson T. Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol. 2009;27(3):158–167
  2. Dohan DM, Choukroun J. PRP, cPRP, PRF, PRG, PRGF, FC. How to find your way in the jungle of platelet concentrates?. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(3):305–306
  3. 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(6):638–646
  4. Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part I: technological concepts and evolution. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e37–e44
  5. Keceli HG, Sengun D, Berberoglu A, Karabulut E. Use of platelet gel with connective tissue grafts for root coverage: a randomized-controlled trial. J Clin Periodontol. 2008;35(3):255–262
  6. Graziani F, Ivanovski S, Cei S, Ducci F, Tonetti M, Gabriele M. The in vitro effect of different PRP concentrations on osteoblasts and fibroblasts. Clin Oral Implants Res. 2006;17(2):212–219
  7. Cenni E, Ciapetti G, Pagani S, Perut F, Giunti A, Baldini N. Effects of activated platelet concentrates on human primary cultures of fibroblasts and osteoblasts. J Periodontol. 2005;76(3):323–328
  8. Yamada Y, Ueda M, Naiki T, Takahashi M, Hata K, Nagasaka T. Autogenous injectable bone for regeneration with mesenchymal stem cells and platelet-rich plasma: tissue-engineered bone regeneration. Tissue Eng. 2004;10(5–6):955–964
  9. Oliva A, Passaro I, Di Pasquale R, Di Feo A, Criscuolo M, Zappia V, et al. Ex vivo expansion of bone marrow stromal cells by platelet-rich plasma: a promising strategy in maxillo-facial surgery. Int J Immunopathol Pharmacol. 2005;18(3 Suppl.):47–53
  10. Doucet C, Ernou I, Zhang Y, Llense JR, Begot L, Holy X, et al. Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications. J Cell Physiol. 2005;205(2):228–236
  11. Yamada Y, Ueda M, Hibi H, Nagasaka T. Translational research for injectable tissue-engineered bone regeneration using mesenchymal stem cells and platelet-rich plasma: from basic research to clinical case study. Cell Transplant. 2004;13(4):343–355
  12. Yamada Y, Ueda M, Naiki T, Nagasaka T. Tissue-engineered injectable bone regeneration for osseointegrated dental implants. Clin Oral Implants Res. 2004;15(5):589–597
  13. Ohya M, Yamada Y, Ozawa R, Ito K, Takahashi M, Ueda M. Sinus floor elevation applied tissue-engineered bone. Comparative study between mesenchymal stem cells/platelet-rich plasma (PRP) and autogenous bone with PRP complexes in rabbits. Clin Oral Implants Res. 2005;16(5):622–629
  14. Kinoshita K, Hibi H, Yamada Y, Ueda M. Promoted new bone formation in maxillary distraction osteogenesis using a tissue-engineered osteogenic material. J Craniofac Surg. 2008;19(1):80–87
  15. Ueda M, Yamada Y, Ozawa R, Okazaki Y. Clinical case reports of injectable tissue-engineered bone for alveolar augmentation with simultaneous implant placement. Int J Periodontics Restorative Dent. 2005;25(2):129–137
  16. Kitoh H, Kitakoji T, Tsuchiya H, Katoh M, Ishiguro N. Transplantation of culture expanded bone marrow cells and platelet rich plasma in distraction osteogenesis of the long bones. Bone. 2007;40(2):522–528
  17. Kitoh H, Kitakoji T, Tsuchiya H, Mitsuyama H, Nakamura H, Katoh M, et al. Transplantation of marrow-derived mesenchymal stem cells and platelet-rich plasma during distraction osteogenesis—a preliminary result of three cases. Bone. 2004;35(4):892–898
  18. Kasten P, Vogel J, Luginbuhl R, Niemeyer P, Weiss S, Schneider S, et al. Influence of platelet-rich plasma on osteogenic differentiation of mesenchymal stem cells and ectopic bone formation in calcium phosphate ceramics. Cells Tissues Organs. 2006;183(2):68–79
  19. Dallari D, Fini M, Stagni C, Torricelli P, Nicoli Aldini N, Giavaresi G, et al. In vivo study on the healing of bone defects treated with bone marrow stromal cells, platelet-rich plasma, and freeze-dried bone allografts, alone and in combination. J Orthop Res. 2006;24(5):877–888
  20. Filho Cerruti H, Kerkis I, Kerkis A, Tatsui NH, da Costa Neves A, Bueno DF, et al. Allogenous bone grafts improved by bone marrow stem cells and platelet growth factors: clinical case reports. Artif Organs. 2007;31(4):268–273
  21. Lucarelli E, Fini M, Beccheroni A, Giavaresi G, Di Bella C, Aldini NN, et al. Stromal stem cells and platelet-rich plasma improve bone allograft integration. Clin Orthop Relat Res. 2005;435:62–68
  22. Arpornmaeklong P, Kochel M, Depprich R, Kubler NR, Wurzler KK. Influence of platelet-rich plasma (PRP) on osteogenic differentiation of rat bone marrow stromal cells. An in vitro study. Int J Oral Maxillofac Surg. 2004;33(1):60–70
  23. Vogel JP, Szalay K, Geiger F, Kramer M, Richter W, Kasten P. Platelet-rich plasma improves expansion of human mesenchymal stem cells and retains differentiation capacity and in vivo bone formation in calcium phosphate ceramics. Platelets. 2006;17(7):462–469
  24. Lucarelli E, Beccheroni A, Donati D, Sangiorgi L, Cenacchi A, Del Vento AM, et al. Platelet-derived growth factors enhance proliferation of human stromal stem cells. Biomaterials. 2003;24(18):3095–3100
  25. Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part II: platelet-related biologic features. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e45–50
  26. Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part III: leucocyte activation: a new feature for platelet concentrates?. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e51–e55
  27. Choukroun J, Adda F, Schoeffler C, Vervelle A. Une opportunité en paro-implantologie: le PRF. Implantodontie. 2001;42:55–62
  28. Dohan Ehrenfest DM, Del Corso M, Diss A, Mouhyi J, Charrier JB. Three-dimensional architecture and cell composition of a Choukroun's Platelet-Rich Fibrin (PRF) clot and membrane. J Periodontol; in press.
  29. Dohan Ehrenfest DM, De Peppo GM, Doglioli P, Sammartino G. Slow release of growth factors and thrombospondin-1 in Choukroun's platelet-rich fibrin (PRF): a gold standard to achieve for all surgical platelet concentrates technologies. Growth Factors. 2009;27(1):63–69
  30. Dohan Ehrenfest DM, Diss A, Odin G, Doglioli P, Hippolyte MP, Charrier JB. In vitro effects of Choukroun's PRF (platelet-rich fibrin) on human gingival fibroblasts, dermal prekeratinocytes, preadipocytes and maxillofacial osteoblasts in primary cultures. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108(3):341–352
  31. Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part IV: clinical effects on tissue healing. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):e56–e60
  32. Choukroun J, Diss A, Simonpieri A, Girard MO, Schoeffler C, Dohan SL, et al. Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part V: histologic evaluations of PRF effects on bone allograft maturation in sinus lift. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101(3):299–303
  33. Saadoun AP, Touati B. Soft tissue recession around implants: is it still unavoidable? Part II. Pract Proced Aesthet Dent. 2007;19(2):81–87[quiz 8]
  34. Diss A, Dohan DM, Mouhyi J, Mahler P. Osteotome sinus floor elevation using Choukroun's platelet-rich fibrin as grafting material: a 1-year prospective pilot study with microthreaded implants. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;105(5):572–579
  35. Simonpieri A, Del Corso M, Sammartino G, Dohan Ehrenfest DM. The relevance of Choukroun's platelet rich fibrin (PRF) and metronidazole during complex maxillary rehabilitations using bone allograft. Part I: a new grafting protocol. Implant Dent. 2009;18(2):102–111
  36. Simonpieri A, Del Corso M, Sammartino G, Dohan Ehrenfest DM. The relevance of Choukroun's platelet-rich fibrin (PRF) and metronidazole during complex maxillary rehabilitations using bone allograft. Part II: implant surgery, prosthodontics and survival. Implant Dent. 2009;18(3):220–229
  37. Choukroun JI, Braccini F, Diss A, Giordano G, Doglioli P, Dohan DM. Influence of platelet rich fibrin (PRF) on proliferation of human preadipocytes and tympanic keratinocytes: a new opportunity in facial lipostructure (Coleman's technique) and tympanoplasty?. Rev Laryngol Otol Rhinol (Bord). 2007;128(1–2):27–32
  38. Braccini F, Dohan DM. The relevance of Choukroun's platelet rich fibrin (PRF) during facial aesthetic lipostructure (Coleman's technique): preliminary results. Rev Laryngol Otol Rhinol (Bord). 2007;128(4):255–260
  39. Charrier JB, Monteil JP, Albert S, Collon S, Bobin S, Dohan Ehrenfest DM. Relevance of Choukroun's platelet-rich fibrin (PRF) and SMAS flap in primary reconstruction after superficial or subtotal parotidectomy in patients with focal pleiomorphic adenoma: a new technique. Rev Laryngol Otol Rhinol (Bord). 2008;129(5):313–318
  40. Mazor Z, Horowitz RA, Del Corso M, Prasad HS, Rohrer MD, Dohan Ehrenfest DM. Sinus floor augmentation with simultaneous implant placement using Choukroun's PRF (platelet-rich fibrin) as sole grafting material: a radiological and histological study at 6 months. J Periodontol. 2009;80(12):2056–2064
  41. Del Corso M, Sammartino G, Dohan Ehrenfest DM. Choukroun's platelet-rich fibrin (PRF) membranes in periodontal surgery: understanding the biomaterial or believing into the magic of growth factors?. J Periodontol. 2009;80(11):1694–1697
  42. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63
  43. Dohan DM, Del Corso M, Charrier J-B. Cytotoxicity analyses of Choukroun's PRF (platelet rich fibrin) on a wide range of human cells: the answer to a commercial controversy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(5):587–593
  44. He L, Lin Y, Hu X, Zhang Y, Wu H. A comparative study of platelet-rich fibrin (PRF) and platelet-rich plasma (PRP) on the effect of proliferation and differentiation of rat osteoblasts in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108(5):707–713
  45. Gurevich O, Vexler A, Marx G, Prigozhina T, Levdansky L, Slavin S, et al. Fibrin microbeads for isolating and growing bone marrow-derived progenitor cells capable of forming bone tissue. Tissue Eng. 2002;8(4):661–672
  46. Zhu SJ, Choi BH, Jung JH, Lee SH, Huh JY, You TM, et al. A comparative histologic analysis of tissue-engineered bone using platelet-rich plasma and platelet-enriched fibrin glue. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;102(2):175–179
  47. Ito K, Yamada Y, Naiki T, Ueda M. Simultaneous implant placement and bone regeneration around dental implants using tissue-engineered bone with fibrin glue, mesenchymal stem cells and platelet-rich plasma. Clin Oral Implants Res. 2006;17(5):579–586
  48. Everts PA, van Zundert A, Schonberger JP, Devilee RJ, Knape JT. What do we use: platelet-rich plasma or platelet-leukocyte gel?. J Biomed Mater Res A. 2008;85(4):1135–1136
  49. Cieslik-Bielecka A, Gazdzik TS, Bielecki TM, Cieslik T. Why the platelet-rich gel has antimicrobial activity?. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;103(3):303–305[author reply 5–6]
  50. Moojen DJ, Everts PA, Schure RM, Overdevest EP, van Zundert A, Knape JT, et al. Antimicrobial activity of platelet-leukocyte gel against Staphylococcus aureus. J Orthop Res. 2008;26(3):404–410
  51. El-Sharkawy H, Kantarci A, Deady J, Hasturk H, Liu H, Alshahat M, et al. Platelet-rich plasma: growth factors and pro- and anti-inflammatory properties. J Periodontol. 2007;78(4):661–669
  52. Italiano JE, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, et al. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood. 2008;111(3):1227–1233
  53. Maria OM, Khosravi R, Mezey E, Tran SD. Cells from bone marrow that evolve into oral tissues and their clinical applications. Oral Dis. 2007;13(1):11–16
  54. Igarashi A, Segoshi K, Sakai Y, Pan H, Kanawa M, Higashi Y, et al. Selection of common markers for bone marrow stromal cells from various bones using real-time RT-PCR: effects of passage number and donor age. Tissue Eng. 2007;13(10):2405–2417
  55. Ng AM, Saim AB, Tan KK, Tan GH, Mokhtar SA, Rose IM, et al. Comparison of bioengineered human bone construct from four sources of osteogenic cells. J Orthop Sci. 2005;10(2):192–199

PII: S0003-9969(10)00023-3

doi: 10.1016/j.archoralbio.2010.01.004

Archives of Oral Biology
Volume 55, Issue 3 , Pages 185-194 , March 2010

Article Tools

* Image Usage & Resolution