Efficacy of platelet concentrates in bone healing: A systematic review on animal studies – Part B: Large-size animal models

References

• Sommeling CE, Heyneman A, Hoeksema H, et al. The use of platelet-rich plasma in plastic surgery: a systematic review. J Plast Reconstr Aesthet Surg 2013;66(3):301–311.
   PubMed Web of Science ®Google Scholar
• Vinaya Kumar R, Shubhashini N. Platelet rich fibrin: a new paradigm in periodontal regeneration. Cell Tissue Bank 2013;14(3):453–463.
   PubMed Web of Science ®Google Scholar
• Alsousou J, Ali A, Willett K, Harrison P. The role of platelet-rich plasma in tissue regeneration. Platelets 2013;24(3):173–182.
   PubMed Web of Science ®Google Scholar
• Dohan DM, 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–e50.
   PubMed Web of Science ®Google Scholar
• 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 clot and membrane. J Periodontol 2010;81(4):546–555.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Dohan Ehrenfest DM, Bielecki T, Jimbo R, Barbe G, Del Corso M, Inchingolo F, Sammartino G. Do the fibrin architecture and leukocyte content influence the growth factor release of platelet concentrates? An evidence-based answer comparing a pure platelet-rich plasma (P-PRP) gel and a leukocyte- and platelet-rich fibrin (L-PRF). Curr Pharm Biotechnol 2012;13(7):1145–1152.
   PubMed Web of Science ®Google Scholar
• Kobayashi E, Flückiger L, Fujioka-Kobayashi M, et al. Comparative release of growth factors from PRP, PRF, and advanced-PRF. Clin Oral Investig 2016;20(9):2353–2360.
   PubMed Web of Science ®Google Scholar
• Schär MO, Diaz-Romero J, Kohl S, et al. Platelet-rich concentrates differentially release growth factors and induce cell migration in vitro. Clin Orthop Relat Res 2015;473(5):1635–1643.
   PubMed Web of Science ®Google Scholar
• Maitz P, Kandler B, Fischer MB, Watzek G, Gruber R. Activated platelets retain their potential to induce osteoclast-like cell formation in murine bone marrow cultures. Platelets 2006;17(7):477–483.
   PubMed Web of Science ®Google Scholar
• Intini G. The use of platelet-rich plasma in bone reconstruction therapy. Biomaterials 2009;30(28):4956–4966.
   PubMed Web of Science ®Google Scholar
• Del Fabbro M, Bortolin M, Taschieri S, Ceci C, Weinstein RL. Antimicrobial properties of platelet-rich preparations. A systematic review of the current pre-clinical evidence. Platelets 2016;27(4):276–285.
   PubMed Web of Science ®Google Scholar
• Nami N, Feci L, Napoliello L, et al. Crosstalk between platelets and PBMC: new evidence in wound healing. Platelets 2016;27(2):143–148.
   PubMed Web of Science ®Google Scholar
• Iqbal J, Pepkowitz SH, Klapper E. Platelet-rich plasma for the replenishment of bone. Curr Osteoporos Rep 2011;9(4):258–263.
   PubMedGoogle Scholar
• Panda S, Doraiswamy J, Malaiappan S, Varghese SS, Del Fabbro M. Additive effect of autologous platelet concentrates in treatment of intrabony defects: a systematic review and meta-analysis. J Investig Clin Dent 2016;7(1):13–26.
   PubMed Web of Science ®Google Scholar
• Griffin XL, Smith CM, Costa ML. The clinical use of platelet-rich plasma in the promotion of bone healing: a systematic review. Injury 2009;40(2):158–162.
   PubMed Web of Science ®Google Scholar
• Peric M, Dumic-Cule I, Grcevic D, et al. The rational use of animal models in the evaluation of novel bone regenerative therapies. Bone 2015;70:73–86.
   PubMed Web of Science ®Google Scholar
• Rodriguez IA, Growney Kalaf EA, Bowlin GL, Sell SA. Platelet-rich plasma in bone regeneration: engineering the delivery for improved clinical efficacy. Biomed Res Int 2014;2014:392398.
   PubMedGoogle Scholar
• Del Fabbro M, Bortolin M, Taschieri S, Weinstein RL. Effect of autologous growth factors in maxillary sinus augmentation: a systematic review. Clin Implant Dent Relat Res 2013;15(2):205–216.
   PubMed Web of Science ®Google Scholar
• Ali S, Bakry SA, Abd-Elhakam H. Platelet-rich fibrin in maxillary sinus augmentation: a systematic review. J Oral Implantol 2015;41(6):746–753.
   PubMed Web of Science ®Google Scholar
• Wroblewski AP, Mejia HA, Wright VJ. Application of platelet-rich plasma to enhance tissue repair. Oper Tech Orthop 2010;20(2):98–105.
   Google Scholar
• Del Fabbro M, Gallesio G, Mozzati M. Autologous platelet concentrates for bisphosphonate-related osteonecrosis of the jaw treatment and prevention. A systematic review of the literature. Eur J Cancer 2015;51(1):62–74.
   PubMed Web of Science ®Google Scholar
• Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010;8(6):e1000412.
   PubMed Web of Science ®Google Scholar
• Liu H-Y, Wu ATH, Tsai C-Y, et al. The balance between adipogenesis and osteogenesis in bone regeneration by platelet-rich plasma for age-related osteoporosis. Biomaterials 2011;32(28):6773–6780.
   PubMed Web of Science ®Google Scholar
• Oryan A, Meimandi Parizi A, Shafiei-Sarvestani Z, Bigham AS. Effects of combined hydroxyapatite and human platelet rich plasma on bone healing in rabbit model: radiological, macroscopical, hidtopathological and biomechanical evaluation. Cell Tissue Bank 2012;13(4):639–651.
   PubMed Web of Science ®Google Scholar
• Parizi AM, Oryan A, Shafiei-Sarvestani Z, Bigham AS. Human platelet rich plasma plus Persian Gulf coral effects on experimental bone healing in rabbit model: radiological, histological, macroscopical and biomechanical evaluation. J Mater Sci Mater Med 2012;23(2):473–483.
   PubMed Web of Science ®Google Scholar
• Tawfik HE, Abu-Seida AM, Hashem AA, El-Khawlani MM. Treatment of experimental furcation perforations with mineral trioxide aggregate, platelet rich plasma or platelet rich fibrin in dogs’ teeth. Exp Toxicol Pathol 2016;68(6):321–327.
   PubMed Web of Science ®Google Scholar
• Hernandez-Fernandez A, Vélez R, Soldado F, et al. Effect of administration of platelet-rich plasma in early phases of distraction osteogenesis: an experimental study in an ovine femur model. Injury 2013;44(7):901–907.
   PubMed Web of Science ®Google Scholar
• Mooren RECM, Dankers ACA, Merkx MAW, et al. The effect of platelet-rich plasma on early and late bone healing using a mixture of particulate autogenous cancellous bone and Bio-Oss: an experimental study in goats. Int J Oral Maxillofac Surg 2010;39(4):371–378.
   PubMed Web of Science ®Google Scholar
• Fennis JPM, Stoelinga PJW, Jansen JA. Mandibular reconstruction: a histological and histomorphometric study on the use of autogenous scaffolds, particulate cortico-cancellous bone grafts and platelet rich plasma in goats. Int J Oral Maxillofac Surg 2004;33(1):48–55.
   PubMed Web of Science ®Google Scholar
• Fennis JPM, Stoelinga PJW, Jansen JA. Mandibular reconstruction: a clinical and radiographic animal study on the use of autogenous scaffolds and platelet-rich plasma. Int J Oral Maxillofac Surg 2002;31(3):281–286.
   PubMed Web of Science ®Google Scholar
• Mooren RECM, Merkx MAW, Bronkhorst EM, Jansen JA, Stoelinga PJW. The effect of platelet-rich plasma on early and late bone healing: an experimental study in goats. Int J Oral Maxillofac Surg 2007;36(7):626–631.
   PubMed Web of Science ®Google Scholar
• Scholz M, Schleicher P, Eindorf T, et al. Cages augmented with mineralized collagen and platelet-rich plasma as an osteoconductive/inductive combination for interbody fusion. Spine (Phila Pa 1976) 2010;35(7):740–746.
   PubMed Web of Science ®Google Scholar
• Jakse N, Tangl S, Gilli R, et al. Influence of PRP on autogenous sinus grafts. An experimental study on sheep. Clin Oral Implants Res 2003;14(5):578–583.
   PubMed Web of Science ®Google Scholar
• Carvalho MD, Suaid FF, Santamaria MP, et al. Platelet-rich plasma plus bioactive glass in the treatment of intra-bony defects: a study in dogs. J Appl Oral Sci 2011;19(1):82–89.
   PubMed Web of Science ®Google Scholar
• Hatakeyama I, Marukawa E, Takahashi Y, Omura K. Effects of platelet-poor plasma, platelet-rich plasma, and platelet-rich fibrin on healing of extraction sockets with buccal dehiscence in dogs. Tissue Eng Part A 2014;20(3–4):874–882.
   PubMed Web of Science ®Google Scholar
• Choi B-H, Im C-J, Huh J-Y, Suh -J-J, Lee S-H. Effect of platelet-rich plasma on bone regeneration in autogenous bone graft. Int J Oral Maxillofac Surg 2004;33(1):56–59.
   PubMed Web of Science ®Google Scholar
• Jungbluth P, Wild M, Grassmann J-P, et al. Platelet-rich plasma on calcium phosphate granules promotes metaphyseal bone healing in mini-pigs. J Orthop Res 2010;28(11):1448–1455.
   PubMed Web of Science ®Google Scholar
• Li H, Zou X, Xue Q, et al. Anterior lumbar interbody fusion with carbon fiber cage loaded with bioceramics and platelet-rich plasma. An experimental study on pigs. Eur Spine J 2004;13(4):354–358.
   PubMed Web of Science ®Google Scholar
• Hakimi M, Jungbluth P, Sager M, et al. Combined use of platelet-rich plasma and autologous bone grafts in the treatment of long bone defects in mini-pigs. Injury 2010;41(7):717–723.
   PubMed Web of Science ®Google Scholar
• Schlegel K, Donath K, Rupprecht S, et al. De novo bone formation using bovine collagen and platelet-rich plasma. Biomaterials 2004;25(23):5387–5393.
   PubMed Web of Science ®Google Scholar
• Gianakos A, Zambrana L, Savage-Elliott I, Lane JM, Kennedy JG. Platelet-rich plasma in the animal long-bone model: an analysis of basic science evidence. Orthopedics 2015;38(12):e1079–90.
   PubMed Web of Science ®Google Scholar
• Tavakolinejad S, Ebrahimzadeh Bidskan A, Ashraf H, Hamidi Alamdari D. A glance at methods for cleft palate repair. Iran Red Crescent Med J 2014;16(9):e15393. doi: 10.5812/ircmj.15393.
   PubMed Web of Science ®Google Scholar
• Del Fabbro M, Corbella S, Taschieri S, Francetti L, Weinstein R. Autologous platelet concentrate for post-extraction socket healing: a systematic review. Eur J Oral Implantol 2014;7(4):333–344.
   PubMed Web of Science ®Google Scholar
• Muschler GF, Raut VP, Patterson TE, et al. The design and use of animal models for translational research in bone tissue engineering and regenerative medicine. Tissue Eng Part B 2010;16(1):123–145.
   PubMed Web of Science ®Google Scholar
• Moran CJ, Ramesh A, Brama PAJ, et al. The benefits and limitations of animal models for translational research in cartilage repair. J Exp Orthop 2016;3(1):1. doi: 10.1186/s40634-015-0037-x.
   PubMedGoogle Scholar
• Tambella AM, Attili AR, Dini F, et al. Autologous platelet gel to treat chronic decubital ulcers: a randomized, blind controlled clinical trial in dogs. Vet Surg 2014;43(6):726–733.
   PubMed Web of Science ®Google Scholar
• Gomes PS, Fernandes MH. Rodent models in bone-related research: the relevance of calvarial defects in the assessment of bone regeneration strategies. Lab Anim 2011;45(1):14–24.
   PubMed Web of Science ®Google Scholar
• Fisher DM, Wong JM-L, Crowley C, Khan WS. Preclinical and clinical studies on the use of growth factors for bone repair: a systematic review. Curr Stem Cell Res Ther 2013;8(3):260–268.
   PubMed Web of Science ®Google Scholar
• Roffi A, Filardo G, Kon E, Marcacci M. Does PRP enhance bone integration with grafts, graft substitutes, or implants? A systematic review. BMC Musculoskelet Disord 2013;14:330. doi: 10.1186/1471-2474-14-330.
   PubMed Web of Science ®Google Scholar
• Plachokova AS, Van Den Dolder J, Jjjp VDB, Jansen JA. Bone regenerative properties of rat, goat and human platelet-rich plasma. Int J Oral Maxillofac Surg 2009;38(8):861–869.
   PubMed Web of Science ®Google Scholar
• Marukawa E, Oshina H, Iino G, Morita K, Omura K. Reduction of bone resorption by the application of platelet-rich plasma (PRP) in bone grafting of the alveolar cleft. J Craniomaxillofac Surg 2011;39(4):278–283.
   PubMed Web of Science ®Google Scholar
• Daif ET. Effect of autologous platelet-rich plasma on bone regeneration in mandibular fractures. Dent Traumatol 2013;29(5):399–403.
   PubMed Web of Science ®Google Scholar
• Lee C, Nishihara K, Okawachi T, et al. A quantitative radiological assessment of outcomes of autogenous bone graft combined with platelet-rich plasma in the alveolar cleft. Int J Oral Maxillofac Surg 2009;38(2):117–125.
   PubMed Web of Science ®Google Scholar
• Wei L-C, Lei G-H, Sheng P, et al. Efficacy of platelet-rich plasma combined with allograft bone in the management of displaced intra-articular calcaneal fractures: a prospective cohort study. J Orthop Res 2012;30(10):1570–1576.
   PubMed Web of Science ®Google Scholar
• Cho A-R, Kim H-K, Kwon J-Y, et al. The incorporation of platelet-rich plasma into calcium phosphate cement enhances bone regeneration in osteoporosis. Pain Physician 2014;17(6):E737–45.
   PubMed Web of Science ®Google Scholar
• Chen L, Yang X, Huang G, et al. Platelet-rich plasma promotes healing of osteoporotic fractures. Orthopedics 2013;36(6):e687–94.
   PubMed Web of Science ®Google Scholar
• Weibrich G, Hansen T, Kleis W, Buch R, Hitzler WE. Effect of platelet concentration in platelet-rich plasma on peri-implant bone regeneration. Bone 2004;34(4):665–671.
   PubMed Web of Science ®Google Scholar
• McCarrel TM, Minas T, Fortier LA. Optimization of leukocyte concentration in platelet-rich plasma for the treatment of tendinopathy. J Bone Joint Surg Am 2012;94(19):e143(1-8).
   PubMedGoogle Scholar
• Bielecki T, Dohan Ehrenfest DM, Everts PA, Wiczkowski A. The role of leukocytes from L-PRP/L-PRF in wound healing and immune defense: new perspectives. Curr Pharm Biotechnol 2012;13(7):1153–1162.
   PubMed Web of Science ®Google Scholar
• Omar OM, Granéli C, Ekström K, et al. The stimulation of an osteogenic response by classical monocyte activation. Biomaterials 2011;32(32):8190–8204.
   PubMed Web of Science ®Google Scholar
• Alexander KA, Chang MK, Maylin ER, et al. Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J Bone Miner Res 2011;26(7):1517–1532.
   PubMed Web of Science ®Google Scholar
• Malhotra A, Pelletier MH, Yu Y, Walsh WR. Can platelet-rich plasma (PRP) improve bone healing? A comparison between the theory and experimental outcomes. Arch Orthop Trauma Surg 2013;133(2):153–165.
   PubMed Web of Science ®Google Scholar
• Bettega G, Brun J-P, Boutonnat J, et al. Autologous platelet concentrates for bone graft enhancement in sinus lift procedure. Transfusion 2009;49(4):779–785.
   PubMed Web of Science ®Google Scholar
• Cieslik-Bielecka A, Bielecki T, Gazdzik TS, Cieslik T, Szczepanski T. Improved treatment of mandibular odontogenic cysts with platelet-rich gel. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105(4):423–429.
   PubMed Web of Science ®Google Scholar
• Christgau M, Moder D, Hiller K-A, et al. Growth factors and cytokines in autologous platelet concentrate and their correlation to periodontal regeneration outcomes. J Clin Periodontol 2006;33(11):837–845.
   PubMed Web of Science ®Google Scholar
• Ouyang X, Qiao J. Effect of platelet-rich plasma in the treatment of periodontal intrabony defects in humans. Chin Med J (Engl) 2006;119(18):1511–1521.
   PubMed Web of Science ®Google Scholar
• Raghoebar GM, Schortinghuis J, Liem RSB, et al. Does platelet-rich plasma promote remodeling of autologous bone grafts used for augmentation of the maxillary sinus floor? Clin. Oral Implants Res 2005;16(3):349–356.
   PubMed Web of Science ®Google Scholar
• Smith SE, Roukis TS. Bone and wound healing augmentation with platelet-rich plasma. Clin Podiatr Med Surg 2009;26(4):559–588.
   PubMedGoogle Scholar
• Penteado LAM, Colombo CED, Penteado RAPM, Assis AO, Gurgel BCV. Evaluation of bioactive glass and platelet-rich plasma for bone healing in rabbit calvarial defects. J Oral Sci 2013;55(3):225–232.
   PubMed Web of Science ®Google Scholar
• Kilborn SH, Trudel G, Uhthoff H. Review of growth plate closure compared with age at sexual maturity and lifespan in laboratory animals. Contemp Top Lab Anim Sci 2002;41(5):21–26.
   PubMedGoogle Scholar
• Emilov-Velev K, Clemente-de-Arriba C, Má A-G, Moreno-Sansalvador EM, Campo-Loarte J. Bone regeneration in experimental animals using calcium phosphate cement combined with platelet growth factors and human growth hormone. Rev Esp Cir Ortop Traumatol 2015;59(3):200–210.
   PubMedGoogle Scholar