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Platelet-Rich Plasma in Regenerative Medicine

  • Joseph Alsousou
  • Paul HarrisonEmail author
Chapter

Abstract

The clinical application of platelet-rich plasma (PRP) has been increasing sharply in the last two decades. Its role as a potential regenerative agent and ease of application have allowed it to take huge share in the fast-evolving biological therapy field. The reported effect of PRP on a range of tissue types including bone, cartilage, tendon and muscle has attracted clinical interest in fields such as trauma, orthopaedic, maxillofacial and plastic surgery where effective healing of tissues is critical for successful outcome. The results of in vitro and animal studies that largely report positive effects of PRP on cellular and matrix regeneration have been the main drive for its translation to clinical settings. Despite the lack of appropriately powered trials, PRP administration remains an attractive strategy given its cost-effective, minimally invasive nature and the autologous nature of PRP. In this chapter, the current literature on the use of PRP in regenerative medicine is reviewed highlighting both some of the controversy surrounding this approach and some emerging clinical applications. A new PRP classification system is presented to allow better description of the variable clinical PRP products and their correlated outcome.

Keywords

Anterior Cruciate Ligament Cartilage Oligomeric Matrix Protein Bovine Thrombin Growth Factor Content Chronic Tendinopathy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Akeda K, An HS, Okuma M et al (2006) Platelet-rich plasma stimulates porcine articular chondrocyte proliferation and matrix biosynthesis. Osteoarthritis Cartilage 14:1272–1280PubMedCrossRefGoogle Scholar
  2. Almdahl SM, Veel T, Halvorsen P et al (2011) Randomized prospective trial of saphenous vein harvest site infection after wound closure with and without topical application of autologous platelet-rich plasma. Eur J Cardiothorac Surg 39:44–48PubMedCrossRefGoogle Scholar
  3. Alsousou J (2014) Platelet rich plasma in regenerative tendon repair mechanobiological interactions and clinical application. In: University of Oxford dgi (ed) Thesis (D. Phil.) University of Oxford, 2013Google Scholar
  4. Alsousou J, Thompson M, Hulley P et al (2009) The biology of platelet-rich plasma and its application in trauma and orthopaedic surgery: a review of the literature. J Bone Joint Surg Br 91:987–996PubMedCrossRefGoogle Scholar
  5. Alsousou J, Hulley P, Thompson M, Mcnally E, Willett K (2010) The effect of platelet rich plasma (PRP) on tendon regeneration: an in vitro tissue culture study. In: International Symposium on Ligament and Tendon XI. ISL&T, University of California, p 58Google Scholar
  6. Alsousou J, Ali A, Willett K et al (2013) The role of platelet-rich plasma in tissue regeneration. Platelets 24:173–182PubMedCrossRefGoogle Scholar
  7. Anitua E, Andia I, Ardanza B et al (2004) Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb Haemost 91:4–15PubMedGoogle Scholar
  8. Anitua E, Andí I, Sanchez M et al (2005) Autologous preparations rich in growth factors promote proliferation and induce VEGF and HGF production by human tendon cells in culture. J Orthop Res 23:281–286PubMedCrossRefGoogle Scholar
  9. Anonymous (2015) Platelet rich plasma in Achilles tendon healing: PATH-2 TrialGoogle Scholar
  10. Arpornmaeklong P, Kochel M, Depprich R et al (2004) Influence of platelet-rich plasma (PRP) on osteogenic differentiation of rat bone marrow stromal cells. An in vitro study. Int J Oral Maxillofac Surg 33:60–70PubMedCrossRefGoogle Scholar
  11. Aspenberg P, Virchenko O (2004) Platelet concentrate injection improves Achilles tendon repair in rats. Acta Orthop Scand 75:93–99PubMedCrossRefGoogle Scholar
  12. Balbo R, Avonto I, Marenchino D et al (2010) Platelet gel for the treatment of traumatic loss of finger substance. Blood Transfus 8:255–259PubMedPubMedCentralGoogle Scholar
  13. Bertoldi C, Pinti M, Zaffe D et al (2009) Morphologic, histochemical, and functional analysis of platelet-rich plasma activity on skeletal cultured cells. Transfusion 49:1728–1737PubMedCrossRefGoogle Scholar
  14. Bertrand-Duchesne MP, Grenier D, Gagnon G (2010) Epidermal growth factor released from platelet-rich plasma promotes endothelial cell proliferation in vitro. J Periodontal Res 45:87–93PubMedCrossRefGoogle Scholar
  15. Bielecki T, Dohan Ehrenfest DM, Everts PA et al (2012) The role of leukocytes from L-PRP/L-PRF in wound healing and immune defense: new perspectives. Curr Pharm Biotechnol 13:1153–1162PubMedCrossRefGoogle Scholar
  16. Bir SC, Esaki J, Marui A et al (2011) Therapeutic treatment with sustained-release platelet-rich plasma restores blood perfusion by augmenting ischemia-induced angiogenesis and arteriogenesis in diabetic mice. J Vasc Res 48:195–205PubMedCrossRefGoogle Scholar
  17. Bosch G, Van Schie HT, De Groot MW et al (2010) Effects of platelet-rich plasma on the quality of repair of mechanically induced core lesions in equine superficial digital flexor tendons: a placebo-controlled experimental study. J Orthop Res 28:211–217PubMedGoogle Scholar
  18. Broggini N, Hofstetter W, Hunziker E et al (2011) The influence of PRP on early bone formation in membrane protected defects. A histological and histomorphometric study in the rabbit calvaria. Clin Implant Dent Relat Res 13:1–12PubMedCrossRefGoogle Scholar
  19. Castelnovo L, Dosquet C, Gaudric A et al (2000) Human platelet suspension stimulates porcine retinal glial proliferation and migration in vitro. Invest Ophthalmol Vis Sci 41:601–609PubMedGoogle Scholar
  20. Castricini R, Longo UG, De Benedetto M et al (2011) Platelet-rich plasma augmentation for arthroscopic rotator cuff repair: a randomized controlled trial. Am J Sports Med 39:258–265PubMedCrossRefGoogle Scholar
  21. Cattaneo M, Cerletti C, Harrison P et al (2013) Recommendations for the standardization of light transmission aggregometry: a Consensus of the Working Party from the Platelet Physiology Subcommittee of SSC/ISTH. J Thromb Haemost 11:1183–1189CrossRefGoogle Scholar
  22. Cenni E, Fotia C, Rustemi E et al (2011) Idiopathic and secondary osteonecrosis of the femoral head show different thrombophilic changes and normal or higher levels of platelet growth factors. Acta Orthop 82:42–49PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cervelli V, Lucarini L, Spallone D et al (2010) Use of platelet rich plasma and hyaluronic acid on exposed tendons of the foot and ankle. J Wound Care 19(186):188–190Google Scholar
  24. Cervelli V, Gentile P, De Angelis B et al (2011a) Application of enhanced stromal vascular fraction and fat grafting mixed with PRP in post-traumatic lower extremity ulcers. Stem Cell Res 6:103–111PubMedCrossRefGoogle Scholar
  25. Cervelli V, Lucarini L, Spallone D et al (2011b) Use of platelet-rich plasma and hyaluronic acid in the loss of substance with bone exposure. Adv Skin Wound Care 24:176–181PubMedCrossRefGoogle Scholar
  26. Cheng M, Wang H, Yoshida R et al (2010) Platelets and plasma proteins are both required to stimulate collagen gene expression by anterior cruciate ligament cells in three-dimensional culture. Tissue Eng Part A 16:1479–1489PubMedPubMedCentralCrossRefGoogle Scholar
  27. Choi BH, Zhu SJ, Kim BY et al (2005) Effect of platelet-rich plasma (PRP) concentration on the viability and proliferation of alveolar bone cells: an in vitro study. Int J Oral Maxillofac Surg 34:420–424PubMedCrossRefGoogle Scholar
  28. Cieslik-Bielecka A, Bielecki T, Gazdzik TS et al (2009) Autologous platelets and leukocytes can improve healing of infected high-energy soft tissue injury. Transfus Apher Sci 41:9–12PubMedCrossRefGoogle Scholar
  29. Cmolik BL, Spero JA, Magovern GJ (1993) Redo cardiac surgery: Late bleeding complications from topical thrombin induced factor five deficiency. J Thorac Cardiovasc Surg 105:222–227PubMedGoogle Scholar
  30. Coppinger JA, Toomey S et al (2004) Characterization of the protein released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood 103:2096–2104PubMedCrossRefGoogle Scholar
  31. Creaney L, Wallace A, Curtis M et al (2011) Growth factor-based therapies provide additional benefit beyond physical therapy in resistant elbow tendinopathy: a prospective, single-blind, randomised trial of autologous blood injections versus platelet-rich plasma injections. Br J Sports Med 45:966–971PubMedCrossRefGoogle Scholar
  32. Creeper F, Lichanska AM, Marshall RI et al (2009) The effect of platelet-rich plasma on osteoblast and periodontal ligament cell migration, proliferation and differentiation. J Periodontal Res 44:258–265PubMedCrossRefGoogle Scholar
  33. Crovetti G, Martinelli G, Issi M et al (2004) Platelet gel for healing cutaneous chronic wounds. Transfus Apher Sci 30:145–151PubMedCrossRefGoogle Scholar
  34. Curi MM, Cossolin GS, Koga DH et al (2007) Treatment of avascular osteonecrosis of the mandible in cancer patients with a history of bisphosphonate therapy by combining bone resection and autologous platelet-rich plasma: report of 3 cases. J Oral Maxillofac Surg 65:349–355PubMedCrossRefGoogle Scholar
  35. De Mos M, Van Der Windt AE, Jahr H et al (2008) Can platelet-rich plasma enhance tendon repair? a cell culture study. Am J Sports Med 36:1171–1178PubMedCrossRefGoogle Scholar
  36. De Vos RJ, Van Veldhoven PL, Moen MH et al (2010a) Autologous growth factor injections in chronic tendinopathy: a systematic review. Br Med Bull 95:63–77PubMedCrossRefGoogle Scholar
  37. De Vos RJ, Weir A, Van Schie HTM et al (2010b) Platelet-rich plasma injection for chronic achilles tendinopathy: a randomized controlled trial. JAMA 303:144–149PubMedCrossRefGoogle Scholar
  38. De Vos RJ, Weir A, Tol JL et al (2011) No effects of PRP on ultrasonographic tendon structure and neovascularisation in chronic midportion Achilles tendinopathy. Br J Sports Med 45:387–392PubMedCrossRefGoogle Scholar
  39. Derossi R, Coelho AC, Mello GS et al (2009) Effects of platelet-rich plasma gel on skin healing in surgical wound in horses. Acta Cir Bras 24:276–281PubMedCrossRefGoogle Scholar
  40. Dohan Ehrenfest DM, Rasmusson L, Albrektsson T (2009) Classification of platelet concentrates: from pure platelet-rich plasma (P-PRP) to leucocyte- and platelet-rich fibrin (L-PRF). Trends Biotechnol 27:158–167PubMedCrossRefGoogle Scholar
  41. Dohan Ehrenfest DM, Bielecki T, Mishra A et al (2012) In search of a consensus terminology in the field of platelet concentrates for surgical use: platelet-rich plasma (PRP), platelet-rich fibrin (PRF), fibrin gel polymerization and leukocytes. Curr Pharm Biotechnol 13:1131–1137PubMedCrossRefGoogle Scholar
  42. Dragica SBG, Dragoslav D, Primo R (2007) Allogeneic platelet gel with autologous cancellous bone graft for the treatment of a large bone defect. Eur Surg Res 39:170–174CrossRefGoogle Scholar
  43. Driver VR, Hanft J, Fylling CP et al (2006) A prospective, randomized, controlled trial of autologous platelet-rich plasma gel for the treatment of diabetic foot ulcers. Ostomy Wound Manage 52:68–70, 72, 74 passimPubMedGoogle Scholar
  44. Duan J, Kuang W, Tan J et al (2011) Differential effects of platelet rich plasma and washed platelets on the proliferation of mouse MSC cells. Mol Biol Rep 38:2485–2490PubMedCrossRefGoogle Scholar
  45. Engebretsen L, Steffen K, Alsousou J et al (2010) IOC consensus paper on the use of platelet-rich plasma in sports medicine. Br J Sports Med 44:1072–1081PubMedCrossRefGoogle Scholar
  46. Everts PA, Brown Mahoney C, Hoffmann JJ, Schönberger JP, Box HA, van Zundert A, Knape JT (2006) Platelet-rich plasma preparation using three devices: implications for platelet activation and platelet growth factor release. Growth Factors 24:165–171PubMedCrossRefGoogle Scholar
  47. Feng Y, Sun Y, Jia W et al (2010) Platelet-rich plasma and 1,25(OH)2 vitamin D3 synergistically stimulate osteogenic differentiation of adult human mesenchymal stem cells. Biotechnol Lett 32:635–642PubMedCrossRefGoogle Scholar
  48. Fennis JP, Stoelinga PJ, Jansen JA (2002) Mandibular reconstruction: a clinical and radiographic animal study on the use of autogenous scaffolds and platelet-rich plasma. Int J Oral Maxillofac Surg 31:281–286PubMedCrossRefGoogle Scholar
  49. Franklin S, Zargar N, Willett K et al (2012) Human tenocyte cellular signalling response in the presence of platelet-rich concentrate. J Bone Joint Surg 94-B:6Google Scholar
  50. Frykberg RG, Driver VR, Carman D et al (2010) Chronic wounds treated with a physiologically relevant concentration of platelet-rich plasma gel: a prospective case series. Ostomy Wound Manage 56:36–44PubMedGoogle Scholar
  51. Fufa D, Shealy B, Jacobson M et al (2008) Activation of platelet-rich plasma using soluble type I collagen. J Oral Maxillofac Surg 66:684–690PubMedPubMedCentralCrossRefGoogle Scholar
  52. Gandhi A, Bibbo C, Pinzur M et al (2005) The role of platelet-rich plasma in foot and ankle surgery. Foot Ankle Clin 10:621–637, viiiPubMedCrossRefGoogle Scholar
  53. Gaweda K, Tarczynska M, Krzyzanowski W (2010) Treatment of Achilles tendinopathy with platelet-rich plasma. Int J Sports Med 31:577–583PubMedCrossRefGoogle Scholar
  54. Gentile P, Cervelli V (2010) Autologous platelet-rich plasma: guidelines in plastic surgery. Plast Reconstr Surg 126:269e–270ePubMedCrossRefGoogle Scholar
  55. Gibble JW, Ness PM (1990) Fibrin glue: the perfect operative sealant? Transfusion 30:741–747PubMedCrossRefGoogle Scholar
  56. Giovanini AF, Gonzaga CC, Zielak JC et al (2011) Platelet-rich plasma (PRP) impairs the craniofacial bone repair associated with its elevated TGF-beta levels and modulates the co-expression between collagen III and alpha-smooth muscle actin. J Orthop Res 29:457–463PubMedCrossRefGoogle Scholar
  57. Gosens T, Peerbooms JC, Van Laar W et al (2011) Ongoing positive effect of platelet-rich plasma versus corticosteroid injection in lateral epicondylitis: a double-blind randomized controlled trial with 2-year follow-up. Am J Sports Med 39:1200–1208PubMedCrossRefGoogle Scholar
  58. Hadad I, Johnstone BH, Brabham JG et al (2010) Development of a porcine delayed wound-healing model and its use in testing a novel cell-based therapy. Int J Radiat Oncol Biol Phys 78:888–896PubMedCrossRefGoogle Scholar
  59. Hamilton B, Knez W, Eirale C et al (2010) Platelet enriched plasma for acute muscle injury. Acta Orthop Belg 76:443–448PubMedGoogle Scholar
  60. Harrison P (2004) Measuring platelet function? Hematol J 5(Suppl 3):S164–169PubMedCrossRefGoogle Scholar
  61. Harrison P, Mumford A, Briggs C, Liesner R, Winter M, Machin S (2011a) BCSH guidelines for platelet function testing. Br J Haematol and BCSH website 155(1):30–44CrossRefGoogle Scholar
  62. Harrison S, Vavken P, Kevy S, Jackobson M, Zurakowski D, Murray M (2011b) Platelet activation by collagen provides sustained release of anabolic cytokines. Am J Sports Med 39:729–734PubMedPubMedCentralCrossRefGoogle Scholar
  63. Hartmann EK, Heintel T, Morrison RH et al (2010) Influence of platelet-rich plasma on the anterior fusion in spinal injuries: a qualitative and quantitative analysis using computer tomography. Arch Orthop Trauma Surg 130:909–914PubMedCrossRefGoogle Scholar
  64. Herouy Y, Mellios P, Bandemir E et al (2000) Autologous platelet-derived wound healing factor promotes angiogenesis via alphavbeta3-integrin expression in chronic wounds. Int J Mol Med 6:515–519PubMedGoogle Scholar
  65. Ho CH, Chan IH (1995) The influence of time of storage, temperature of storage, platelet number in platelet-rich plasma, packed cell, mean platelet volume, hemoglobin concentration, age, and sex on platelet aggregation test. Ann Hematol 71:129–133PubMedCrossRefGoogle Scholar
  66. Huang S, Wang Z (2010) Influence of platelet-rich plasma on proliferation and osteogenic differentiation of skeletal muscle satellite cells: an in vitro study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 110:453–462PubMedCrossRefGoogle Scholar
  67. Ishida K, Kuroda R, Miwa M et al (2007) The regenerative effects of platelet-rich plasma on meniscal cells in vitro and its in vivo application with biodegradable gelatin hydrogel. Tissue Eng 13:1103–1112PubMedCrossRefGoogle Scholar
  68. Jungbluth P, Wild M, Grassmann JP et al (2010) Platelet-rich plasma on calcium phosphate granules promotes metaphyseal bone healing in mini-pigs. J Orthop Res 28:1448–1455PubMedCrossRefGoogle Scholar
  69. Kajikawa Y, Morihara T, Sakamoto H et al (2008) Platelet-rich plasma enhances the initial mobilization of circulation-derived cells for tendon healing. J Cell Physiol 215:837–845PubMedCrossRefGoogle Scholar
  70. Kampa RJ, Connell DA (2010) Treatment of tendinopathy: is there a role for autologous whole blood and platelet rich plasma injection? Int J Clin Pract 64:1813–1823PubMedCrossRefGoogle Scholar
  71. Kevy S, Jacobson MS (2004) Comparison of methods for point of care preparation of autologous platelet gel. J Extra Corpor Technol 36:28–35PubMedGoogle Scholar
  72. Kon E, Filardo G, Delcogliano M et al (2009) Platelet-rich plasma: new clinical application: a pilot study for treatment of jumper’s knee. Injury 40:598–603PubMedCrossRefGoogle Scholar
  73. Krupski WC, Reilly LM, Perez S et al (1991) A prospective randomized trial of autologous platelet-derived wound healing factors for treatment of chronic nonhealing wounds: a preliminary report. J Vasc Surg 14:526–532, discussion 532–526PubMedCrossRefGoogle Scholar
  74. Lacci KM, Dardik A (2010) Platelet-rich plasma: support for its use in wound healing. Yale J Biol Med 83:1–9PubMedPubMedCentralGoogle Scholar
  75. Landesberg RRM, Glickman R (2000) Quantification of growth factors levels using a simplified method of platelet rich plasma gel preparation. J Oral Maxillofac Surg 58:297–300PubMedCrossRefGoogle Scholar
  76. Landesberg R, Moses M, Karpatkin M (1998) Risks of using platelet rich plasma gel. J Oral Maxillofac Surg 56:1116–1998PubMedCrossRefGoogle Scholar
  77. Lawlor DK, Derose G, Harris KA et al (2011) The role of platelet-rich plasma in inguinal wound healing in vascular surgery patients. Vasc Endovascular Surg 45:241–245PubMedCrossRefGoogle Scholar
  78. Lee JY, Nam H, Park YJ et al (2011) The effects of platelet-rich plasma derived from human umbilical cord blood on the osteogenic differentiation of human dental stem cells. In Vitro Cell Dev Biol Anim 47:157–164PubMedCrossRefGoogle Scholar
  79. Li NY, Yuan RT, Chen T et al (2009) Effect of platelet-rich plasma and latissimus dorsi muscle flap on osteogenesis and vascularization of tissue-engineered bone in dogs. J Oral Maxillofac Surg 67:1850–1858PubMedCrossRefGoogle Scholar
  80. Lowery GL, Kulkarni S, Pennisi AE (1999) Use of autologous growth factors in lumbar spinal fusion. Bone 25:47S–50SPubMedCrossRefGoogle Scholar
  81. Lucarelli E, Fini M, Beccheroni A et al (2005) Stromal stem cells and platelet-rich plasma improve bone allograft integration. Clin Orthop Relat Res 435:62–68CrossRefGoogle Scholar
  82. Lyras DN, Kazakos K, Verettas D et al (2009) The influence of platelet-rich plasma on angiogenesis during the early phase of tendon healing. Foot Ankle Int 30:1101–1106PubMedCrossRefGoogle Scholar
  83. Lyras DN, Kazakos K, Verettas D et al (2010a) Immunohistochemical study of angiogenesis after local administration of platelet-rich plasma in a patellar tendon defect. Int Orthop 34:143–148PubMedCrossRefGoogle Scholar
  84. Lyras DN, Kazakos K, Agrogiannis G et al (2010b) Experimental study of tendon healing early phase: is IGF-1 expression influenced by platelet rich plasma gel? Orthop Traumatol Surg Res 96:381–387PubMedCrossRefGoogle Scholar
  85. Lyras DN, Kazakos K, Tryfonidis M et al (2010c) Temporal and spatial expression of TGF-beta1 in an Achilles tendon section model after application of platelet-rich plasma. Foot Ankle Surg 16:137–141PubMedCrossRefGoogle Scholar
  86. Lyras DN, Kazakos K, Georgiadis G et al (2011) Does a single application of PRP alter the expression of IGF-I in the early phase of tendon healing? J Foot Ankle Surg 50:276–282PubMedCrossRefGoogle Scholar
  87. Maffulli N, Del Buono A (2012) Platelet plasma rich products in musculoskeletal medicine: any evidence? Surgeon 10:148–150PubMedCrossRefGoogle Scholar
  88. Man D, Plosker H, Winland-Brown JE (2001) The use of autologous platelet-rich plasma (platelet gel) and autologous platelet-poor plasma (fibrin glue) in cosmetic surgery. Plast Reconstr Surg 107:229–237, discussion 238–229PubMedCrossRefGoogle Scholar
  89. Marck RE, Montagne HL, Tuinebreijer WE et al (2013) Time course of thrombocytes in burn patients and its predictive value for outcome. Burns 39:714–722PubMedCrossRefGoogle Scholar
  90. Marck RE, Middelkoop E, Breederveld RS (2014) Considerations on the use of platelet-rich plasma, specifically for burn treatment. J Burn Care Res 35:219–227PubMedCrossRefGoogle Scholar
  91. Mariano R, Messora M, De Morais A et al (2010) Bone healing in critical-size defects treated with platelet-rich plasma: a histologic and histometric study in the calvaria of diabetic rat. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109:72–78PubMedCrossRefGoogle Scholar
  92. Marlovits S, Mousavi M, Gabler C et al (2004) A new simplified technique for producing platelet-rich plasma: a short technical note. Eur Spine J 13(Suppl 1):S102–106PubMedPubMedCentralCrossRefGoogle Scholar
  93. Marx RE (2001) Platelet-rich plasma (PRP): what is PRP and what is not PRP? Implant Dent 10:225–228PubMedCrossRefGoogle Scholar
  94. Marx RE (2004) Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg 62:489–496PubMedCrossRefGoogle Scholar
  95. Marx RE, Carlson ER, Eichstaedt RM et al (1998) Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 85:638–646PubMedCrossRefGoogle Scholar
  96. Matsuo R, Nakano Y, Ohkohchi N (2011) Platelet administration via the portal vein promotes liver regeneration in rats after 70 % hepatectomy. Ann Surg 253:759–763PubMedCrossRefGoogle Scholar
  97. Milano G, Sanna Passino E, Deriu L et al (2010) The effect of platelet rich plasma combined with microfractures on the treatment of chondral defects: an experimental study in a sheep model. Osteoarthritis Cartilage 18:971–980PubMedCrossRefGoogle Scholar
  98. Mishra A, Velotta J, Brinton TJ et al (2011) RevaTen platelet-rich plasma improves cardiac function after myocardial injury. Cardiovasc Revasc Med 12:158–163PubMedCrossRefGoogle Scholar
  99. Mishra A, Harmon K, Woodall J et al (2012) Sports medicine applications of platelet rich plasma. Curr Pharm Biotechnol 13:1185–1195PubMedCrossRefGoogle Scholar
  100. Morizaki Y, Zhao C, An KN et al (2010) The effects of platelet-rich plasma on bone marrow stromal cell transplants for tendon healing in vitro. J Hand Surg [Am] 35:1833–1841CrossRefGoogle Scholar
  101. Nagaveni NB, Praveen RB, Umashankar KV et al (2010) Efficacy of platelet-rich-plasma (PRP) in bone regeneration after cyst enucleation in pediatric patients—a clinical study. J Clin Pediatr Dent 35:81–87PubMedCrossRefGoogle Scholar
  102. Nakamura S, Ishihara M, Takikawa M et al (2010) Platelet-rich plasma (PRP) promotes survival of fat-grafts in rats. Ann Plast Surg 65:101–106PubMedCrossRefGoogle Scholar
  103. Nurden A (2011) Platelets, inflammation and tissue regeneration. Thromb Haemost 105(Suppl 1):S13–33PubMedCrossRefGoogle Scholar
  104. O’Connell SM, Impeduglia T, Hessler K et al (2008) Autologous platelet-rich fibrin matrix as cell therapy in the healing of chronic lower-extremity ulcers. Wound Repair Regen 16:749–756PubMedCrossRefGoogle Scholar
  105. Oprea WE, Karp JM, Hosseini MM et al (2003) Effect of platelet releasate on bone cell migration and recruitment in vitro. J Craniofac Surg 14:292–300PubMedCrossRefGoogle Scholar
  106. Pantou AL, Markopoulou CE, Dereka XE et al (2010) The effect of platelet-rich plasma (PRP) combined with a bone allograft on human periodontal ligament (PDL) cells. Cell Tissue Bank 13:81–88PubMedCrossRefGoogle Scholar
  107. Pessoa RS, Oliveira SR, Menezes HH et al (2009) Effects of platelet-rich plasma on healing of alveolar socket: split-mouth histological and histometric evaluation in Cebus apella monkeys. Indian J Dent Res 20:442–447PubMedCrossRefGoogle Scholar
  108. Pietrzak W, Eppley B (2005) Platelet rich plasma: biology and new technology. J Craniofac Surg 16:1043–1054PubMedCrossRefGoogle Scholar
  109. Radice F, Yánez R, Gutiérrez V et al (2010) Comparison of magnetic resonance imaging findings in anterior cruciate ligament grafts with and without autologous platelet-derived growth factors. Arthroscopy 26:50–57PubMedCrossRefGoogle Scholar
  110. Randelli PS, Arrigoni P, Cabitza P et al (2008) Autologous platelet rich plasma for arthroscopic rotator cuff repair. A pilot study. Disabil Rehabil 30:1584–1589PubMedCrossRefGoogle Scholar
  111. Rodrigues SV, Acharya AB, Thakur SL (2011) An evaluation of platelet-rich plasma without thrombin activation with or without anorganic bone mineral in the treatment of human periodontal intrabony defects. Platelets 22:353–360PubMedCrossRefGoogle Scholar
  112. Sadoghi P, Rosso C, Valderrabano V et al (2012) The role of platelets in the treatment of Achilles tendon injuries. J Orthop Res 31:111–118PubMedCrossRefGoogle Scholar
  113. Sanchez AR, Sheridan PJ, Kupp LI (2003) Is platelet-rich plasma the perfect enhancement factor? A current review. Int J Oral Maxillofac Implants 18:93–103PubMedGoogle Scholar
  114. Sanchez M, Anitua E, Azofra J et al (2007) Comparison of surgically repaired Achilles tendon tears using platelet-rich fibrin matrices. Am J Sports Med 35:245–251PubMedCrossRefGoogle Scholar
  115. Sanchez M, Anitua E, Azofra J et al (2010) Ligamentization of tendon grafts treated with an endogenous preparation rich in growth factors: gross morphology and histology. Arthroscopy 26:470–480PubMedCrossRefGoogle Scholar
  116. Scala M, Gipponi M, Mereu P et al (2010) Regeneration of mandibular osteoradionecrosis defect with platelet rich plasma gel. In Vivo 24:889–893PubMedGoogle Scholar
  117. Schepull T, Kvist J, Norrman H et al (2011) Autologous platelets have no effect on the healing of human achilles tendon ruptures: a randomized single-blind study. Am J Sports Med 39:38–47PubMedCrossRefGoogle Scholar
  118. Schnabel LV, Mohammed HO, Miller BJ et al (2007) Platelet rich plasma (PRP) enhances anabolic gene expression patterns in flexor digitorum superficialis tendons. J Orthop Res 25:230–240PubMedCrossRefGoogle Scholar
  119. Schoendorfer DW, Williamson LH, Sheckler VL, Fitzgerald BP (1990) Platelet Collection with the autopheresis-C apheresis system. Vox Sang 58:100–104PubMedCrossRefGoogle Scholar
  120. Seijas R, Santana-Suarez RY, Garcia-Balletbo M et al (2010) Delayed union of the clavicle treated with plasma rich in growth factors. Acta Orthop Belg 76:689–693PubMedGoogle Scholar
  121. Sheth U, Simunovic N, Klein G et al (2012) Efficacy of autologous platelet-rich plasma use for orthopaedic indications: a meta-analysis. J Bone Joint Surg Am 94:298–307PubMedCrossRefGoogle Scholar
  122. Silva A, Sampaio R (2009) Anatomic ACL reconstruction: does the platelet-rich plasma accelerate tendon healing? Knee Surg Sports Traumatol Arthrosc 17:676–682PubMedCrossRefGoogle Scholar
  123. Slater M, Patava J, Kingham K et al (1995) Involvement of platelets in stimulating osteogenic activity. J Orthop Res 13:655–663PubMedCrossRefGoogle Scholar
  124. Soffer E, Ouhayoun JP, Dosquet C et al (2004) Effects of platelet lysates on select bone cell functions. Clin Oral Implants Res 15:581–588PubMedCrossRefGoogle Scholar
  125. Sweeney J, Kouttab N, Holme S et al (2006) Storage of platelet-rich plasma–derived platelet concentrate pools in plasma and additive solution. Transfusion 46:835–840PubMedCrossRefGoogle Scholar
  126. Tanidir ST, Yuksel N, Altintas O et al (2010) The effect of subconjunctival platelet-rich plasma on corneal epithelial wound healing. Cornea 29:664–669PubMedCrossRefGoogle Scholar
  127. Taylor DW, Petrera M, Hendry M et al (2011) A systematic review of the use of platelet-rich plasma in sports medicine as a new treatment for tendon and ligament injuries. Clin J Sport Med 21:344–352PubMedCrossRefGoogle Scholar
  128. Tohidnezhad M, Varoga D, Wruck CJ et al (2011) Platelet-released growth factors can accelerate tenocyte proliferation and activate the anti-oxidant response element. Histochem Cell Biol 135:453–460PubMedCrossRefGoogle Scholar
  129. Van Den Dolder J, Mooren R, Vloon AP et al (2006) Platelet-rich plasma: quantification of growth factor levels and the effect on growth and differentiation of rat bone marrow cells. Tissue Eng 12:3067–3073PubMedCrossRefGoogle Scholar
  130. Vogrin M, Rupreht M, Crnjac A et al (2010a) The effect of platelet-derived growth factors on knee stability after anterior cruciate ligament reconstruction: a prospective randomized clinical study. Wien Klin Wochenschr 122(Suppl 2):91–95PubMedCrossRefGoogle Scholar
  131. Vogrin M, Rupreht M, Dinevski D et al (2010b) Effects of a platelet gel on early graft revascularization after anterior cruciate ligament reconstruction: a prospective, randomized, double-blind, clinical trial. Eur Surg Res 45:77–85PubMedCrossRefGoogle Scholar
  132. Volpi P, Quaglia A, Schoenhuber H et al (2010) Growth factors in the management of sport-induced tendinopathies: results after 24 months from treatment. A pilot study. J Sports Med Phys Fitness 50:494–500PubMedGoogle Scholar
  133. Weibrich G, Kleis WK, Hafner G et al (2002) Growth factor levels in platelet-rich plasma and correlations with donor age, sex, and platelet count. J Craniomaxillofac Surg 30:97–102PubMedCrossRefGoogle Scholar
  134. Weibrich G, Hansen T, Kleis W et al (2004) Effect of platelet concentration in platelet-rich plasma on peri-implant bone regeneration. Bone 34:665–671PubMedCrossRefGoogle Scholar
  135. Whitman DH, Berry RL, Green DM (1997) Platelet gel: an autologous alternative to fibrin glue with applications in oral and maxillofacial surgery. J Oral Maxillofac Surg 55:1294–1299PubMedCrossRefGoogle Scholar
  136. Yamaguchi R, Terashima H, Yoneyama S et al (2012) Effects of platelet-rich plasma on intestinal anastomotic healing in rats: PRP concentration is a key factor. J Surg Res 173:258–266PubMedCrossRefGoogle Scholar
  137. Yu W, Wang J, Yin J (2011) Platelet-rich plasma: a promising product for treatment of peripheral nerve regeneration after nerve injury. Int J Neurosci 121:176–180PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute of Translational MedicineUniversity of LiverpoolLiverpoolUK
  2. 2.Institute of Inflammation and Ageing, College of Medical and Dental SciencesUniversity of BirminghamBirminghamUK

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