The effect of platelet rich plasma combined with microfractures on the treatment of chondral defects: An experimental study in a sheep model

Osteoarthritis and Cartilage

Volumn 18, Issue 7, 2010, Pages 971-980

  Milano, G ^a   Sanna Passino, E ^b   Deriu, L ^a   Careddu, G ^b   Manunta, L ^b   Manunta, A ^b   Saccomanno, M F ^a   Fabbriciani, C ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF SASSARI   (Italy)

Author keywords

Animal model; Cartilage defect; Cartilage repair; Microfractures; Platelet rich plasma

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CARTILAGE; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; HEALING; HISTOLOGY; MICROFRACTURE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RIGIDITY; SHEEP; THROMBOCYTE RICH PLASMA; TISSUE REPAIR;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROCYTES; FEMALE; FRACTURES, CARTILAGE; MODELS, ANIMAL; PLATELET-RICH PLASMA; RANDOM ALLOCATION; SHEEP; STATISTICS AS TOPIC; WOUND HEALING;

EID: 77954216768     PISSN: 10634584     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.joca.2010.03.013     Document Type: Article

References (66)

1. Furukawa T., Eyre D.R., Koide S., Glimcher M.J. Biochemical studies on repair cartilage resurfacing experimental defects in the rabbit knee. J Bone Joint Surg Am 1980, 62:79-89.
2. Frisbie D.D., Oxford J.T., Southwood L., Trotter G.W., Rodkey W.G., Steadman J.R., et al. Early events in cartilage repair after subchondral bone microfracture. Clin Orthop Relat Res 2003, 407:215-227.
3. Knutsen G., Engebretsen L., Ludvigsen T.C., Drogset J.O., Grøntvedt T., Solheim E., et al. Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial. J Bone Joint Surg Am 2004, 86:455-464.
4. Gobbi A., Nunag P., Malinowski K. Treatment of full thickness chondral lesions of the knee with microfracture in a group of athletes. Knee Surg Sports Traumatol Arthrosc 2005, 13:213-221.
5. Gudas R., Kalesinskas R.J., Kimtys V., Stankevicius E., Toliusis V., Bernotavicius G., et al. A prospective randomized clinical study of mosaic osteochondral autologous transplantation versus microfracture for the treatment of osteochondral defects in the knee joint in young athletes. Arthroscopy 2005, 21:1066-1075.
6. Bae D.K., Yoon K.H., Song S.J. Cartilage healing after microfracture in osteoarthritic knees. Arthroscopy 2006, 22:367-374.
7. Imhof H., Sulzbacher I., Grampp S., Czerny C., Youssefzadeh S., Kainberger F. Subchondral bone and cartilage disease: a rediscovered functional unit. Invest Radiol 2000, 35:581-588.
8. Johnstone B., Hering T.M., Caplan A.I., Goldberg V.M., Yoo J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998, 238:265-272.
9. Barry F., Boynton R.E., Liu B., Murphy J.M. Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp Cell Res 2001, 268:189-200.
10. Mizuta H., Kudo S., Nakamura E., Otsuka Y., Takagi K., Hiraki Y. Active proliferation of mesenchymal cells prior to the chondrogenic repair response in rabbit full-thickness defects of articular cartilage. Osteoarthritis Cartilage 2004, 12:586-596.
11. Davidson D., Blanc A., Filion D., Wang H., Plut P., Pfeffer G., et al. Fibroblast growth factor (FGF) 18 signals through FGF receptor 3 to promote chondrogenesis. J Biol Chem 2005, 280:20509-20515.
12. Hills R.L., Belanger L.M., Morris E.A. Bone morphogenetic protein 9 is a potent anabolic factor for juvenile bovine cartilage, but not adult cartilage. J Orthop Res 2005, 23:611-617.
13. Li W.G., Xu X.X. The expression of N-cadherin, fibronectin during chondrogenic differentiation of MSC induced by TGF-beta(1). Chin J Traumatol 2005, 8:349-351.
14. Yoon B.S., Ovchinnikov D.A., Yoshii I., Mishina Y., Behringer R.R., Lyons K.M. Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci USA 2005, 102:5062-5067.
15. Djouad F., Mrugala D., Noël D., Jorgensen C. Engineered mesenchymal stem cells for cartilage repair. Regen Med 2006, 1:529-537.
16. Jin E.J., Park J.H., Lee S.Y., Chun J.S., Bang O.S., Kang S.S. Wnt-5a is involved in TGF-beta3-stimulated chondrogenic differentiation of chick wing bud mesenchymal cells. Int J Biochem Cell Biol 2006, 38:183-195.
17. Neumann K., Dehne T., Endres M., Erggelet C., Kaps C., Ringe J., et al. Chondrogenic differentiation capacity of human mesenchymal progenitor cells derived from subchondral cortico-spongious bone. J Orthop Res 2008, 26:1449-1456.
18. Marx R.E. Platelet-rich plasma (PRP): what is PRP and what is not PRP?. Implant Dent 2001, 10:225-228.
19. Eppley B.L., Woodell J.E., Higgins J. Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plast Reconstr Surg 2004, 114:1502-1508.
20. Gaissmaier C., Fritz J., Krackhardt T., Flesch I., Aicher W.K., Ashammakhi N. Effect of human platelet supernatant on proliferation and matrix synthesis of human articular chondrocytes in monolayer and three-dimensional alginate cultures. Biomaterials 2005, 26:1953-1960.
21. Akeda K., An H.S., Okuma M., Attawia M., Miyamoto K., Thonar E.J., et al. Platelet-rich plasma stimulates porcine articular chondrocyte proliferation and matrix biosynthesis. Osteoarthritis Cartilage 2006, 14:1272-1280.
22. Zaky S.H., Ottonello A., Strada P., Cancedda R., Mastrogiacomo M. Platelet lysate favours in vitro expansion of human bone marrow stromal cells for bone and cartilage engineering. J Tissue Eng Regen Med 2008, 2:472-481.
23. Drengk A., Zapf A., Stürmer E.K., Stürmer K.M., Frosch K.H. Influence of platelet-rich plasma on chondrogenic differentiation and proliferation of chondrocytes and mesenchymal stem cells. Cells Tissues Organs 2009, 189:317-326.
24. Mishra A., Tummala P., King A., Lee B., Kraus M., Tse V., et al. Buffered platelet-rich plasma enhances mesenchymal stem cell proliferation and chondrogenic differentiation. Tissue Eng Part C Methods 2009, 15:431-435.
25. Peterson L., Minas T., Brittberg M., Nilsson A., Sjogren-Jansson E., Lindahl A. Two- to 9-year outcome after autologous chondrocytes transplantation of the knee. Clin Orthop Relat Res 2000, 374:212-234.
26. van den Borne M.P., Raijmakers N.J., Vanlauwe J., Victor J., de Jong S.N., Bellemans J., International Cartilage Repair Society, et al. International Cartilage Repair Society (ICRS) and Oswestry macroscopic cartilage evaluation scores validated for use in Autologous Chondrocyte Implantation (ACI) and microfracture. Osteoarthritis Cartilage 2007, 15:1397-1402.
27. O'Driscoll S.W., Keeley F.W., Salter R.B. Durability of regenerated articular cartilage produced by free autogenous periosteal grafts in major full-thickness defects in joint surfaces under the influence of continuous passive motion. A follow-up report at one year. J Bone Joint Surg Am 1988, 70:595-606.
28. Brehm W., Aklin B., Yamashita T., Rieser F., Trüb T., Jakob R.P., et al. Repair of superficial osteochondral defects with an autologous scaffold-free cartilage construct in a caprine model: implantation method and short-term results. Osteoarthritis Cartilage 2006, 14:1214-1226.
29. Knutsen G., Drogset J.O., Engebretsen L., Grøntvedt T., Isaksen V., Ludvigsen T.C., et al. A randomized trial comparing autologous chondrocyte implantation with microfracture. Findings at five years. J Bone Joint Surg Am 2007, 89:2105-2112.
30. Magnussen R.A., Dunn W.R., Carey J.L., Spindler K.P. Treatment of focal articular cartilage defects in the knee: a systematic review. Clin Orthop Relat Res 2008, 466:952-962.
31. Saris D.B., Vanlauwe J., Victor J., Haspl M., Bohnsack M., Fortems Y., et al. Characterized chondrocyte implantation results in better structural repair when treating symptomatic cartilage defects of the knee in a randomized controlled trial versus microfracture. Am J Sports Med 2008, 36:235-246.
32. Mithoefer K., McAdams T., Williams R.J., Kreuz P.C., Mandelbaum B.R. Clinical efficacy of the microfracture technique for articular cartilage repair in the knee: an evidence-based systematic analysis. Am J Sports Med 2009, 37:2053-2063.
33. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
34. Majumdar M.K., Banks V., Peluso D.P., Morris E.A. Isolation, characterization, and chondrogenic potential of human bone marrow-derived multipotential stromal cells. J Cell Physiol 2000, 185:98-106.
35. Bosnakovski D., Mizuno M., Kim G., Ishiguro T., Okumura M., Iwanaga T., et al. Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells in pellet cultural system. Exp Hematol 2004, 32:502-509.
36. Li W.J., Tuli R., Okafor C., Derfoul A., Danielson K.G., Hall D.J., et al. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 2005, 26:599-609.
37. Wakitani S., Goto T., Pineda S.J., Young R.G., Mansour J.M., Caplan A.I., et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 1994, 76:579-592.
38. Im G.I., Kim D.Y., Shin J.H., Hyun C.W., Cho W.H. Repair of cartilage defect in the rabbit with cultured mesenchymal stem cells from bone marrow. J Bone Joint Surg Br 2001, 83:289-294.
39. Wakitani S., Imoto K., Yamamoto T., Saito M., Murata N., Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 2002, 10:199-206.
40. Shao X.X., Hutmacher D.W., Ho S.T., Goh J.C., Lee E.H. Evaluation of a hybrid scaffold/cell construct in repair of high-load-bearing osteochondral defects in rabbits. Biomaterials 2006, 27:1071-1080.
41. Zhou G., Liu W., Cui L., Wang X., Liu T., Cao Y. Repair of porcine articular osteochondral defects in non-weightbearing areas with autologous bone marrow stromal cells. Tissue Eng 2006, 12:3209-3221.
42. Kuroda R., Ishida K., Matsumoto T., Akisue T., Fujioka H., Mizuno K., et al. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 2007, 15:226-231.
43. Yan H., Yu C. Repair of full-thickness cartilage defects with cells of different origin in a rabbit model. Arthroscopy 2007, 23:178-187.
44. Güneş T., Sen C., Erdem M., Köseoĝlu R.D., Filiz N.O. Combination of microfracture and periosteal transplantation techniques for the treatment of full-thickness cartilage defects. Acta Orthop Traumatol Turc 2006, 40:315-323.
45. Kramer J., Böhrnsen F., Lindner U., Behrens P., Schlenke P., Rohwedel J. In vivo matrix-guided human mesenchymal stem cells. Cell Mol Life Sci 2006, 63:616-626.
46. Kang S.W., Bada L.P., Kang C.S., Lee J.S., Kim C.H., Park J.H., et al. Articular cartilage regeneration with microfracture and hyaluronic acid. Biotechnol Lett 2008, 30:435-439.
47. Seedhom B.B., Luo Z.J., Goldsmith A.J., Toyoda T., Lorrison J.C., Guardamagna L. In-situ engineering of cartilage repair: a pre-clinical in-vivo exploration of a novel system. Proc Inst Mech Eng [H] 2007, 221:475-488.
48. Wegener B., Schrimpf F.M., Pietschmann M.F., Milz S., Berger-Lohr M., Bergschmidt P., et al. Matrix-guided cartilage regeneration in chondral defects. Biotechnol Appl Biochem 2009, 53:63-70.
49. Hoemann C.D., Hurtig M., Rossomacha E., Sun J., Chevrier A., Shive M.S., et al. Chitosan-glycerol phosphate/blood implants improve hyaline cartilage repair in ovine microfracture defects. J Bone Joint Surg Am 2005, 87:2671-2686.
50. Kuo A.C., Rodrigo J.J., Reddi A.H., Curtiss S., Grotkopp E., Chiu M. Microfracture and bone morphogenetic protein 7 (BMP-7) synergistically stimulate articular cartilage repair. Osteoarthritis Cartilage 2006, 14:1126-1135.
51. Erggelet C., Neumann K., Endres M., Haberstroh K., Sittinger M., Kaps C. Regeneration of ovine articular cartilage defects by cell-free polymer-based implants. Biomaterials 2007, 28:5570-5580.
52. Morisset S., Frisbie D.D., Robbins P.D., Nixon A.J., McIlwraith C.W. IL-1ra/IGF-1 gene therapy modulates repair of microfractured chondral defects. Clin Orthop Relat Res 2007, 462:221-228.
53. Zhang X., Zheng Z., Liu P., Ma Y., Lin L., Lang N., et al. The synergistic effects of microfracture, perforated decalcified cortical bone matrix and adenovirus-bone morphogenetic protein-4 in cartilage defect repair. Biomaterials 2008, 29:4616-4629.
54. Kaps C., Loch A., Haisch A., Smolian H., Burmester G.R., Häupl T., et al. Human platelet supernatant promotes proliferation but not differentiation of articular chondrocytes. Med Biol Eng Comput 2002, 40:485-490.
55. Wu W., Chen F., Liu Y., Ma Q., Mao T. Autologous injectable tissue-engineered cartilage by using platelet-rich plasma: experimental study in a rabbit model. J Oral Maxillofac Surg 2007, 65:1951-1957.
56. Steadman J.R., Rodkey W.G., Rodrigo J.J. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res 2001, 391:S362-S369.
57. Frisbie D.D., Cross M.W., McIlwraith C.W. A comparative study of articular cartilage thickness in the stifle of animal species used in human pre-clinical studies compared to articular cartilage thickness in the human knee. Vet Comp Orthop Traumatol 2006, 19:142-146.
58. Chen H., Sun J., Hoemann C.D., Lascau-Coman V., Ouyang W., McKee M.D., et al. Drilling and microfracture lead to different bone structure and necrosis during bone-marrow stimulation for cartilage repair. J Orthop Res 2009, 27:1432-1438.
59. Ting V., Sims C.D., Brecht L.E., McCarthy J.G., Kasabian A.K., Connelly P.R., et al. In vitro prefabrication of human cartilage shapes using fibrin glue and human chondrocytes. Ann Plast Surg 1998, 40:413-420.
60. Silverman R.P., Passaretti D., Huang W., Randolph M.A., Yaremchuk M.J. Injectable tissue-engineered cartilage using a fibrin glue polymer. Plast Reconstr Surg 1999, 103:1809-1818.
61. Xu J.W., Zaporojan V., Peretti G.M., Roses R.E., Morse K.B., Roy A.K., et al. Injectable tissue-engineered cartilage with different chondrocyte sources. Plast Reconstr Surg 2004, 113:1361-1371.
62. Borzini P., Mazzucco L. Tissue regeneration and in loco administration of platelet derivatives: clinical outcome, heterogeneous products, and heterogeneity of the effector mechanisms. Transfusion 2005, 45:1759-1767.
63. Weibrich G., Kleis W.K., Hitzler W.E., Hafner G. Comparison of the platelet concentrate collection system with the plasma-rich-in-growth-factors kit to produce platelet-rich plasma: a technical report. Int J Oral Maxillofac Implants 2005, 20:118-123.
64. Leitner G.C., Gruber R., Neumüller J., Wagner A., Kloimstein P., Höcker P., et al. Platelet content and growth factor release in platelet-rich plasma: a comparison of four different systems. Vox Sang 2006, 91:135-139.
65. Marx R.E. Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg 2004, 62:489-496.
66. Frisbie D.D., Morisset S., Ho C.P., Rodkey W.G., Steadman J.R., McIlwraith C.W. Effects of calcified cartilage on healing of chondral defects treated with microfracture in horses. Am J Sports Med 2006, 34:1824-1831.