Mesenchymal stem cells for the treatment of cartilage lesions: From preclinical findings to clinical application in orthopaedics

Knee Surgery, Sports Traumatology, Arthroscopy

Volumn 21, Issue 8, 2013, Pages 1717-1729

  Filardo, Giuseppe ^a   Madry, Henning ^b   Jelic, Mislav ^c   Roffi, Alice ^a   Cucchiarini, Magali ^b   Kon, Elizaveta ^a  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b SAARLAND UNIVERSITY   (Germany)

^c KBC Zagreb   (Croatia)

Author keywords

Cartilage; Injection; Mesenchymal stem cells; Surgical repair

Indexed keywords

TISSUE SCAFFOLD;

ADIPOSE TISSUE; ANIMAL; ARTICULAR CARTILAGE; CELL CULTURE; CYTOLOGY; HUMAN; INJURY; INTRAARTICULAR DRUG ADMINISTRATION; KNEE INJURY; MESENCHYMAL STEM CELL TRANSPLANTATION; PHYSIOLOGY; REGENERATION; REVIEW; SYNOVIUM;

ADIPOSE TISSUE; ANIMALS; CARTILAGE, ARTICULAR; CELLS, CULTURED; HUMANS; INJECTIONS, INTRA-ARTICULAR; KNEE INJURIES; MESENCHYMAL STEM CELL TRANSPLANTATION; REGENERATION; SYNOVIAL MEMBRANE; TISSUE SCAFFOLDS;

EID: 84880578702     PISSN: 09422056     EISSN: 14337347     Source Type: Journal    
DOI: 10.1007/s00167-012-2329-3     Document Type: Review

References (88)

1. Adachi N, Ochi M, Deie M, Ito Y (2005) Transplant of mesenchymal stem cells and hydroxyapatite ceramics to treat severe osteochondral damage after septic arthritis of the knee. J Rheumatol 32(8): 1615-1618.
2. Breitbach M, Bostani T, Roell W, Xia Y, Dewald O, Nygren JM, Fries JW, Tiemann K, Bohlen H, Hescheler J, Welz A, Bloch W, Jacobsen SE, Fleischmann BK (2007) Potential risks of bone marrow cell transplantation into infarcted hearts. Blood 110(4): 1362-1369.
3. Buda R, Vannini F, Cavallo M, Grigolo B, Cenacchi A, Giannini S (2010) Osteochondral lesions of the knee: a new one-step repair technique with bone-marrow-derived cells. J Bone Joint Surg Am 92(2): 2-11.
4. Cao L, Yang F, Liu G, Yu D, Li H, Fan Q, Gan Y, Tang T, Dai K (2011) The promotion of cartilage defect repair using adenovirus mediated Sox9 gene transfer of rabbit bone marrow mesenchymal stem cells. Biomaterials 32(16): 3910-3920.
5. Caplan AI, Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98(5): 1076-1084.
6. Caplan AI, Koutroupas S (1973) The control of muscle and cartilage development in the chick limb: the role of differential vascularization. J Embryol Exp Morphol 29(3): 571-583.
7. Caplan AI (2005) Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng 11(7-8): 1198-1211.
8. Centeno CJ, Busse D, Kisiday J, Keohan C, Freeman M, Karli D (2008) Increased knee cartilage volume in degenerative joint disease using percutaneously implanted, autologous mesenchymal stem cells. Pain Physician 11(3): 343-353.
9. Chang CH, Kuo TF, Lin FH, Wang JH, Hsu YM, Huang HT, Loo ST, Fang HW, Liu HC, Wang WC (2011) Tissue engineering-based cartilage repair with mesenchymal stem cells in a porcine model. J Orthop Res 29(12): 1874-1880.
10. Chen FH (2008) Mesenchymal stem cells in arthritic diseases. Arthr Res Ther 10(5): 223.
11. Chen WC, Yao CL, Wei YH, Chu IM (2011) Evaluating osteochondral defect repair potential of autologous rabbit bone marrow cells on type II collagen scaffold. Cytotechnology 63(1): 13-23.
12. Chen J, Chen H, Li P, Diao H, Zhu S, Dong L, Wang R, Guo T, Zhao J, Zhang J (2011) Simultaneous regeneration of articular cartilage and subchondral bone in vivo using MSCs induced by a spatially controlled gene delivery system in bilayered integrated scaffolds. Biomaterials 32(21): 4793-4805.
13. Cucchiarini M, Ekici M, Schetting S, Kohn D, Madry H (2011) Metabolic activities and chondrogenic differentiation of human mesenchymal stem cells following recombinant adeno-associated virus-mediated gene transfer and overexpression of fibroblast growth factor 2. Tissue Eng Part A 17(15-16): 1921-1933.
14. Cucchiarini M, Madry H (2005) Gene therapy for cartilage defects. J Gene Med 7(12): 1495-1509.
15. Davatchi F, Abdollahi BS, Mohyeddin M, Shahram F, Nikbin B (2011) Mesenchymal stem cell therapy for knee osteoarthritis. Preliminary report of four patients. Int J Rheum Dis 14(2): 211-215.
16. De Bari C, Dell'Accio F, Karystinou A, Guillot PV, Fisk NM, Jones EA, McGonagle D, Khan IM, Archer CW, Mitsiadis TA, Donaldson AN, Luyten FP, Pitzalis C (2008) A biomarker-based mathematical model to predict bone-forming potency of human synovial and periosteal mesenchymal stem cells. Arthritis Rheum 58(1): 240-250.
17. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4): 315-317.
18. Dragoo JL, Carlson G, McCormick F, Khan-Farooqi H, Zhu M, Zuk PA, Benhaim P (2007) Healing full-thickness cartilage defects using adipose-derived stem cells. Tissue Eng 13(7): 1615-1621.
19. Emadedin M, Aghdami N, Taghiyar L, Fazeli R, Moghadasali R, Jahangir S, Farjad R, Baghaban Eslaminejad M (2012) Intra-articular injection of autologous mesenchymal stem cells in six patients with knee osteoarthritis. Arch Iran Med 15(7): 422-428.
20. Fortier LA, Potter HG, Rickey EJ, Schnabel LV, Foo LF, Chong LR, Stokol T, Cheetham J, Nixon AJ (2010) Concentrated bone marrow aspirate improves full-thickness cartilage repair compared with microfracture in the equine model. J Bone Joint Surg Am 92(10): 1927-1937.
21. Friedenstein AJ, Piatetzky-Shapiro II, Petrakova KV (1966) Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 6(3): 381-390.
22. Frisbie DD, Lu Y, Kawcak CE, DiCarlo EF, Binette F, McIlwraith CW (2009) In vivo evaluation of autologous cartilage fragment-loaded scaffolds implanted into equine articular defects and compared with autologous chondrocyte implantation. Am J Sports Med 37(1): 71S-80S.
23. Giannini S, Buda R, Cavallo M, Ruffilli A, Cenacchi A, Cavallo C, Vannini F (2010) Cartilage repair evolution in post-traumatic osteochondral lesions of the talus: from open field autologous chondrocyte to bone-marrow-derived cells transplantation. Injury 41(11): 1196-1203.
24. Giannini S, Buda R, Vannini F, Cavallo M, Grigolo B (2009) One-step bone marrow-derived cell transplantation in talar osteochondral lesions. Clin Orthop Relat Res 467(12): 3307-3320.
25. Gigante A, Calcagno S, Cecconi S, Ramazzotti D, Manzotti S, Enea D (2011) Use of collagen scaffold and autologous bone marrow concentrate as a one-step cartilage repair in the knee: histological results of second-look biopsies at 1 year follow-up. Int J Immunopathol Pharmacol 24(1 Suppl 2): 69-72.
26. Gobbi A, Karnatzikos G, Scotti C, Mahajan V, Mazzucco L, Grigolo B (2011) One-step cartilage repair with bone marrow aspirate concentrated cells and collagen matrix in full-thickness knee cartilage lesions: results at 2 year follow up. Cartilage 2(3): 286-299.
27. Grande DA, Mason J, Light E, Dines D (2003) Stem cells as platforms for delivery of genes to enhance cartilage repair. J Bone Joint Surg Am 85-A(2): 111-116.
28. Guo X, Zheng Q, Yang S, Shao Z, Yuan Q, Pan Z, Tang S, Liu K, Quan D (2006) Repair of full-thickness articular cartilage defects by cultured mesenchymal stem cells transfected with the transforming growth factor beta1 gene. Biomed Mater 1(4): 206-215.
29. Haleem AM, Singergy AA, Sabry D, Atta HM, Rashed LA, Chu CR, El Shewy MT, Azzam A, Abdel Aziz MT (2010) The clinical use of human culture-expanded autologous bone marrow mesenchymal stem cells transplanted on platelet-rich fibrin glue in the treatment of articular cartilage defects: a pilot study and preliminary results. Cartilage 1(4): 253-261.
30. He Q, Wan C, Li G (2007) Concise review: multipotent mesenchymal stromal cells in blood. Stem Cells 25(1): 69-77.
31. Hori J, Deie M, Kobayashi T, Yasunaga Y, Kawamata S, Ochi M (2011) Articular cartilage repair using an intra-articular magnet and synovium-derived cells. J Orthop Res 29(4): 531-538.
32. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A (2005) International Society for Cellular Therapy. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 7(5): 393-395.
33. Im GI, Lee JH (2010) Repair of osteochondral defects with adipose stem cells and a dual growth factor-releasing scaffold in rabbits. J Biomed Mater Res B Appl Biomater 92(2): 552-560.
34. Im GI, Kim HJ, Lee JH (2011) Chondrogenesis of adipose stem cells in a porous PLGA scaffold impregnated with plasmid DNA containing SOX trio (SOX-5, -6 and -9) genes. Biomaterials 32(19): 4385-4392.
35. Ivkovic A, Pascher A, Hudetz D, Maticic D, Jelic M, Dickinson S, Loparic M, Haspl M, Windhager R, Pecina M (2010) Articular cartilage repair by genetically modified bone marrow aspirate in sheep. Gene Ther 17(6): 779-789.
36. Kasemkijwattana C, Hongeng S, Kesprayura S, Rungsinaporn V, Chaipinyo K, Chansiri K (2011) Autologous bone marrow mesenchymal stem cells implantation for cartilage defects: two cases report. J Med Assoc Thai 94(3): 395-400.
37. Katayama R, Wakitani S, Tsumaki N, Morita Y, Matsushita I, Gejo R, Kimura T (2004) Repair of articular cartilage defects in rabbits using CDMP1 gene-transfected autologous mesenchymal cells derived from bone marrow. Rheumatology (Oxford) 43(8): 980-985.
38. Kim HJ, Im GI (2009) Chondrogenic differentiation of adipose tissue-derived mesenchymal stem cells: greater doses of growth factor are necessary. J Orthop Res 27(5): 612-619.
39. Koga H, Muneta T, Ju YJ, Nagase T, Nimura A, Mochizuki T, Ichinose S, von der Mark K, Sekiya I (2007) Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells 25(3): 689-696.
40. Koga H, Engebretsen L, Brinchmann JE, Muneta T, Sekiya I (2009) Mesenchymal stem cell-based therapy for cartilage repair: a review. Knee Surg Sports Traumatol Arthrosc 17: 1289-1297.
41. Koga H, Muneta T, Nagase T, Nimura A, Ju YJ, Mochizuki T, Sekiya I (2008) Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res 333(2): 207-215.
42. Koh YG, Choi YJ (2012) Infrapatellar fat pad-derived mesenchymal stem cell therapy for knee osteoarthritis. Knee doi: 10. 1016/j. knee. 2012. 04. 001 (epub 14 May 2012).
43. Kon E, Filardo G, Roffi A, Andriolo L, Marcacci M (2012) New trends for knee cartilage regeneration: from cell-free scaffolds to mesenchymal stem cells. Curr Rev Musculoskelet Med 5(3): 236-243.
44. Krampera M, Pizzolo G, Aprili G, Franchini M (2006) Mesenchymal stem cells for bone, cartilage, tendon and skeletal muscle repair. Bone 39: 678-683.
45. Kubo S, Cooper GM, Matsumoto T, Phillippi JA, Corsi KA, Usas A, Li G, Fu FH, Huard J (2009) Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle-derived stem cells. Arthritis Rheum 60(1): 155-165.
46. Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, Ohgushi H, Wakitani S, Kurosaka M (2007) Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 15(2): 226-231.
47. Kuroda R, Usas A, Kubo S, Corsi K, Peng H, Rose T, Cummins J, Fu FH, Huard J (2006) Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum 54(2): 433-442.
48. Lee JM, Kim BS, Lee H, Im GI (2012) In vivo tracking of mesenchymal stem cells using fluorescent nanoparticles in an osteochondral repair model. Mol Ther 20(7): 1434-1442.
49. Lee JM, Im GI (2012) SOX trio-co-transduced adipose stem cells in fibrin gel to enhance cartilage repair and delay the progression of osteoarthritis in the rat. Biomaterials 33(7): 2016-2024.
50. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, Marshak DR, Flake AW (2000) Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6(11): 1282-1286.
51. Liu TM, Guo XM, Tan HS, Hui JH, Lim B, Lee EH (2011) Zinc-finger protein 145, acting as an upstream regulator of SOX9, improves the differentiation potential of human mesenchymal stem cells for cartilage regeneration and repair. Arthritis Rheum 63(9): 2711-2720.
52. Lodi D, Iannitti T, Palmieri B (2011) Stem cells in clinical practice: applications and warnings. J Exp Clin Cancer Res 30: 9.
53. Madry H, Grün UW, Knutsen G (2011) Cartilage repair and joint preservation: medical and surgical treatment options. Dtsch Arztebl Int 108(40): 669-677.
54. Masuoka K, Asazuma T, Hattori H, Yoshihara Y, Sato M, Matsumura K, Matsui T, Takase B, Nemoto K, Ishihara M (2006) Tissue engineering of articular cartilage with autologous cultured adipose tissue-derived stromal cells using atelocollagen honeycomb-shaped scaffold with a membrane sealing in rabbits. J Biomed Mater Res B Appl Biomater 79(1): 25-34.
55. McIlwraith CW, Frisbie DD, Rodkey WG, Kisiday JD, Werpy NM, Kawcak CE, Steadman JR (2011) Evaluation of intra-articular mesenchymal stem cells to augment healing of microfractured chondral defects. Arthroscopy 27(11): 1552-1561.
56. Mimura T, Imai S, Okumura N, Li L, Nishizawa K, Araki S, Ueba H, Kubo M, Mori K, Matsusue Y (2011) Spatiotemporal control of proliferation and differentiation of bone marrow-derived mesenchymal stem cells recruited using collagen hydrogel for repair of articular cartilage defects. J Biomed Mater Res B Appl Biomater 98B(2): 360-368.
57. Mokbel AN, El Tookhy OS, Shamaa AA, Rashed LA, Sabry D, El Sayed AM (2011) Homing and reparative effect of intra-articular injection of autologus mesenchymal stem cells in osteoarthritic animal model. BMC Musculoskelet Disord 15(12): 259.
58. Mosna F, Sensebé L, Krampera M (2010) Human bone marrow and adipose tissue mesenchymal stem cells: a user's guide. Stem Cells Dev 19(10): 1449-1470.
59. Mueller MB, Tuan RS (2008) Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58(5): 1377-1388.
60. Nathan S, De Das S, Thambyah A, Fen C, Goh J, Lee EH (2003) Cell-based therapy in the repair of osteochondral defects: a novel use for adipose tissue. Tissue Eng 9(4): 733-744.
61. Nejadnik H, Hui JH, Feng Choong EP, Tai BC, Lee EH (2010) Autologous bone marrow-derived mesenchymal stem cells versus autologous chondrocyte implantation: an observational cohort study. Am J Sports Med 38(6): 1110-1116.
62. Pagnotto MR, Wang Z, Karpie JC, Ferretti M, Xiao X, Chu CR (2007) Adeno-associated viral gene transfer of transforming growth factor-beta1 to human mesenchymal stem cells improves cartilage repair. Gene Ther 14(10): 804-813.
63. Pak J (2011) Regeneration of human bones in hip osteonecrosis and human cartilage in knee osteoarthritis with autologous adipose-tissue-derived stem cells: a case series. J Med Case Rep 5: 296.
64. Park J, Gelse K, Frank S, von der Mark K, Aigner T, Schneider H (2006) Transgene-activated mesenchymal stem cells for articular cartilage repair: a comparison of primary bone marrow-, perichondrium/periosteum- and fat-derived cells. J Gene Med 8(1): 112-125.
65. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M (2001) Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344(5): 385-386.
66. Re'em T, Witte F, Willbold E, Ruvinov E, Cohen S (2012) Simultaneous regeneration of articular cartilage and subchondral bone induced by spatially presented TGF-beta and BMP-4 in a bilayer affinity binding system. Acta Biomater 8(9): 3283-3293.
67. Rubio D, Garcia-Castro J, Martín MC, de la Fuente R, Cigudosa JC, Lloyd AC, Bernad A (2005) Spontaneous human adult stem cell transformation. Cancer Res 65(8): 3035-3039.
68. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T (2005) Comparison of human stem cells derived from various mesenchymal tissues. Superiority of synovium as a cell source. Arthritis Rheum 52(8): 2521-2529.
69. Saw KY, Anz A, Merican S, Tay YG, Ragavanaidu K, Jee CSY, McGuire DA (2011) Articular cartilage regeneration with autologous peripheral blood progenitor cells and hyaluronic acid after arthroscopic subchondral drilling: a report of 5 cases with histology. Arthroscopy 27(4): 493-506.
70. Saw KY, Hussin P, Loke SC, Azam M, Chen HC, Tay YG, Low S, Wallin KL, Ragavanaidu K (2009) Articular cartilage regeneration with autologous marrow aspirate and hyaluronic acid: an experimental study in a goat model. Arthroscopy 25(12): 1391-1400.
71. Schäffler A, Büchler C (2007) Concise review: adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 25(4): 818-827.
72. Sensebé L, Krampera M, Schrezenmeier H, Bourin P, Giordano R (2010) Mesenchymal stem cells for clinical application. Vox Sang 98(2): 93-107.
73. Shimomura K, Ando W, Tateishi K, Nansai R, Fujie H, Hart DA, Kohda H, Kita K, Kanamoto T, Mae T, Nakata K, Shino K, Yoshikawa H, Nakamura N (2010) The influence of skeletal maturity on allogenic synovial mesenchymal stem cell-based repair of cartilage in a large animal model. Biomaterials 31(31): 8004-8011.
74. Singer NG, Caplan AI (2011) Mesenchymal stem cells: mechanisms of inflammation. Annu Rev Pathol 6: 457-478.
75. Spencer ND, Gimble JM, Lopez MJ (2011) Mesenchymal stromal cells: past, present, and future. Vet Surg 40(2): 129-139.
76. Sukarto A, Yu C, Flynn LE, Amsden BG (2012) Co-delivery of adipose-derived stem cells and growth factor-loaded microspheres in RGD-grafted N-methacrylate glycol chitosan gels for focal chondral repair. Biomacromolecules 13(8): 2490-2502.
77. Varma HS, Dadarya B, Vidyarthi A (2010) The new avenues in the management of osteoarthritis of knee-stem cells. J Indian Med Assoc 108: 583-585.
78. Venkatesan JK, Ekici M, Madry H, Schmitt G, Kohn D, Cucchiarini M (2012) SOX9 gene transfer via safe, stable, replication-defective recombinant adeno-associated virus vectors as a novel, powerful tool to enhance the chondrogenic potential of human mesenchymal stem cells. Stem Cell Res Ther 3(3): 22.
79. Vinatier C, Bouffi C, Merceron C, Gordeladze J, Brondello JM, Jorgensen C, Weiss P, Guicheux J, Noël D (2009) Cartilage tissue engineering: towards a biomaterial-assisted mesenchymal stem cell therapy. Curr Stem Cell Res Ther 4(4): 318-329.
80. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI, Goldberg VM (1994) Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 76(4): 579-592.
81. Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M (2002) Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 10(3): 199-206.
82. Wakitani S, Yamamoto T (2002) Response of the donor and recipient cells in mesenchymal cell transplantation to cartilage defect. Microsc Res Tech 58(1): 14-18.
83. Wakitani S, Mitsuoka T, Nakamura N, Toritsuka Y, Nakamura Y, Horibe S (2004) Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: two case reports. Cell Transplant 13(5): 595-600.
84. Wakitani S, Nawata M, Tensho K, Okabe T, Machida H, Ohgushi H (2007) Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: three case reports involving nine defects in five knees. J Tissue Eng Regen Med 1(1): 74-79.
85. Wakitani S, Okabe T, Horibe S, Mitsuoka T, Saito M, Koyama T, Nawata M, Tensho K, Kato H, Uematsu K, Kuroda R, Kurosaka M, Yoshiya S, Hattori K, Ohgushi H (2011) Safety of autologous bone marrow-derived mesenchymal stem cell transplantation for cartilage repair in 41 patients with 45 joints followed for up to 11 years and 5 months. J Tissue Eng Regen Med 5(2): 146-150.
86. Xie X, Wang Y, Zhao C, Guo S, Liu S, Jia W, Tuan RS, Zhang C (2012) Comparative evaluation of MSCs from bone marrow and adipose tissue seeded in PRP-derived scaffold for cartilage regeneration. Biomaterials 33(29): 7008-7018.
87. Zhang Y, Wang F, Chen J, Ning Z, Yang L (2012) Bone marrow-derived mesenchymal stem cells versus bone marrow nucleated cells in the treatment of chondral defects. Int Orthop 36(5): 1079-1086.
88. Zscharnack M, Hepp P, Richter R, Aigner T, Schulz R, Somerson J, Josten C, Bader A, Marquass B (2010) Repair of chronic osteochondral defects using predifferentiated mesenchymal stem cells in an ovine model. Am J Sports Med 38(9): 1857-1869.