Repair of meniscal lesions using a scaffold-free tissue-engineered construct derived from allogenic synovial MSCs in a miniature swine model

Biomaterials

Volumn 34, Issue 9, 2013, Pages 2185-2193

  Moriguchi, Yu ^a   Tateishi, Kosuke ^a   Ando, Wataru ^a   Shimomura, Kazunori ^a   Yonetani, Yasukazu ^a   Tanaka, Yoshinari ^b   Kita, Keisuke ^b   Hart, David A ^c   Gobbi, Alberto ^d   Shino, Konsei ^a   Yoshikawa, Hideki ^a   Nakamura, Norimasa ^a,e  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA ROSAI HOSPITAL   (Japan)

^c UNIVERSITY OF CALGARY   (Canada)

^d Orthopaedic Arthroscopic Surgery International   (Italy)

^e OSAKA HEALTH SCIENCE UNIVERSITY   (Japan)

Author keywords

Allogeneic; Meniscal repair; Stem cell; Synovium; Tissue engineering

Indexed keywords

ALLOGENEIC; ASCORBIC ACIDS; CELL-BASED; CONTROL GROUPS; DEGENERATIVE CHANGES; HIGH DENSITY; MENISCAL REPAIR; MESENCHYMAL STEM CELL; SUSPENSION CULTURES; SYNOVIUM; TIBIAL PLATEAU; TISSUE INTEGRATION; TISSUE-ENGINEERED CONSTRUCTS;

CELL CULTURE; DEFECTS; FLOWCHARTING; MONOLAYERS; ORGANIC ACIDS; REPAIR; STEM CELLS; TISSUE; TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

ASCORBIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; KNEE MENISCUS RUPTURE; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; SWINE; TISSUE ENGINEERING;

ANIMALS; CELL DIFFERENTIATION; FEASIBILITY STUDIES; FEMALE; MALE; MENISCI, TIBIAL; MESENCHYMAL STROMAL CELLS; SWINE; SWINE, MINIATURE; SYNOVIAL MEMBRANE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; WOUND HEALING;

SUIDAE; SUS;

EID: 84872407398     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.11.039     Document Type: Article

References (57)

1. Rattner J.B., Matyas J.R., Barclay L., Holowaychuk S., Sciore P., Lo I.K., et al. New understanding of the complex structure of knee menisci: implications for injury risk and repair potential for athletes. Scand J Med Sci Sports 2011, 21:543-553.
2. King D. The healing of semilunar cartilages. J Bone Joint Surg 1936, 18:333-342.
3. Levy I.M., Torzilli P.A., Gould J.D., Warren R.F. The effect of lateral meniscectomy on motion of the knee. J Bone Joint Surg Am 1989, 71:401-406.
4. Ahmed A.M., Burke D.L. In-vitro measurement of static pressure distribution in synovial joints - part I: tibial surface of the knee. J Biomech Eng 1983, 105:216-225.
5. Krause W.R., Pope M.H., Johnson R.J., Wilder D.G. Mechanical changes in the knee after meniscectomy. J Bone Joint Surg Am 1976, 58:599-604.
6. Arnoczky S.P., Warren R.F. Microvasculature of the human meniscus. Am J Sports Med 1982, 10:90-95.
7. Henning C.E., Lynch M.A., Clark J.R. Vascularity for healing of meniscus repairs. Arthroscopy 1987, 3:13-18.
8. Baratz M.E., Fu F.H., Mengato R. Meniscal tears: the effect of meniscectomy and of repair on intraarticular contact areas and stress in the human knee. A preliminary report. Am J Sports Med 1986, 14:270-275.
9. Fukubayashi T., Kurosawa H. The contact area and pressure distribution pattern of the knee. A study of normal and osteoarthrotic knee joints. Acta Orthop Scand 1980, 51:871-879.
10. Voloshin A.S., Wosk J. Shock absorption of meniscectomized and painful knees: a comparative in vivo study. J Biomed Eng 1983, 5:157-161.
11. LeRoux M.A., Arokoski J., Vail T.P., Guilak F., Hyttinen M.M., Kiviranta I., et al. Simultaneous changes in the mechanical properties, quantitative collagen organization, and proteoglycan concentration of articular cartilage following canine meniscectomy. J Orthop Res 2000, 18:383-392.
12. Sprinz R. The role of the meniscus in the healing process, following excision of the articular surfaces of the mandibular joint in rabbits. J Anat 1963, 97:345-352.
13. Ehrlich M.G., Mankin H.J., Jones H., Grossman A., Crispen C., Ancona D. Biochemical confirmation of an experimental osteoarthritis model. J Bone Joint Surg Am 1975, 57:392-396.
14. Elmer R.M., Moskowitz R.W., Frankel V.H. Meniscal regeneration and postmeniscectomy degenerative joint disease. Clin Orthop Relat Res 1977, 304-310.
15. Heatley F.W. The meniscus - can it be repaired? An experimental investigation in rabbits. J Bone Joint Surg Br 1980, 62:397-402.
16. Paatsama S. The structure and histopathology of the canine meniscus. Am J Vet Res 1954, 15:495-499.
17. Cox J.S., Nye C.E., Schaefer W.W., Woodstein I.J. The degenerative effects of partial and total resection of the medial meniscus in dogs' knees. Clin Orthop Relat Res 1975, 178-183.
18. Little C.B., Ghosh P., Bellenger C.R. Topographic variation in biglycan and decorin synthesis by articular cartilage in the early stages of osteoarthritis: an experimental study in sheep. J Orthop Res 1996, 14:433-444.
19. Lutfi A.M. Morphological changes in the articular cartilage after meniscectomy. An experimental study in the monkey. J Bone Joint Surg Br 1975, 57:525-528.
20. Lynch M.A., Henning C.E., Glick K.R. Knee joint surface changes. Long-term follow-up meniscus tear treatment in stable anterior cruciate ligament reconstructions. Clin Orthop Relat Res 1983, 148-153.
21. Roos H., Lauren M., Adalberth T., Roos E.M., Jonsson K., Lohmander L.S. Knee osteoarthritis after meniscectomy: prevalence of radiographic changes after twenty-one years, compared with matched controls. Arthritis Rheum 1998, 41:687-693.
22. Andersson-Molina H., Karlsson H., Rockborn P. Arthroscopic partial and total meniscectomy: a long-term follow-up study with matched controls. Arthroscopy 2002, 18:183-189.
23. Weinand C., Peretti G.M., Adams S.B., Randolph M.A., Savvidis E., Gill T.J. Healing potential of transplanted allogeneic chondrocytes of three different sources in lesions of the avascular zone of the meniscus: a pilot study. Arch Orthop Trauma Surg 2006, 126:599-605.
24. Hickery M.S., Bayliss M.T., Dudhia J., Lewthwaite J.C., Edwards J.C., Pitsillides A.A. Age-related changes in the response of human articular cartilage to IL-1alpha and transforming growth factor-beta (TGF-beta): chondrocytes exhibit a diminished sensitivity to TGF-beta. J Biol Chem 2003, 278:53063-53071.
25. Mesiha M., Zurakowski D., Soriano J., Nielson J.H., Zarins B., Murray M.M. Pathologic characteristics of the torn human meniscus. Am J Sports Med 2007, 35:103-112.
26. 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.
27. Krebsbach P.H., Kuznetsov S.A., Bianco P., Robey P.G. Bone marrow stromal cells: characterization and clinical application. Crit Rev Oral Biol Med 1999, 10:165-181.
28. Shimomura K., Ando W., Tateishi K., Nansai R., Fujie H., Hart D.A., et al. The influence of skeletal maturity on allogenic synovial mesenchymal stem cell-based repair of cartilage in a large animal model. Biomaterials 2010, 31:8004-8011.
29. De Bari C., Dell'Accio F., Tylzanowski P., Luyten F.P. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 2001, 44:1928-1942.
30. Sakaguchi Y., Sekiya I., Yagishita K., Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005, 52:2521-2529.
31. Arnoczky S.P., Warren R.F. The microvasculature of the meniscus and its response to injury. An experimental study in the dog. Am J Sports Med 1983, 11:131-141.
32. Horie M., Sekiya I., Muneta T., Ichinose S., Matsumoto K., Saito H., et al. Intra-articular injected synovial stem cells differentiate into meniscal cells directly and promote meniscal regeneration without mobilization to distant organs in rat massive meniscal defect. Stem Cells 2009, 27:878-887.
33. Mizuno K., Muneta T., Morito T., Ichinose S., Koga H., Nimura A., et al. Exogenous synovial stem cells adhere to defect of meniscus and differentiate into cartilage cells. J Med Dent Sci 2008, 55:101-111.
34. Pereira H., Frias A.M., Oliveira J.M., Espregueira-Mendes J., Reis R.L. Tissue engineering and regenerative medicine strategies in meniscus lesions. Arthroscopy 2011, 27:1706-1719.
35. Daniels A.U., Andriano K.P., Smutz W.P., Chang M.K., Heller J. Evaluation of absorbable poly(ortho esters) for use in surgical implants. J Appl Biomater 1994, 5:51-64.
36. van der Elst M., Klein C.P., de Blieck-Hogervorst J.M., Patka P., Haarman H.J. Bone tissue response to biodegradable polymers used for intra medullary fracture fixation: a long-term in vivo study in sheep femora. Biomaterials 1999, 20:121-128.
37. Yang C., Hillas P.J., Baez J.A., Nokelainen M., Balan J., Tang J., et al. The application of recombinant human collagen in tissue engineering. BioDrugs 2004, 18:103-119.
38. Martin M.J., Muotri A., Gage F., Varki A. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 2005, 11:228-232.
39. Ando W., Tateishi K., Hart D.A., Katakai D., Tanaka Y., Nakata K., et al. Cartilage repair using an in vitro generated scaffold-free tissue-engineered construct derived from porcine synovial mesenchymal stem cells. Biomaterials 2007, 28:5462-5470.
40. Ando W., Tateishi K., Katakai D., Hart D.A., Higuchi C., Nakata K., et al. In vitro generation of a scaffold-free tissue-engineered construct (TEC) derived from human synovial mesenchymal stem cells: biological and mechanical properties and further chondrogenic potential. Tissue Eng Part A 2008, 14:2041-2049.
41. Peretti G.M., Gill T.J., Xu J.W., Randolph M.A., Morse K.R., Zaleske D.J. Cell-based therapy for meniscal repair: a large animal study. Am J Sports Med 2004, 32:146-158.
42. Sekiya I., Vuoristo J.T., Larson B.L., Prockop D.J. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci U S A 2002, 99:4397-4402.
43. Freemont A.J., Hoyland J. Lineage plasticity and cell biology of fibrocartilage and hyaline cartilage: its significance in cartilage repair and replacement. Eur J Radiol 2006, 57:32-36.
44. Dutton A.Q., Choong P.F., Goh J.C., Lee E.H., Hui J.H. Enhancement of meniscal repair in the avascular zone using mesenchymal stem cells in a porcine model. J Bone Joint Surg Br 2010, 92:169-175.
45. Chevrier A., Nelea M., Hurtig M.B., Hoemann C.D., Buschmann M.D. Meniscus structure in human, sheep, and rabbit for animal models of meniscus repair. J Orthop Res 2009, 27:1197-1203.
46. Ghadially F.N., Wedge J.H., Lalonde J.M. Experimental methods of repairing injured menisci. J Bone Joint Surg Br 1986, 68:106-110.
47. Vodicka P., Smetana K., Dvorankova B., Emerick T., Xu Y.Z., Ourednik J., et al. The miniature pig as an animal model in biomedical research. Ann N Y Acad Sci 2005, 1049:161-171.
48. Koski J.A., Ibarra C., Rodeo S.A., Warren R.F. Meniscal injury and repair: clinical status. Orthop Clin North Am 2000, 31:419-436.
49. Lyyra T., Kiviranta I., Vaatainen U., Helminen H.J., Jurvelin J.S. In vivo characterization of indentation stiffness of articular cartilage in the normal human knee. J Biomed Mater Res 1999, 48:482-487.
50. Achari Y., Reno C.R., Frank C.B., Hart D.A. Carrageenan-induced transient inflammation in a rabbit knee model: molecular changes consistent with an early osteoarthritis phenotype. Inflamm Res 2012, 61:907-914.
51. Nauta A.J., Fibbe W.E. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007, 110:3499-3506.
52. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res 2006, 312:2169-2179.
53. Nasef A., Ashammakhi N., Fouillard L. Immunomodulatory effect of mesenchymal stromal cells: possible mechanisms. Regen Med 2008, 3:531-546.
54. Pabbruwe M.B., Kafienah W., Tarlton J.F., Mistry S., Fox D.J., Hollander A.P. Repair of meniscal cartilage white zone tears using a stem cell/collagen-scaffold implant. Biomaterials 2010, 31:2583-2591.
55. Nerurkar N.L., Han W., Mauck R.L., Elliott D.M. Homologous structure-function relationships between native fibrocartilage and tissue engineered from MSC-seeded nanofibrous scaffolds. Biomaterials 2011, 32:461-468.
56. Hennerbichler A., Moutos F.T., Hennerbichler D., Weinberg J.B., Guilak F. Repair response of the inner and outer regions of the porcine meniscus in vitro. Am J Sports Med 2007, 35:754-762.
57. McNulty A.L., Moutos F.T., Weinberg J.B., Guilak F. Enhanced integrative repair of the porcine meniscus in vitro by inhibition of interleukin-1 or tumor necrosis factor alpha. Arthritis Rheum 2007, 56:3033-3042.