Bioactive stratified polymer ceramic-hydrogel scaffold for integrative osteochondral repair

Annals of Biomedical Engineering

Volumn 38, Issue 6, 2010, Pages 2183-2196

  Jiang, Jie ^a   Tang, Amy ^a   Ateshian, Gerard A ^a   Edward Guo, X ^a   Hung, Clark T ^a   Lu, Helen H ^a,b  

^a Fu Foundation School of Engineering and Applied Science   (United States)

^b Howard Hughes Medical Institute   (United States)

Author keywords

Bioactive glass; Hydrogel; Interface; Microsphere; Osteochondral; Tissue engineering

Indexed keywords

AGAROSE; ARTICULAR CARTILAGES; CARTILAGE REPAIR; CELL DENSITY; CHONDROCYTES; CHONDROGENESIS; COCULTURE; COMPOSITE MICROSPHERES; DESIGN AND OPTIMIZATION; HYDROGEL SCAFFOLDS; IN-VIVO; INTERFACE REGIONS; MINERALIZATION POTENTIAL; OSTEOCHONDRAL; OSTEOCHONDRAL TISSUE ENGINEERING; POLY LACTIDE-CO-GLYCOLIDE; SOFT TISSUE;

BIOMECHANICS; BIOMIMETICS; BODY FLUIDS; BONE; CARTILAGE; CELL CULTURE; GRAFTS; HYDROGELS; LIGAMENTS; MECHANICAL PROPERTIES; MICROSPHERES; OPTIMIZATION; PHASE INTERFACES; REPAIR; SCAFFOLDS; TISSUE ENGINEERING;

BIOACTIVE GLASS;

BIOMATERIAL; POLYMER; TISSUE SCAFFOLD;

ANIMAL; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CATTLE; CELL CULTURE; CERAMICS; CHEMISTRY; CYTOLOGY; EQUIPMENT; EQUIPMENT DESIGN; HYDROGEL; INSTRUMENTATION; OSTEOBLAST; PHYSIOLOGY; TISSUE ENGINEERING;

ANIMALS; BIOCOMPATIBLE MATERIALS; CATTLE; CELLS, CULTURED; CERAMICS; CHONDROCYTES; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; HYDROGELS; OSTEOBLASTS; OSTEOGENESIS; POLYMERS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 77954658858     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-010-0038-y     Document Type: Article

References (83)

1. Ahsan, T., L. M. Lottman, F. Harwood, D. Amiel, and R. L. Sah. Integrative cartilage repair: inhibition by betaaminopropionitrile. J. Orthop. Res. 17:850-857, 1999.
2. Akizuki, S., Y. Yasukawa, and T. Takizawa. A new method of hemostasis for cementless total knee arthroplasty. Bull. Hosp. Jt. Dis. 56:222-224, 1997.
3. Alhadlaq, A., and J. J. Mao. Tissue-engineered neogenesis of human-shaped mandibular condyle from rat mesenchymal stem cells. J. Dent. Res. 82:951-956, 2003.
4. Alhadlaq, A., and J. J. Mao. Tissue-engineered osteochondral constructs in the shape of an articular condyle. J. Bone Joint Surg. Am. 87:936-944, 2005.
5. Allan, K. S., R. M. Pilliar, J. Wang, M. D. Grynpas, and R. A. Kandel. Formation of biphasic constructs containing cartilage with a calcified zone interface. Tissue Eng. 13:167-177, 2007.
6. Angele, P., R. Kujat, M. Nerlich, J. Yoo, V. Goldberg, and B. Johnstone. Engineering of osteochondral tissue with bone marrow mesenchymal progenitor cells in a derivatized hyaluronan-gelatin composite sponge. Tissue Eng. 5:545-554, 1999.
7. Athanasiou, K. A., M. P. Rosenwasser, J. A. Buckwalter, T. I. Malinin, and V. C. Mow. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J. Orthop. Res. 9:330-340, 1991.
8. Beiser, I. H., and I. O. Kanat. Subchondral bone drilling: a treatment for cartilage defects. J. Foot Surg. 29:595-601, 1990.
9. Benya, P. D., and J. D. Shaffer. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30:215-224, 1982.
10. Boccaccini, A. R., and J. J. Blaker. Bioactive composite materials for tissue engineering scaffolds. Expert Rev. Med. Devices 2:303-317, 2005.
11. Bullough, P. G. The geometry of diarthrodial joints, its physiologic maintenance, and the possible significance of age-related changes in geometry-to-load distribution and the development of osteoarthritis. Clin. Orthop. Relat Res. 61-66, 1981.
12. Bullough, P. G. The role of joint architecture in the etiology of arthritis. Osteoarthr. Cartil. 12(Suppl A):S2-S9, 2004.
13. Bullough, P. G., and A. Jagannath. The morphology of the calcification front in articular cartilage. Its significance in joint function. J. Bone Joint Surg. Br. 65:72-78, 1983.
14. Burr, D. B. Anatomy and physiology of the mineralized tissues: Role in the pathogenesis of osteoarthrosis. Osteoarthr. Cartil. 12(Suppl A):S20-S30, 2004.
15. Buschmann, M. D., Y. A. Gluzband, A. J. Grodzinsky, and E. B. Hunziker. Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J. Cell Sci. 108(Pt 4):1497-1508, 1995.
16. Buschmann, M. D., Y. A. Gluzband, A. J. Grodzinsky, J. H. Kimura, and E. B. Hunziker. Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix. J. Orthop. Res. 10:745-758, 1992.
17. Cao, T., K. H. Ho, and S. H. Teoh. Scaffold design and in vitro study of osteochondral coculture in a threedimensional porous polycaprolactone scaffold fabricated by fused deposition modeling. Tissue Eng. 9(Suppl 1):S103-S112, 2003.
18. Chowdhury, T. T., D. L. Bader, and D. A. Lee. Dynamic compression counteracts il-1 beta-induced release of nitric oxide and pge2 by superficial zone chondrocytes cultured in agarose constructs. Osteoarthr. Cartil. 11:688-696, 2003.
19. Collins, D. H. The Pathology of Articular and Spinal Diseases. Baltimore, MD: William & Wilkins, 1950.
20. D;Lima, D. D., S. Hashimoto, P. C. Chen, C. W. Colwell, Jr., and M. K. Lotz. Impact of mechanical trauma on matrix and cells. Clin. Orthop. Relat Res. S90-S99, 2001.
21. Elisseeff, J., C. Puleo, F. Yang, and B. Sharma. Advances in skeletal tissue engineering with hydrogels. Orthod. Craniofac. Res. 8:150-161, 2005.
22. Fawns, H. T., and J. W. Landells. Histochemical studies of rheumatic conditions. I. Observations on the fine structures of the matrix of normal bone and cartilage. Ann. Rheum. Dis. 12:105-113, 1953.
23. Frenkel, S. R., G. Bradica, J. H. Brekke, S. M. Goldman, K. Ieska, P. Issack, M. R. Bong, H. Tian, J. Gokhale, R. D. Coutts, and R. T. Kronengold. Regeneration of articular cartilage-evaluation of osteochondral defect repair in the rabbit using multiphasic implants. Osteoarthr. Cartil. 13:798-807, 2005.
24. Gao, J., J. E. Dennis, L. A. Solchaga, A. S. Awadallah, V. M. Goldberg, and A. I. Caplan. Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng. 7:363-371, 2001.
25. Gao, J., J. E. Dennis, L. A. Solchaga, V. M. Goldberg, and A. I. Caplan. Repair of osteochondral defect with tissueengineered two-phase composite material of injectable calcium phosphate and hyaluronan sponge. Tissue Eng. 8:827-837, 2002.
26. Hangody, L., G. Kish, Z. Karpati, I. Szerb, and I. Udvarhelyi. Arthroscopic autogenous osteochondral mosaicplasty for the treatment of femoral condylar articular defects. A preliminary report. Knee Surg. Sports Traumatol. Arthrosc. 5:262-267, 1997. (Pubitemid 127541076)
27. Harley, B. A., A. K. Lynn, Z. Wissner-Gross, W. Bonfield, I. V. Yannas, and L. J. Gibson. Design of a multiphase osteochondral scaffold iii: fabrication of layered scaffolds with continuous interfaces. J. Biomed. Mater. Res. A 92: 1078-1093.
28. Harper, M. C. Viscous isoamyl 2-cyanoacrylate as an osseous adhesive in the repair of osteochondral osteotomies in rabbits. J. Orthop. Res. 6:287-292, 1988.
29. Havelka, S., V. Horn, D. Spohrova, and P. Valouch. The calcified-noncalcified cartilage interface: the tidemark. Acta Biol. Hung. 35:271-279, 1984.
30. Haynes, D. W. The mineralization front of articular cartilage. Metab. Bone Dis. Rel. Res. 2(suppl):55-59, 1980.
31. Hench, L. L. Bioceramics: from concept to clinic. J. Am. Ceram. Soc. 74(7):1487-1510, 1991.
32. Hench, L. L., and J. M. Polak. Third-generation biomedical materials. Science 295:1014-1017, 2002.
33. Holland, T. A., E. W. Bodde, L. S. Baggett, Y. Tabata, A. G. Mikos, and J. A. Jansen. Osteochondral repair in the rabbit model utilizing bilayered, degradable oligo(poly (ethylene glycol) fumarate) hydrogel scaffolds. J. Biomed. Mater. Res. A 75:156-167, 2005.
34. Hung, C. T., E. G. Lima, R. L. Mauck, E. Taki, M. A. LeRoux, H. H. Lu, R. G. Stark, X. E. Guo, and G. A. Ateshian. Anatomically shaped osteochondral constructs for articular cartilage repair. J. Biomech. 36:1853-1864, 2003.
35. Hunziker, E. B., and I. M. Driesang. Functional barrier principle for growth-factor-based articular cartilage repair. Osteoarthr. Cartil. 11:320-327, 2003.
36. Hunziker, E. B., I. M. Driesang, and C. Saager. Structural barrier principle for growth factor-based articular cartilage repair. Clin. Orthop. Relat. Res. S182-S189, 2001.
37. Jackson, D. W., M. J. Scheer, and T. M. Simon. Cartilage substitutes: overview of basic science and treatment options. J. Am. Acad. Orthop. Surg. 9:37-52, 2001.
38. Jiang, J., S. B. Nicoll, and H. H. Lu. Co-culture of osteoblasts and chondrocytes modulates cellular differentiation in vitro. Biochem. Biophys. Res. Commun. 338:762-770, 2005.
39. Kandel, R. A., M. Grynpas, R. Pilliar, J. Lee, J. Wang, S. Waldman, P. Zalzal, and M. Hurtig. Repair of osteochondral defects with biphasic cartilage-calcium polyphosphate constructs in a sheep model. Biomaterials 27:4120-4131, 2006.
40. Khanarian, N. T., S. A. McArdle, and H. H. Lu. Effects of 45s5 bioactive glass particles on chondrocyte biosynthesis and mineralization. Society for Biomaterials Proceedings, 2009.
41. Kim, Y. J., R. L. Sah, J. Y. Doong, and A. J. Grodzinsky. Fluorometric assay of DNA in cartilage explants using hoechst 33258. Anal. Biochem. 174:168-176, 1988.
42. Lane, L. B., and P. G. Bullough. Age-related changes in the thickness of the calcified zone and the number of tidemarks in adult human articular cartilage. J. Bone Jt. Surg. Br. 62:372-375, 1980.
43. Lemperg, R. The subchondral bone plate of the femoral head in adult rabbits. I. Spontaneus remodelling studied by microradiography and tetracycline labelling. Virchows Arch. A Pathol. Pathol. Anat. 352:1-13, 1971.
44. Lethbridge-Cejku, M., J. S. Schiller, and L. Bernadel. Summary health statistics for U.S. adults: National Health Interview Survey, 2002. Vital Health Stat. 10.222:1-151, 2004.
45. Lima, E. G., L. Bian, K. W. Ng, R. L. Mauck, B. A. Byers, R. S. Tuan, G. A. Ateshian, and C. T. Hung. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with tgf-beta3. Osteoarthr. Cartil. 15:1025-1033, 2007.
46. Lu, H. H., S. F. El Amin, K. D. Scott, and C. T. Laurencin. Three-dimensional, bioactive, biodegradable, polymerbioactive glass composite scaffolds with improved mechanical properties support collagen synthesis and mineralization of human osteoblast-like cells in vitro. J. Biomed. Mater. Res. 64A:465-474, 2003.
47. Lu, H. H., J. M. Vo, J. Lin, S. Shin, M. Cozin, R. Tsay, and R. Landesberg. Controlled delivery of growth factors derived from platelet-rich plasma for bone formation. J. Biomed. Mater. Res. A 86A(4):1128-1136, 2008.
48. Lu, H. H., A. Tang, S. C. Oh, J. P. Spalazzi, and K. Dionisio. Compositional effects on the formation of a calcium phosphate layer and the response of osteoblast-like cells on polymer-bioactive glass composites. Biomaterials 26:6323-6334, 2005.
49. Lyons, T. J., R. W. Stoddart, S. F. McClure, and J. McClure. The tidemark of the chondro-osseous junction of the normal human knee joint. J. Mol. Histol. 36:207-215, 2005.
50. Matava, M. J., and P. A. Hughes. Removal of a retained herbert-whipple screw with use of the osteochondral autograft transfer system (oats) core harvester: a case report. Am. J. Orthop. 33:598-601, 2004.
51. Mauck, R. L., S. L. Seyhan, G. A. Ateshian, and C. T. Hung. Influence of seeding density and dynamic deformational loading on the developing structure/function relationships of chondrocyte-seeded agarose hydrogels. Ann. Biomed. Eng. 30:1046-1056, 2002.
52. Mauck, R. L., C. C. Wang, E. S. Oswald, G. A. Ateshian, and C. T. Hung. The role of cell seeding density and nutrient supply for articular cartilage tissue engineering with deformational loading. Osteoarthr. Cartil. 11:879-890, 2003.
53. Mow, V. C., W. Y. Gu, F. H. Chen, and R. Huiskes. Structure and function of articular cartilage and meniscus. In: Basic Orthopaedic Biomechanics and Mechano-biology. Philadelphia: Lippincott Williams and Wilkins, 2007, pp. 181-258.
54. Mow, V. C., C. S. Proctor, M. A. Kelly, M. Nordin, H. F. Victor, and K. Forssen. Biomechanics of articular cartilage. In: Basic Biomechanics of the Musculoskeletal System. Philadelphia, PA: Lea and Febiger, 1989, pp. 31-58.
55. Ng, K. W., L. E. Kugler, S. B. Doty, G. A. Ateshian, and C. T. Hung. Scaffold degradation elevates the collagen content and dynamic compressive modulus in engineered articular cartilage. Osteoarthr. Cartil. 17:220-227, 2009.
56. Ng, K. W., E. G. Lima, L. Bian, C. J. O;Conor, P. S. Jayabalan, A. M. Stoker, K. Kuroki, C. R. Cook, G. A. Ateshian, J. L. Cook, and C. T. Hung. Passaged adult chondrocytes can form engineered cartilage with functional mechanical properties: a canine model. Tissue Eng. A 16:1041-1051, 2009.
57. Niederauer, G. G., M. A. Slivka, N. C. Leatherbury, D. L. Korvick, H. H. Harroff, W. C. Ehler, C. J. Dunn, and K. Kieswetter. Evaluation of multiphase implants for repair of focal osteochondral defects in goats. Biomaterials 21:2561-2574, 2000.
58. O;Driscoll, S. W., F. W. Keeley, and R. B. Salter. The chondrogenic potential of free autogenous periosteal grafts for biological resurfacing of major full-thickness defects in joint surfaces under the influence of continuous passive motion. An experimental investigation in the rabbit. J. Bone Jt. Surg. Am. 68:1017-1035, 1986.
59. Ochi, M., Y. Uchio, M. Tobita, and M. Kuriwaka. Current concepts in tissue engineering technique for repair of cartilage defect. Artif. Organs 25:172-179, 2001.
60. Oegema, Jr., T. R., R. J. Carpenter, F. Hofmeister, and R. C. Thompson, Jr. The interaction of the zone of calcified cartilage and subchondral bone in osteoarthritis. Microsc. Res. Tech. 37:324-332, 1997.
61. Oegema, Jr., T. R., S. L. Johnson, T. Meglitsch, and R. J. Carpenter. Prostaglandins and the zone of calcified cartilage in osteoarthritis. Am. J. Ther. 3:139-149, 1996.
62. Oegema, T. R., Jr., R. C. Thompson, Jr., and C.-G. K. Brandt. Cartilage-bone interface (tidemark). In: Cartilage Changes in Osteoarthritis. Indianapolis, IN: Indiana School of Medicine Publ., 1990, pp. 43-52.
63. Oegema, T. R., Jr., R. C. Thompson, Jr., K. E. Kuettner, R. Schleyerbach, J. G. Peyron, and V. C. Hascall. The zone of calcified cartilage. Its role in osteoarthritis. In: Articular Cartilage and Osteoarthritis. New York, NY: Raven Press, 1992, pp. 319-331.
64. Oettmeier, R., K. Abendroth, and S. Oettmeier. Analyses of the tidemark on human femoral heads. I. Histochemical, ultrastructural and microanalytic characterization of the normal structure of the intercartilaginous junction. Acta Morphol. Hung. 37:155-168, 1989.
65. Radin, E. L., D. B. Burr, B. Caterson, D. Fyhrie, T. D. Brown, and R. D. Boyd. Mechanical determinants of osteoarthrosis. Semin. Arthr. Rheum. 21:12-21, 1991.
66. Reddy, G. K., and C. S. Enwemeka. A simplified method for the analysis of hydroxyproline in biological tissues. Clin. Biochem. 29:225-229, 1996.
67. Redler, I., V. C. Mow, M. L. Zimny, and J. Mansell. The ultrastructure and biomechanical significance of the tidemark of articular cartilage. Clin. Orthop. Relat Res. 112:357-362, 1975.
68. Redman, S. N., S. F. Oldfield, and C. W. Archer. Current strategies for articular cartilage repair. Eur. Cell Mater. 9:23-32, 2005.
69. Roberts, S. R., M. M. Knight, D. A. Lee, and D. L. Bader. Mechanical compression influences intracellular ca2+signaling in chondrocytes seeded in agarose constructs. J. Appl. Physiol. 90:1385-1391, 2001.
70. Schaefer, D., I. Martin, G. Jundt, J. Seidel, M. Heberer, A. Grodzinsky, I. Bergin, G. Vunjak-Novakovic, and L. E. Freed. Tissue-engineered composites for the repair of large osteochondral defects. Arthr. Rheum. 46:2524-2534, 2002.
71. Schaefer, D., I. Martin, P. Shastri, R. F. Padera, R. Langer, L. E. Freed, and G. Vunjak-Novakovic. In vitro generation of osteochondral composites. Biomaterials 21:2599-2606, 2000.
72. Schek, R. M., J. M. Taboas, S. J. Hollister, and P. H. Krebsbach. Tissue engineering osteochondral implants for temporomandibular joint repair. Orthod. Craniofac. Res. 8:313-319, 2005.
73. Schek, R. M., J. M. Taboas, S. J. Segvich, S. J. Hollister, and P. H. Krebsbach. Engineered osteochondral grafts using biphasic composite solid free-form fabricated scaffolds. Tissue Eng. 10:1376-1385, 2004.
74. Shao, X., J. C. Goh, D. W. Hutmacher, E. H. Lee, and G. Zigang. Repair of large articular osteochondral defects using hybrid scaffolds and bone marrow-derived mesenchymal stem cells in a rabbit model. Tissue Eng. 12:1539-1551, 2006.
75. Sherwood, J. K., S. L. Riley, R. Palazzolo, S. C. Brown, D. C. Monkhouse, M. Coates, L. G. Griffith, L. K. Landeen, and A. Ratcliffe. A three-dimensional osteochondral composite scaffold for articular cartilage repair. Biomaterials 23:4739-4751, 2002.
76. Singh, S., C. C. Lee, and B. K. Tay. Results of arthroscopic abrasion arthroplasty in osteoarthritis of the knee joint. Singapore Med. J. 32:34-37, 1991.
77. Sledge, S. L. Microfracture techniques in the treatment of osteochondral injuries. Clin. Sports Med. 20:365-377, 2001.
78. Solchaga, L. A., J. Gao, J. E. Dennis, A. Awadallah, M. Lundberg, A. I. Caplan, and V. M. Goldberg. Treatment of osteochondral defects with autologous bone marrow in a hyaluronan-based delivery vehicle. Tissue Eng. 8:333-347, 2002.
79. Solchaga, L. A., J. S. Temenoff, J. Gao, A. G. Mikos, A. I. Caplan, and V. M. Goldberg. Repair of osteochondral defects with hyaluronan- and polyester-based scaffolds. Osteoarthr. Cartil. 13:297-309, 2005.
80. Spalazzi, J. P., K. L. Dionisio, J. Jiang, and H. H. Lu. Osteoblast and chondrocyte interactions during coculture on scaffolds. IEEE Eng. Med. Biol. Mag. 22:27-34, 2003.
81. Teixeira, C. C., M. Hatori, P. S. Leboy, M. Pacifici, and I. M. Shapiro. A rapid and ultrasensitive method for measurement of DNA, calcium and protein content, and alkaline phosphatase activity of chondrocyte cultures. Calcif. Tissue Int. 56:252-256, 1995.
82. Thambyah, A. A hypothesis matrix for studying biomechanical factors associated with the initiation and progression of posttraumatic osteoarthritis. Med. Hypotheses 64:1157-1161, 2005.
83. Tuli, R., S. Nandi, W. J. Li, S. Tuli, X. Huang, P. A. Manner, P. Laquerriere, U. Noth, D. J. Hall, and R. S. Tuan. Human mesenchymal progenitor cell-based tissue engineering of a single-unit osteochondral construct. Tissue Eng. 10:1169-1179, 2004.