High amplitude direct compressive strain enhances mechanical properties of scaffold-free tissue-engineered cartilage

Tissue Engineering - Part A

Volumn 17, Issue 9-10, 2011, Pages 1401-1411

  Hoenig, Elisa ^a   Winkler, Thomas ^a   Mielke, Gabriela ^a   Paetzold, Helge ^a   Schuettler, Daniel ^a   Goepfert, Christiane ^b   MacHens, Hans Günther ^c   Morlock, Michael M ^a   Schilling, Arndt F ^a,c  

^a Biomechanics Section   (Germany)

^b HAMBURG UNIVERSITY OF TECHNOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; ELASTIC MODULI; ELASTICITY; HYDROXYAPATITE; LIGAMENTS; MECHANICAL PROPERTIES; SCAFFOLDS (BIOLOGY); STRAIN;

BIOCHEMICAL PROPERTIES; CHONDROCYTES; COLLAGEN CONTENT; COMPRESSION AMPLITUDE; COMPRESSIVE STRAIN; CONTROL GROUPS; DYNAMIC COMPRESSION; GLYCOSAMINOGLYCANS; HIGH AMPLITUDES; HIGHER LOADS; IN-VIVO; MECHANICAL STIMULATION; POSITIVE CORRELATIONS; POSITIVE EFFECTS; TISSUE ENGINEERED CARTILAGE; YOUNG'S MODULUS;

CARTILAGE;

SUS;

ANIMAL; ARTICLE; CARTILAGE; CARTILAGE CELL; COMPRESSIVE STRENGTH; FEMALE; PHYSIOLOGICAL STRESS; SWINE; TISSUE ENGINEERING; WEIGHT BEARING;

ANIMALS; CARTILAGE; CHONDROCYTES; COMPRESSIVE STRENGTH; FEMALE; STRESS, PHYSIOLOGICAL; SWINE; TISSUE ENGINEERING; WEIGHT-BEARING;

EID: 79955001095     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0395     Document Type: Article

References (58)

1. Mankin, H.J. The response of articular cartilage to mechanical injury. J Bone Joint Surg Am 64, 460, 1982
2. Kotlarz, H., Gunnarsson, C.L., Fang, H., and Rizzo, J.A. Insurer and out-of-pocket costs of osteoarthritis in the US: evidence from national survey data. Arthritis Rheum 60, 3546, 2009
3. Newman, A.P. Articular cartilage repair. Am J Sports Med 26, 309, 1998
4. Buschmann, M.D., Gluzband, Y.A., Grodzinsky, A.J., and Hunziker, E.B. Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J Cell Sci 108 (Pt 4), 1497, 1995
5. Vunjak-Novakovic, G., Martin, I., Obradovic, B., Treppo, S., Grodzinsky, A.J., Langer, R., and Freed, L.E. Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage. J Orthop Res 17, 130, 1999
6. Duda, G.N., Haisch, A., Endres, M., Gebert, C., Schroeder, D., Hoffmann, J.E., and Sittinger, M. Mechanical quality of tissue engineered cartilage: results after 6 and 12 weeks in vivo. J Biomed Mater Res 53, 673, 2000
7. Waldman, S.D., Grynpas, M.D., Pilliar, R.M., and Kandel, R.A. Characterization of cartilagenous tissue formed on calcium polyphosphate substrates in vitro. J Biomed Mater Res 62, 323, 2002
8. Palmoski, M., Perricone, E., and Brandt, K.D. Development and reversal of a proteoglycan aggregation defect in normal canine knee cartilage after immobilization. Arthritis Rheum 22, 508, 1979
9. Jurvelin, J., Kiviranta, I., Saamanen, A.M., Tammi, M., and Helminen, H.J. Partial restoration of immobilization-induced softening of canine articular cartilage after remobilization of the knee (stifle) joint. J Orthop Res 7, 352, 1989
10. Mauck, R.L., Soltz, M.A., Wang, C.C., Wong, D.D., Chao, P.H., Valhmu, W.B., Hung, C.T., and Ateshian, G.A. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122, 252, 2000
11. Waldman, S.D., Spiteri, C.G., Grynpas, M.D., Pilliar, R.M., and Kandel, R.A. Long-term intermittent compressive stimulation improves the composition and mechanical properties of tissue-engineered cartilage. Tissue Eng 10, 1323, 2004
12. Kisiday, J.D., Jin, M., DiMicco, M.A., Kurz, B., and Grodzinsky, A.J. Effects of dynamic compressive loading on chondrocyte biosynthesis in self-assembling peptide scaffolds. J Biomech 37, 595, 2004
13. Eckstein, F., Lemberger, B., Gratzke, C., Hudelmaier, M., Glaser, C., Englmeier, K.H., and Reiser, M. In vivo cartilage deformation after different types of activity and its dependence on physical training status. Ann Rheum Dis 64, 291, 2005
14. Bingham, J.T., Papannagari, R., Van, D.V., Gross, C., Gill, T.J., Felson, D.T., Rubash, H.E., and Li, G. In vivo cartilage contact deformation in the healthy human tibiofemoral joint. Rheumatology (Oxford) 47, 1622, 2008
15. Buschmann, M., Gluzband, Y., Grodzinsky, A., Kimura, J., Hunziker, E. Chondrocytes in agarose culture synthesize a mechanically functional extracellular matrix. J Orthop Res 10, 745, 1992
16. Matissek, R., Schnepel, F.M., and Steiner, G. Lebensmittelanalytik. Berlin: Springer Verlag, 1992
17. Brown, S., Worsfold, M., and Sharp, C. Microplate assay for the measurement of hydroxyproline in acid-hydrolyzed tissue samples. Biotechniques 30, 38, 2001
18. Brunk, C.F., Jones, K.C., and James, T.W. Assay for nanogram quantities of DNA in cellular homogenates. Anal Biochem 92, 497, 1979
19. Brehm, W., Aklin, B., Yamashita, T., Rieser, F., Trub, T., Jakob, R.P., and Mainil-Varlet, P. Repair of superficial osteochondral defects with an autologous scaffold-free cartilage construct in a caprine model: implantation method and short-term results. Osteoarthritis Cartilage 14, 1214, 2006
20. Han, E.H., Bae, W.C., Hsieh-Bonassera, N.D., Wong, V.W., Schumacher, B.L., Gortz, S., Masuda, K., Bugbee, W.D., and Sah, R.L. Shaped, stratified, scaffold-free grafts for articular cartilage defects. Clin Orthop Relat Res 466, 1912, 2008
21. Masuda, K., Sah, R.L., Hejna, M.J., and Thonar, E.J. A novel two-step method for the formation of tissue-engineered cartilage by mature bovine chondrocytes: the alginaterecovered- chondrocyte (ARC) method. J Orthop Res 21, 139, 2003
22. Murdoch, A.D., Grady, L.M., Ablett, M.P., Katopodi, T., Meadows, R.S., and Hardingham, T.E. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 25, 2786, 2007
23. Wiegandt, K., Goepfert, C., Poertner, R. Improving in vitro generated cartilage-carrier-constructs by optimizing growth factor combination. Open Biomed Eng J 1, 85, 2007
24. Hu, J.C., and Athanasiou, K.A. A self-assembling process in articular cartilage tissue engineering. Tissue Eng 12, 969, 2006
25. Murphy, C.L., and Sambanis, A. Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes. Tissue Eng 7, 791, 2001
26. Elder, S.H., Goldstein, S.A., Kimura, J.H., Soslowsky, L.J., and Spengler, D.M. Chondrocyte differentiation is modulated by frequency and duration of cyclic compressive loading. Ann Biomed Eng 29, 476, 2001
27. Lima, E.G., Bian, L., Ng, K.W., Mauck, R.L., Byers, B.A., Tuan, R.S., Ateshian, G.A., and Hung, C.T. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-beta3. Osteoarthritis Cartilage 15, 1025, 2007
28. Concaro, S., Nicklasson, E., Ellowsson, L., Lindahl, A., Brittberg, M., and Gatenholm, P. Effect of cell seeding concentration on the quality of tissue engineered constructs loaded with adult human articular chondrocytes. J Tissue Eng Regen Med 2, 14, 2008
29. Hoemann, C.D., Sun, J., McKee, M.D., Chevrier, A., Rossomacha, E., Rivard, G.E., Hurtig, M., and Buschmann, M.D. Chitosan-glycerol phosphate/blood implants elicit hyaline cartilage repair integrated with porous subchondral bone in microdrilled rabbit defects. Osteoarthritis Cartilage 15, 78, 2007
30. Meinel, L., Hofmann, S., Karageorgiou, V., Zichner, L., Langer, R., Kaplan, D., and Vunjak-Novakovic, G. Engineering cartilage-like tissue using human mesenchymal stem cells and silk protein scaffolds. Biotechnol Bioeng 88, 379, 2004
31. Wang, Y., Kim, H.J., Vunjak-Novakovic, G., and Kaplan, D.L. Stem cell-based tissue engineering with silk biomaterials. Biomaterials 27, 6064, 2006
32. Dare, E.V., Griffith, M., Poitras, P., Kaupp, J.A., Waldman, S.D., Carlsson, D.J., Dervin, G., Mayoux, C., and Hincke, M.T. Genipin cross-linked fibrin hydrogels for in vitro human articular cartilage tissue-engineered regeneration. Cells Tissues Organs 190, 313, 2009
33. Lee, C.R., Breinan, H.A., Nehrer, S., and Spector, M. Articular cartilage chondrocytes in type I and type II collagen- GAG matrices exhibit contractile behavior in vitro. Tissue Eng 6, 555, 2000
34. Nehrer, S., Breinan, H.A., Ramappa, A., Shortkroff, S., Young, G., Minas, T., Sledge, C.B., Yannas, I.V., and Spector, M. Canine chondrocytes seeded in type I and type II collagen implants investigated in vitro. J Biomed Mater Res 38, 95, 1997
35. Grigolo, B., Roseti, L., Fiorini, M., Fini, M., Giavaresi, G., Aldini, N.N., Giardino, R., and Facchini, A. Transplantation of chondrocytes seeded on a hyaluronan derivative (hyaff-11) into cartilage defects in rabbits. Biomaterials 22, 2417, 2001
36. Solchaga, L.A., Yoo, J.U., Lundberg, M., Dennis, J.E., Huibregtse, B.A., Goldberg, V.M., and Caplan, A.I. Hyaluronanbased polymers in the treatment of osteochondral defects. J Orthop Res 18, 773, 2000
37. Mercier, N.R., Costantino, H.R., Tracy, M.A., and Bonassar, L.J. Poly(lactide-co-glycolide) microspheres as a moldable scaffold for cartilage tissue engineering. Biomaterials 26, 1945, 2005
38. Badylak, S.F. The extracellular matrix as a biologic scaffold material. Biomaterials 28, 3587, 2007
39. Baumbach, K., Petersen, J.P., Ueblacker, P., Schroder, J., Gopfert, C., Stork, A., Rueger, J.M., Amling, M., and Meenen, N.M. The fate of osteochondral grafts after autologous osteochondral transplantation: a one-year follow-up study in a minipig model. Arch.Orthop.Trauma Surg 128, 1255, 2008
40. Hu, J.C., and Athanasiou, K.A. Low-density cultures of bovine chondrocytes: effects of scaffold material and culture system. Biomaterials 26, 2001, 2005
41. Ng, K.W., Lima, E.G., Bian, L., O'Conor, C.J., Jayabalan, P.S., Stoker, A.M., Kuroki, K., Cook, C.R., Ateshian, G.A., Cook, J.L., and Hung, C.T. Passaged adult chondrocytes can form engineered cartilage with functional mechanical properties: a canine model. Tissue Eng Part A 16, 1041, 2010
42. Morlock, M., Schneider, E., Bluhm, A., Vollmer, M., Bergmann, G., Muller, V., and Honl, M. Duration and frequency of every day activities in total hip patients. J Biomech 34, 873, 2001
43. Darling, E.M., and Athanasiou, K.A. Articular cartilage bioreactors and bioprocesses. Tissue Eng 9, 9, 2003
44. Bergmann, G., Deuretzbacher, G., Heller, M., Graichen, F., Rohlmann, A., Strauss, J., and Duda, G.N. Hip contact forces and gait patterns from routine activities. J Biomech 34, 859, 2001
45. Lee, D.A., and Bader, D.L. Compressive strains at physiological frequencies influence the metabolism of chondrocytes seeded in agarose. J Orthop Res 15, 181, 1997
46. Chowdhury, T.T., Bader, D.L., Shelton, J.C., and Lee, D.A. Temporal regulation of chondrocyte metabolism in agarose constructs subjected to dynamic compression. Arch Biochem Biophys 417, 105, 2003
47. Bian, L., Fong, J.V., Lima, E.G., Stoker, A.M., Ateshian, G.A., Cook, J.L., and Hung, C.T. Dynamic mechanical loading enhances functional properties of tissue-engineered cartilage using mature canine chondrocytes. Tissue Eng Part A 16, 1781, 2010
48. Korhonen, R.K., Laasanen, M.S., Toyras, J., Rieppo, J., Hirvonen, J., Helminen, H.J., and Jurvelin, J.S. Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. J Biomech 35, 903, 2002
49. Graff, R.D., Kelley, S.S., and Lee, G.M. Role of pericellular matrix in development of a mechanically functional neocartilage. Biotechnol Bioeng 82, 457, 2003
50. Jakob, M., Demarteau, O., Schafer, D., Hintermann, B., Dick, W., Heberer, M., and Martin, I. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81, 368, 2001
51. Pei, M., Seidel, J., Vunjak-Novakovic, G., and Freed, L.E. Growth factors for sequential cellular de- and redifferentiation in tissue engineering. Biochem Biophys Res Commun 294, 149, 2002
52. Wiegandt, K., Goepfert, C., Richter, T., Fritsch, D., Janssen, R., and Portner, R. In vitro generation of cartilage-carrierconstructs on hydroxylapatite ceramics with different surface structures. Open Biomed Eng J 2, 64, 2008
53. Mauck, R.L., Seyhan, S.L., Ateshian, G.A., and Hung, C.T. Influence of seeding density and dynamic deformational loading on the developing structure/function relationships of chondrocyte-seeded agarose hydrogels. Ann Biomed Eng 30, 1046, 2002
54. Yan, D., Zhou, G., Zhou, X., Liu, W., Zhang, W.J., Luo, X., Zhang, L., Jiang, T., Cui, L., and Cao, Y. The impact of low levels of collagen IX and pyridinoline on the mechanical properties of in vitro engineered cartilage. Biomaterials 30, 814, 2009
55. Kreger, S.T., Bell, B.J., Bailey, J., Stites, E., Kuske, J., Waisner, B., and Voytik-Harbin, S.L. Polymerization and matrix physical properties as important design considerations for soluble collagen formulations. Biopolymers 93, 690, 2010
56. Bailey, J.L., Critser, P.J., Whittington, C., Kuske, J.L., Yoder, M.C., and Voytik-Harbin, S.L. Collagen oligomers modulate physical and biological properties of three-dimensional selfassembled matrices. Biopolymers 95, 77, 2011
57. Behrens, P., Bitter, T., Kurz, B., and Russlies, M. Matrixassociated autologous chondrocyte transplantation/implantation (MACT/MACI)-5-year follow-up. Knee 13, 194, 2006
58. Petersen, J.P., Ueblacker, P., Goepfert, C., Adamietz, P., Baumbach, K., Stork, A., Rueger, J.M., Poertner, R., Amling, M., and Meenen, N.M. Long term results after implantation of tissue engineered cartilage for the treatment of osteochondral lesions in a minipig model. J Mater Sci Mater Med 19, 2029, 2008