Tissue-engineered articular cartilage exhibits tension-compression nonlinearity reminiscent of the native cartilage

Journal of Biomechanics

Volumn 46, Issue 11, 2013, Pages 1784-1791

  Kelly, Terri Ann N ^a   Roach, Brendan L ^a   Weidner, Zachary D ^c   Mackenzie Smith, Charles R ^a   O'Connell, Grace D ^a   Lima, Eric G ^d   Stoker, Aaron M ^e   Cook, James L ^f   Ateshian, Gerard A ^b   Hung, Clark T ^a  

^a Department of Earth and Environmental Sciences   (United States)

^b St Luke's Roosevelt Hospital ^*  (United States)

^c ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

^d Open Source Hardware Laboratory   (United States)

^e UNIVERSITY OF MISSOURI   (United States)

^f UNIVERSITY OF MISSOURI   (United States)

Author keywords

Collagen; Compressive properties; Optimized digital image correlation; Osmotic loading; Tensile properties

Indexed keywords

ARTICULAR CARTILAGES; COMPRESSIVE PROPERTIES; DIGITAL IMAGE CORRELATIONS; ENGINEERED CARTILAGE; FRICTIONAL COEFFICIENTS; INTERSTITIAL FLUID PRESSURIZATION; OSMOTIC LOADINGS; UNCONFINED COMPRESSION;

CARTILAGE; COLLAGEN; COMPRESSION TESTING; DYNAMIC LOADS; OSMOSIS; TENSILE PROPERTIES;

TISSUE;

SODIUM CHLORIDE;

ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BIOMECHANICS; CARTILAGE CELL; COMPRESSION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEFORMITY; DEVELOPMENTAL STAGE; DOG; EQUILIBRIUM MODULUS; FRICTION; HYDROGEL; INTERMETHOD COMPARISON; INTERSTITIAL FLUID; KNEE; NONHUMAN; OSMOLARITY; OSMOSIS; OSMOTIC LOADING; PRESSURE; PRIORITY JOURNAL; TENSILE MODULUS; TENSILE STRENGTH; TENSION; TISSUE ENGINEERING; VALIDATION STUDY; VIDEO MICROSCOPY;

COLLAGEN; COMPRESSIVE PROPERTIES; OPTIMIZED DIGITAL IMAGE CORRELATION; OSMOTIC LOADING; TENSILE PROPERTIES;

ANIMALS; BIOMECHANICAL PHENOMENA; CARTILAGE, ARTICULAR; COMPRESSIVE STRENGTH; DOGS; ELASTIC MODULUS; MODELS, BIOLOGICAL; NONLINEAR DYNAMICS; OSMOTIC PRESSURE; STRESS, MECHANICAL; TENSILE STRENGTH; TISSUE ENGINEERING;

EID: 84880037835     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2013.05.017     Document Type: Article

References (52)

1. Amici E., Clark A.H., Normand V., Johnson N.B. Interpenetrating network formation in gellan-agarose gel composites. Biomacromolecules 2000, 1:721-729.
2. Ateshian G.A., Chahine N.O., Basalo I.M., Hung C.T. The correspondence between equilibrium biphasic and triphasic material properties in mixture models of articular cartilage. Journal of Biomechanics 2004, 37:391-400.
3. Basser P.J., Schneiderman R., Bank R.A., Wachtel E., Maroudas A. Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Archives of Biochemistry and Biophysics 1998, 351:207-219.
4. Bian L., Angione S.L., Ng K.W., Lima E.G., Williams D.Y., Mao D.Q., Ateshian G.A., Hung C.T. Influence of decreasing nutrient path length on the development of engineered cartilage. Osteoarthritis Cartilage 2009, 17:677-685.
5. Bian L., Crivello K.M., Ng K.W., Xu D., Williams D.Y., Ateshian G.A., Hung C.T. Influence of temporary chondroitinase ABC-induced glycosaminoglycan suppression on maturation of tissue-engineered cartilage. Tissue Engineering Part A 2009, 15:2065-2072.
6. Bian L., Fong J.V., Lima E.G., Stoker A.M., Ateshian G.A., Cook J.L., Hung C.T. Dynamic mechanical loading enhances functional properties of tissue-engineered cartilage using mature canine chondrocytes. Tissue Engineering Part A 2010, 16:1781-1790.
7. Chahine N.O., Chen F.H., Hung C.T., Ateshian G.A. Direct measurement of osmotic pressure of glycosaminoglycan solutions by membrane osmometry at room temperature. Biophysical Journal 2005, 89:1543-1550.
8. Chahine N.O., Wang C.C., Hung C.T., Ateshian G.A. Anisotropic strain-dependent material properties of bovine articular cartilage in the transitional range from tension to compression. Journal of Biomechanics 2004, 37:1251-1261.
9. Cohen B., Lai W.M., Mow V.C. A transversely isotropic biphasic model for unconfined compression of growth plate and chondroepiphysis. Journal of Biomechanical Engineering 1998, 120:491-496.
10. Ehrlich S., Wolff N., Schneiderman R., Maroudas A., Parker K.H., Winlove C.P. The osmotic pressure of chondroitin sulphate solutions: experimental measurements and theoretical analysis. Biorheology 1998, 35:383-397.
11. Eleswarapu, S.V., Athanasiou, K.A., 2012. TRPV4 channel activation improves the tensile properties of self-assembled articular cartilage constructs. Acta Biomaterialia.
12. Eleswarapu S.V., Chen J.A., Athanasiou K.A. Temporal assessment of ribose treatment on self-assembled articular cartilage constructs. Biochemical and Biophysical Research Communications 2011, 414:431-436.
13. Gemmiti C.V., Guldberg R.E. Fluid flow increases type II collagen deposition and tensile mechanical properties in bioreactor-grown tissue-engineered cartilage. Tissue Engineering 2006, 12:469-479.
14. Gemmiti C.V., Guldberg R.E. Shear stress magnitude and duration modulates matrix composition and tensile mechanical properties in engineered cartilaginous tissue. Biotechnology and Bioengineering 2009, 104:809-820.
15. Grodzinsky A.J. Electromechanical and physicochemical properties of connective tissue. Critical Reviews in Biomedical Engineering 1983, 9:133-199.
16. Huang A.H., Baker B.M., Ateshian G.A., Mauck R.L. Sliding contact loading enhances the tensile properties of mesenchymal stem cell-seeded hydrogels. European Cells & Materials Journal 2012, 24:29-45.
17. Huang A.H., Yeger-McKeever M., Stein A., Mauck R.L. Tensile properties of engineered cartilage formed from chondrocyte- and MSC-laden hydrogels. Osteoarthritis Cartilage 2008, 16:1074-1082.
18. Huang C.Y., Mow V.C., Ateshian G.A. The role of flow-independent viscoelasticity in the biphasic tensile and compressive responses of articular cartilage. Journal of Biomechanical Engineering 2001, 123:410-417.
19. Huang C.Y., Soltz M.A., Kopacz M., Mow V.C., Ateshian G.A. Experimental verification of the roles of intrinsic matrix viscoelasticity and tension-compression nonlinearity in the biphasic response of cartilage. Journal of Biomechanical Engineering 2003, 125:84-93.
20. Huang C.Y., Stankiewicz A., Ateshian G.A., Mow V.C. Anisotropy, inhomogeneity, and tension-compression nonlinearity of human glenohumeral cartilage in finite deformation. Journal of Biomechanics 2005, 38:799-809.
21. Kelly T.A., Ng K.W., Wang C.C., Ateshian G.A., Hung C.T. Spatial and temporal development of chondrocyte-seeded agarose constructs in free-swelling and dynamically loaded cultures. Journal of Biomechanics 2006, 39:1489-1497.
22. Kelly T.A., Wang C.C., Mauck R.L., Ateshian G.A., Hung C.T. Role of cell-associated matrix in the development of free-swelling and dynamically loaded chondrocyte-seeded agarose gels. Biorheology 2004, 41:223-237.
23. Kempson G.E., Freeman M.A., Swanson S.A. Tensile properties of articular cartilage. Nature 1968, 220:1127-1128.
24. Knight M.M., Lee D.A., Bader D.L. The influence of elaborated pericellular matrix on the deformation of isolated articular chondrocytes cultured in agarose. Biochimica et Biophysica Acta 1998, 1405:67-77.
25. Krishnan R., Kopacz M., Ateshian G.A. Experimental verification of the role of interstitial fluid pressurization in cartilage lubrication. Journal of Orthopaedic Research 2004, 22:565-570.
26. Lai W.M., Hou J.S., Mow V.C. A triphasic theory for the swelling and deformation behaviors of articular cartilage. Journal of Biomechanical Engineering 1991, 113:245-258.
27. Lanir Y. Biorheology and fluid flux in swelling tissues, II. Analysis of unconfined compressive response of transversely isotropic cartilage disc. Biorheology 1987, 24:189-205.
28. Lee D.A., Bader D.L. The development and characterization of an in vitro system to study strain-induced cell deformation in isolated chondrocytes. In Vitro Cellular & Developmental Biology Animal 1995, 31:828-835.
29. Lima E.G., Bian L., Ng K.W., Mauck R.L., Byers B.A., Tuan R.S., Ateshian G.A., Hung C.T. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-beta3. Osteoarthritis Cartilage 2007, 15:1025-1033.
30. Maroudas A.I. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 1976, 260:808-809.
31. Mauck R.L., Seyhan S.L., Ateshian G.A., Hung C.T. Influence of seeding density and dynamic deformational loading on the developing structure/function relationships of chondrocyte-seeded agarose hydrogels. Annals of Biomedical Engineering 2002, 30:1046-1056.
32. Mauck R.L., Soltz M.A., Wang C.C., Wong D.D., Chao P.H., Valhmu W.B., Hung C.T., Ateshian G.A. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. Journal of Biomechanical Engineering 2000, 122:252-260.
33. McGowan K.B., Kurtis M.S., Lottman L.M., Watson D., Sah R.L. Biochemical quantification of DNA in human articular and septal cartilage using PicoGreen and Hoechst 33258. Osteoarthritis Cartilage 2002, 10:580-587.
34. Moutos F.T., Guilak F. Functional properties of cell-seeded three-dimensionally woven poly(epsilon-caprolactone) scaffolds for cartilage tissue engineering. Tissue Engineering Part A 2010, 16:1291-1301.
35. Natoli R.M., Responte D.J., Lu B.Y., Athanasiou K.A. Effects of multiple chondroitinase ABC applications on tissue engineered articular cartilage. Journal of Orthopaedic Research 2009, 27:949-956.
36. Natoli R.M., Revell C.M., Athanasiou K.A. Chondroitinase ABC treatment results in greater tensile properties of self-assembled tissue-engineered articular cartilage. Tissue Engineering Part A 2009, 15:3119-3128.
37. Natoli R.M., Skaalure S., Bijlani S., Chen K.X., Hu J., Athanasiou K.A. Intracellular Na(+) and Ca(2+) modulation increases the tensile properties of developing engineered articular cartilage. Arthritis & Rheumatism 2010, 62:1097-1107.
38. Normand V., Lootens D.L., Amici E., Plucknett K.P., Aymard P. New insight into agarose gel mechanical properties. Biomacromolecules 2000, 1:730-738.
39. Overbeek J.T. The Donnan equilibrium. Progress in Biophysics and Chemistry 1956, 6:57-84.
40. Park S., Ateshian G.A. Dynamic response of immature bovine articular cartilage in tension and compression, and nonlinear viscoelastic modeling of the tensile response. Journal of Biomechanical Engineering 2006, 128:623-630.
41. Park S., Hung C.T., Ateshian G.A. Mechanical response of bovine articular cartilage under dynamic unconfined compression loading at physiological stress levels. Osteoarthritis Cartilage 2004, 12:65-73.
42. Park S., Krishnan R., Nicoll S.B., Ateshian G.A. Cartilage interstitial fluid load support in unconfined compression. Journal of Biomechanics 2003, 36:1785-1796.
43. Riesle J., Hollander A.P., Langer R., Freed L.E., Vunjak-Novakovic G. Collagen in tissue-engineered cartilage: types, structure, and crosslinks. Journal of Cellular Biochemistry 1998, 71:313-327.
44. Soltz M.A., Ateshian G.A. A conewise linear elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. Journal of Biomechanical Engineering 2000, 122:576-586.
45. Soulhat J., Buschmann M.D., Shirazi-Adl A. A fibril-network-reinforced biphasic model of cartilage in unconfined compression. Journal of Biomechanical Engineering 1999, 121:340-347.
46. Stegemann H., Stalder K. Determination of hydroxyproline. Clinica Chimica Acta 1967, 18:267-273.
47. Wang C.C., Chahine N.O., Hung C.T., Ateshian G.A. Optical determination of anisotropic material properties of bovine articular cartilage in compression. Journal of Biomechanics 2003, 36:339-353.
48. Wang C.C., Deng J.M., Ateshian G.A., Hung C.T. An automated approach for direct measurement of two-dimensional strain distributions within articular cartilage under unconfined compression. Journal of Biomechanical Engineering 2002, 124:557-567.
49. Wang C.C., Guo X.E., Sun D., Mow V.C., Ateshian G.A., Hung C.T. The functional environment of chondrocytes within cartilage subjected to compressive loading: a theoretical and experimental approach. Biorheology 2002, 39:11-25.
50. Williamson A.K., Chen A.C., Masuda K., Thonar E.J., Sah R.L. Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. Journal of Orthopaedic Research 2003, 21:872-880.
51. Williamson A.K., Masuda K., Thonar E.J., Sah R.L. Growth of immature articular cartilage in vitro: correlated variation in tensile biomechanical and collagen network properties. Tissue Engineering 2003, 9:625-634.
52. Wilson C.G., Palmer A.W., Zuo F., Eugui E., Wilson S., Mackenzie R., Sandy J.D., Levenston M.E. Selective and non-selective metalloproteinase inhibitors reduce IL-1-induced cartilage degradation and loss of mechanical properties. Matrix Biology 2007, 26:259-268.