The effect of collagen crosslinking on the biphasic poroviscoelastic cartilage properties determined from a semi-automated microindentation protocol for stress relaxation

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 34, Issue , 2014, Pages 264-272

  McGann, Megan E ^a   Bonitsky, Craig M ^a   Ovaert, Timothy C ^a   Wagner, Diane R ^a  

^a University of Notre Dame   (United States)

Author keywords

Advanced glycation end products; Articular cartilage; Collagen crosslinking; Finite element; Indentation; Stress relaxation

Indexed keywords

COLLAGEN; FINITE ELEMENT METHOD; INDENTATION; ITERATIVE METHODS; MECHANICAL ENGINEERING; MECHANICAL PROPERTIES; STRESS RELAXATION; UNLOADING;

ADVANCED GLYCATION END PRODUCTS; ARTICULAR CARTILAGES; CARTILAGE MECHANICS; COLLAGEN CROSSLINKING; OLIVER-PHARR METHOD; TIME DEPENDENT BEHAVIOR; TIME-DEPENDENT PROPERTIES; VISCOELASTIC COEFFICIENTS;

CARTILAGE;

ADVANCED GLYCATION END PRODUCT; COLLAGEN; RIBOSE; CROSS LINKING REAGENT;

ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE MATRIX; CROSS LINKING; FINITE ELEMENT ANALYSIS; HARDNESS; LEISURE; NONHUMAN; OLIVER PHARR METHOD; PRIORITY JOURNAL; RELAXATION TIME; SEMI AUTOMATED MICROINDENTATION PROTOCOL; STRESS; STRESS RELAXATION; SURFACE PROPERTY; TRANSDUCER; VISCOELASTICITY; YOUNG MODULUS; ANIMAL; AUTOMATION; BOVINAE; CHEMISTRY; DRUG EFFECTS; ELASTICITY; MATERIALS TESTING; MECHANICAL STRESS; METABOLISM; POROSITY; PROCEDURES; VISCOSITY;

ANIMALS; AUTOMATION; CARTILAGE, ARTICULAR; CATTLE; COLLAGEN; CROSS-LINKING REAGENTS; ELASTICITY; FINITE ELEMENT ANALYSIS; MATERIALS TESTING; POROSITY; RIBOSE; STRESS, MECHANICAL; SURFACE PROPERTIES; VISCOSITY;

EID: 84896081404     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2014.02.013     Document Type: Article

References (55)

1. Akizuki S., Mow V.C., Muller F., Pita J.C., Howell D.S., Manicourt D.H. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J. Orthop. Res. 1986, 4(4):379-392.
2. Ateshian G.A., Soltz M.A., Mauck R.L., Basalo I.M., Hung C.T., Lai W.M. The role of osmotic pressure and tension-compression nonlinearity in the frictional response of articular cartilage. Transp. Porous Media 2003, 50(1-2):5-33.
3. Athanasiou K.A., Rosenwasser M.P., Buckwalter J.A., Malinin T.I., Mow V.C. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J. Orthop. Res. 1991, 9(3):330-340.
4. Bank R.A., Bayliss M.T., Lafeber F.P., Maroudas A., Tekoppele J.M. Ageing and zonal variation in post-translational modification of collagen in normal human articular cartilage. The age-related increase in non-enzymatic glycation affects biomechanical properties of cartilage. Biochem. J. 1998, 330(Pt 1):345-351.
5. Bank R.A., Verzijl N., Lafeber F.P., Tekoppele J.M. Putative role of lysyl hydroxylation and pyridinoline cross-linking during adolescence in the occurrence of osteoarthritis at old age. Osteoarthritis Cartil. 2002, 10(2):127-134.
6. Blum M.M., Ovaert T.C. Experimental and numerical tribological studies of a boundary lubricant functionalized poro-viscoelastic PVA hydrogel in normal contact and sliding. J. Mech. Behav. Biomed. Mater. 2012.
7. Blum M.M., Ovaert T.C. Investigation of friction and surface degradation of innovative boundary lubricant functionalized hydrogel material for use as artificial articular cartilage. Wear 2012.
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. J. Biomech. 2004, 37(8):1251-1261.
9. Chen A.C., Temple M.M., Ng D.M., Verzijl N., DeGroot J., TeKoppele J.M., et al. Induction of advanced glycation end products and alterations of the tensile properties of articular cartilage. Arthritis Rheum. 2002, 46(12):3212-3217.
10. Cheng Y., Cheng C. Relationships between initial unloading slope, contact depth, and mechanical properties for conical indentation in linear viscoelastic solids. J. Mater. Res. 2005, 20(4):1046-1053.
11. DeGroot J., Verzijl N., Jacobs K., Budde M., Bank R, Bijlsma J, et al. Accumulation of advanced glycation endproducts reduces chondrocyte-mediated extracellular matrix turnover in human articular cartilage. Osteoarthritis Cartil. 2001, 9(8):720-726.
12. DeGroot J., Verzijl N., Bank R.A., Lafeber F.P., Bijlsma J.W., TeKoppele J.M. Age-related decrease in proteoglycan synthesis of human articular chondrocytes: the role of nonenzymatic glycation. Arthritis Rheum. 1999, 42(5):1003-1009.
13. DiSilvestro M.R., Suh J.F. A cross-validation of the biphasic poroviscoelastic model of articular cartilage in unconfined compression, indentation, and confined compression. J. Biomech. 2001, 34(4):519-525.
14. Ebenstein D., Pruitt L. Nanoindentation of soft hydrated materials for application to vascular tissues. J. Biomed. Mater. Res. Part A 2004, 69(2):222-232.
15. Habelitz S., Marshall S., Marshall G., Balooch M. Mechanical properties of human dental enamel on the nanometre scale. Arch. Oral Biol. 2001, 46(2):173-183.
16. Han L., Grodzinsky A.J., Ortiz C. Nanomechanics of the cartilage extracellular matrix. Annu. Rev. Mater. Res. 2011, 41:133.
17. Haut R.C., Little R.W. A constitutive equation for collagen fibers. J. Biomech. 1972, 5(5):423-430.
18. Hayes W., Bodine A. Flow-independent viscoelastic properties of articular cartilage matrix. J. Biomech. 1978, 11(8):407-419.
19. Hori R.Y., Mockros L. Indentation tests of human articular cartilage. J. Biomech. 1976, 9(4):259-268.
20. 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. J. Biomech. Eng. 2003, 125(1):84-93.
21. Huang C.Y., Stankiewicz A., Ateshian G.A., Mow V.C. Anisotropy, inhomogeneity, and tension-compression nonlinearity of human glenohumeral cartilage in finite deformation. J. Biomech. 2005, 38(4):799-809.
22. Jeng Y., Mao C., Wu K. Instrumented indentation investigation on the viscoelastic properties of porcine cartilage. J. Bionic Eng. 2013, 10(4):522-531.
23. Kaufman J.D., Klapperich C.M. Surface detection errors cause overestimation of the modulus in nanoindentation on soft materials. J. Mech. Behav. Biomed. Mater. 2009, 2(4):312-317.
24. Kempson G., Freeman M., Swanson S. The determination of a creep modulus for articular cartilage from indentation tests on the human femoral head. J. Biomech. 1971, 4(4):239-250.
25. Kempson G., Spivey C., Swanson S., Freeman M. Patterns of cartilage stiffness on normal and degenerate human femoral heads. J. Biomech. 1971, 4(6):597-609.
26. Kohn J.C., Ebenstein D.M. Eliminating adhesion errors in nanoindentation of compliant polymers and hydrogels. J. Mech. Behav. Biomed. Mater. 2013.
27. Korhonen R., Laasanen M., Töyräs J., Rieppo J., Hirvonen J., Helminen H., et al. Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. J. Biomech. 2002, 35(7):903-909.
28. Lai W.M., Mow V.C. Drag-induced compression of articular cartilage during a permeation experiment. Biorheology 1980, 17(1-2):111-123.
29. Liu K., Ovaert T.C. Poro-viscoelastic constitutive modeling of unconfined creep of hydrogels using finite element analysis with integrated optimization method. J. Mech. Behav. Biomed. Mater. 2011, 4(3):440-450.
30. Liu K., VanLandingham M.R., Ovaert T.C. Mechanical characterization of soft viscoelastic gels via indentation and optimization-based inverse finite element analysis. J. Mech. Behav. Biomed. Mater. 2009, 2(4):355-363.
31. McGann M.E., Vahdati A., Wagner D.R. Methods to assess in vitro wear of articular cartilage. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 2012, 226(8):612-622.
32. Miller G.J., Morgan E.F. Use of microindentation to characterize the mechanical properties of articular cartilage: comparison of biphasic material properties across length scales. Osteoarthritis Cartil. 2010, 18(8):1051-1057.
33. Mow V., Gibbs M., Lai W., Zhu W., Athanasiou K. Biphasic indentation of articular cartilage-II. A numerical algorithm and an experimental study. J. Biomech. 1989, 22(8):853-861.
34. Oliver W.C., Pharr G.M. Improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 1992, 7(6):1564-1583.
35. Oyen M. Nanoindentation of biological and biomimetic materials. Exp. Tech. 2013, 37(1):73-87.
36. Richard F., Villars M., Thibaud S. Viscoelastic modeling and quantitative experimental characterization of normal and osteoarthritic human articular cartilage using indentation. J. Mech. Behav. Biomed. Mater. 2013.
37. Sanjeevi R., Somanathan N., Ramaswamy D. A viscoelastic model for collagen fibres. J. Biomech. 1982, 15(3):181-183.
38. Schinagl R.M., Gurskis D., Chen A.C., Sah R.L. Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. J. Orthop. Res. 1997, 15(4):499-506.
39. Seifzadeh A., Oguamanam D., Trutiak N., Hurtig M., Papini M. Determination of nonlinear fibre-reinforced biphasic poroviscoelastic constitutive parameters of articular cartilage using stress relaxation indentation testing and an optimizing finite element analysis. Comput. Methods Programs Biomed 2012, 107(2):315-326.
40. Shekhawat V., Laurent M., Muehleman C., Wimmer M. Surface topography of viable articular cartilage measured with scanning white light interferometry. Osteoarthritis Cartil. 2009, 17(9):1197-1203.
41. Slaboch C.L., Alber M.S., Rosen E.D., Ovaert T.C. Mechano-rheological properties of the murine thrombus determined via nanoindentation and finite element modeling. J. Mech. Behav. Biomed. Mater. 2012, 10:75-86.
42. Soltz M.A., Ateshian G.A.A. Conewise linear elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. J. Biomech. Eng. 2000, 122(6):576-586.
43. Spirt A.A., Mak A.F., Wassell R.P. Nonlinear viscoelastic properties of articular cartilage in shear. J. Orthop. Res. 1989, 7(1):43-49.
44. Suh J., Bai S. Finite element formulation of biphasic poroviscoelastic model for articular cartilage. J. Biomech. Eng. 1998, 120(2):195-201.
45. Sung H.W., Chang Y., Chiu C.T., Chen C.N., Liang H.C. Crosslinking characteristics and mechanical properties of a bovine pericardium fixed with a naturally occurring crosslinking agent. J. Biomed. Mater. Res. 1999, 47(2):116-126.
46. Tang B., Ngan A. A rate-jump method for characterization of soft tissues using nanoindentation techniques. Soft Matter 2012, 8(22):5974-5979.
47. Thornton G., Leask G., Shrive N., Frank C. Early medial collateral ligament scars have inferior creep behaviour. J. Orthop. Res. 2000, 18(2):238-246.
48. Vahdati A., Wagner D.R. Finite element study of a tissue-engineered cartilage transplant in human tibiofemoral joint. Comput. Methods Biomech. Biomed. Eng. 2012, 15(11):1211-1221.
49. van der Voet A. A comparison of finite element codes for the solution of biphasic poroelastic problems. Proc. Inst. Mech. Eng. H 1997, 211(2):209-211.
50. Verzijl N., DeGroot J., Ben Z.C., Brau-Benjamin O., Maroudas A., Bank R.A., et al. Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possible mechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum. 2002, 46(1):114-123.
51. Wagner D.R., Reiser K.M., Lotz J.C. Glycation increases human annulus fibrosus stiffness in both experimental measurements and theoretical predictions. J. Biomech. 2006, 39(6):1021-1029.
52. Warner M., Taylor W., Clift S. A Method for Determining Contact Between a Non-Porous Surface and Articular Cartilage in a Biphasic FE Model 2001.
53. 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. J. Orthop. Res. 2003, 21(5):872-880.
54. Wilson W., van Donkelaar C.C., van Rietbergen R., Huiskes R. The role of computational models in the search for the mechanical behavior and damage mechanisms of articular cartilage. Med. Eng. Phys. 2005, 27(10):810-826.
55. Zhu W., Mow V.C., Koob T.J., Eyre D.R. Viscoelastic shear properties of articular cartilage and the effects of glycosidase treatments. J. Orthop. Res. 1993, 11(6):771-781.