The role of viscoelasticity of collagen fibers in articular cartilage: axial tension versus compression.

The role of viscoelasticity of collagen fibers in bovine articular cartilage was examined in compression and tension using stress relaxation measurements in the axial direction (normal to the articular surface). Experimentally, for a given axial strain, both peak and equilibrium loads were higher in tension than in compression, whereas stress relaxation was stronger in compression, as indicated by the higher peak-to-equilibrium ratios. A viscoelastic fibril-reinforced model including fluid flow was used for analysis of the experimental data. The collagen fibrillar matrix was assumed to be viscoelastic with a strain-dependent tensile modulus, and the nonfibrillar matrix was modeled as linearly elastic. For axial tension, collagen viscoelasticity was found to account for most of the stress relaxation, while the effects of fluid pressurization on the tensile stress were negligible. In contrast, for axial compression, the dominant mechanism for stress relaxation arose from fluid pressurization, while the associated relaxation in collagen fibers mainly resulted in an increase in radial strain. The effective Poisson's ratio, defined as the ratio of the radial and axial strains, was generally smaller in compression than in tension, and deviated from the true Poisson's ratio in tensile tests because of the frictional contacts between the specimen and the loading platens. Furthermore, lower collagen elasticity in the axial direction was observed than in the radial direction. This study illustrates the essential role of collagen viscoelasticity and interstitial fluid pressurization in the mechanical response of articular cartilage.

[1]  A Shirazi-Adl,et al.  Nonlinear analysis of cartilage in unconfined ramp compression using a fibril reinforced poroelastic model. , 1999, Clinical biomechanics.

[2]  A Shirazi-Adl,et al.  Strain-rate dependent stiffness of articular cartilage in unconfined compression. , 2003, Journal of biomechanical engineering.

[3]  N. Mukherjee,et al.  Load sharing between solid and fluid phases in articular cartilage: II--Comparison of experimental results and u-p finite element predictions. , 1998, Journal of biomechanical engineering.

[4]  Dawn M Elliott,et al.  Direct measurement of the Poisson's ratio of human patella cartilage in tension. , 2002, Journal of biomechanical engineering.

[5]  W C Hayes,et al.  Flow-independent viscoelastic properties of articular cartilage matrix. , 1978, Journal of biomechanics.

[6]  George D. Pins,et al.  Effects of static axial strain on the tensile properties and failure mechanisms of self-assembled collagen fibers , 1997 .

[7]  T D Brown,et al.  Experimental determination of the linear biphasic constitutive coefficients of human fetal proximal femoral chondroepiphysis. , 1986, Journal of biomechanics.

[8]  Koichi Masuda,et al.  Tensile mechanical properties of bovine articular cartilage: Variations with growth and relationships to collagen network components , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[9]  A. Tria,et al.  Viscoelastic Behavior of Osteoarthritic Cartilage , 2001, Connective tissue research.

[10]  J Silvennoinen,et al.  Quantitative MR microscopy of enzymatically degraded articular cartilage , 2000, Magnetic resonance in medicine.

[11]  J Mizrahi,et al.  The "instantaneous" deformation of cartilage: effects of collagen fiber orientation and osmotic stress. , 1986, Biorheology.

[12]  A F Mak,et al.  Unconfined compression of hydrated viscoelastic tissues: a biphasic poroviscoelastic analysis. , 1986, Biorheology.

[13]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[14]  S L Woo,et al.  Quasi-linear viscoelastic properties of normal articular cartilage. , 1980, Journal of biomechanical engineering.

[15]  R. W. Little,et al.  A constitutive equation for collagen fibers. , 1972, Journal of biomechanics.

[16]  A Oloyede,et al.  The dramatic influence of loading velocity on the compressive response of articular cartilage. , 1992, Connective tissue research.

[17]  W Herzog,et al.  Evaluation of the finite element software ABAQUS for biomechanical modelling of biphasic tissues. , 1997, Journal of biomechanics.

[18]  Juha Töyräs,et al.  Fibril reinforced poroelastic model predicts specifically mechanical behavior of normal, proteoglycan depleted and collagen degraded articular cartilage. , 2003, Journal of biomechanics.

[19]  A. Shirazi-Adl,et al.  The role of fibril reinforcement in the mechanical behavior of cartilage. , 2002, Biorheology.

[20]  J S Jurvelin,et al.  Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: I--Simultaneous prediction of reaction force and lateral displacement. , 2001, Journal of biomechanical engineering.

[21]  J. Mizrahi,et al.  The increased swelling and instantaneous deformation of osteoarthritic cartilage is highly correlated with collagen degradation. , 2000, Arthritis and rheumatism.

[22]  S. Woo,et al.  Measurements of nonhomogeneous, directional mechanical properties of articular cartilage in tension. , 1976, Journal of biomechanics.

[23]  A F Mak,et al.  Nonlinear viscoelastic properties of articular cartilage in shear , 1989, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[24]  H. Helminen,et al.  Characterization of enzymatically induced degradation of articular cartilage using high frequency ultrasound. , 1999, Physics in medicine and biology.

[25]  Alice Maroudas,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. , 2002, Arthritis and rheumatism.

[26]  W Herzog,et al.  The role of viscoelasticity of collagen fibers in articular cartilage: theory and numerical formulation. , 2004, Biorheology.

[27]  V C Mow,et al.  The role of flow-independent viscoelasticity in the biphasic tensile and compressive responses of articular cartilage. , 2001, Journal of biomechanical engineering.

[28]  V C Mow,et al.  The biphasic poroviscoelastic behavior of articular cartilage: role of the surface zone in governing the compressive behavior. , 1993, Journal of biomechanics.

[29]  Michael D Buschmann,et al.  Nonlinear tensile properties of bovine articular cartilage and their variation with age and depth. , 2004, Journal of biomechanical engineering.

[30]  J. Suh,et al.  Biphasic Poroviscoelastic Behavior of Hydrated Biological Soft Tissue , 1999 .

[31]  V C Mow,et al.  Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus , 1986, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[32]  S Olsen,et al.  A Finite Element Analysis Methodology for Representing the Articular Cartilage Functional Structure , 2002, Computer methods in biomechanics and biomedical engineering.

[33]  P. Khalsa,et al.  Compressive behavior of articular cartilage is not completely explained by proteoglycan osmotic pressure. , 1997, Journal of biomechanics.

[34]  J. Suh,et al.  Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: II--Effect of variable strain rates. , 2001, Journal of biomechanical engineering.

[35]  V C Mow,et al.  The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. , 1980, The Journal of bone and joint surgery. American volume.

[36]  R Huiskes,et al.  Stresses in the local collagen network of articular cartilage: a poroviscoelastic fibril-reinforced finite element study. , 2004, Journal of biomechanics.

[37]  A. Maroudas,et al.  Balance between swelling pressure and collagen tension in normal and degenerate cartilage , 1976, Nature.

[38]  A. Tria,et al.  Elastic energy storage in human articular cartilage: estimation of the elastic modulus for type II collagen and changes associated with osteoarthritis. , 2002, Matrix biology : journal of the International Society for Matrix Biology.

[39]  S Cusack,et al.  Determination of the elastic constants of collagen by Brillouin light scattering. , 1979, Journal of molecular biology.

[40]  H J Helminen,et al.  Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. , 2002, Journal of biomechanics.

[41]  R. Sanjeevi,et al.  A viscoelastic model for collagen fibres. , 1982, Journal of biomechanics.

[42]  G E Kempson,et al.  The tensile properties of the cartilage of human femoral condyles related to the content of collagen and glycosaminoglycans. , 1973, Biochimica et biophysica acta.

[43]  W M Lai,et al.  Drag-induced compression of articular cartilage during a permeation experiment. , 1980, Biorheology.

[44]  Gerard A Ateshian,et al.  Experimental verification of the roles of intrinsic matrix viscoelasticity and tension-compression nonlinearity in the biphasic response of cartilage. , 2003, Journal of biomechanical engineering.

[45]  G E Kempson,et al.  The effects of leucocyte elastase on the mechanical properties of adult human articular cartilage in tension. , 1981, Biochimica et biophysica acta.

[46]  Neil D. Broom,et al.  The biomechanical ambiguity of the articular surface. , 1993, Journal of anatomy.

[47]  Gerard A Ateshian,et al.  Optical determination of anisotropic material properties of bovine articular cartilage in compression. , 2003, Journal of biomechanics.