A long-standing challenge in the biomechanics of connective tissues (e.g., articular cartilage, ligament, tendon) has been the reported disparities between their tensile and compressive properties. In general, the intrinsic tensile properties of the solid matrices of these tissues are dictated by the collagen content and microstructural architecture, and the intrinsic compressive properties are dictated by their proteoglycan content and molecular organization as well as water content. These distinct materials give rise to a pronounced and experimentally well-documented nonlinear tension–compression stress–strain responses, as well as biphasic or intrinsic extracellular matrix viscoelastic responses. While many constitutive models of articular cartilage have captured one or more of these experimental responses, no single constitutive law has successfully described the uniaxial tensile and compressive responses of cartilage within the same framework. The objective of this study was to combine two previously proposed extensions of the biphasic theory of Mow et al. [1980, ASME J. Biomech. Eng., 102, pp. 73–84] to incorporate tension–compression nonlinearity as well as intrinsic viscoelasticity of the solid matrix of cartilage. The biphasic-conewise linear elastic model proposed by Soltz and Ateshian [2000, ASME J. Biomech. Eng., 122, pp. 576–586] and based on the bimodular stress-strain constitutive law introduced by Curnier et al. [1995, J. Elasticity, 37, pp. 1–38], as well as the biphasic poroviscoelastic model of Mak [1986, ASME J. Biomech. Eng., 108, pp. 123–130], which employs the quasi-linear viscoelastic model of Fung [1981, Biomechanics: Mechanical Properties of Living Tissues, Springer-Verlag, New York], were combined in a single model to analyze the response of cartilage to standard testing configurations. Results were compared to experimental data from the literature and it was found that a simultaneous prediction of compression and tension experiments of articular cartilage, under stress-relaxation and dynamic loading, can be achieved when properly taking into account both flow-dependent and flow-independent viscoelasticity effects, as well as tension–compression nonlinearity.

1.
Mow
,
V. C.
,
Kuei
,
S. C.
,
Lai
,
W. M.
, and
Armstrong
,
C. G.
,
1980
, “
Biphasic Creep and Stress Relaxation of Articular Cartilage in Compression: Theory and Experiments
,”
ASME J. Biomech. Eng.
,
102
, pp.
73
84
.
2.
Frank
,
E. H.
, and
Grodzinsky
,
A. J.
,
1987
, “
Cartilage Electromechanics—II. A Continuum Model of Cartilage Electrokinetics and Correlation With Experiments
,”
J. Biomech.
,
20
, pp.
629
639
.
3.
Lai
,
W. M.
,
Hou
,
J. S.
, and
Mow
,
V. C.
,
1991
, “
A Triphasic Theory for the Swelling and Deformation Behaviors of Articular Cartilage
,”
ASME J. Biomech. Eng.
,
113
, pp.
245
258
.
4.
Ateshian
,
G. A.
,
Warden
,
W. H.
,
Kim
,
J. J.
,
Grelsamer
,
R. P.
, and
Mow
,
V. C.
,
1997
, “
Finite Deformation Biphasic Material Properties of Bovine Articular Cartilage From Confined Compression Experiments
,”
J. Biomech.
,
30
, pp.
1157
1164
.
5.
Huyghe
,
J. M.
, and
Janssen
,
J. D.
,
1997
, “
Quadriphasic Mechanics of Swelling Incompressible Porous Media
,”
Int. J. Eng. Sci.
,
35
, pp.
793
802
.
6.
Gu
,
W. Y.
,
Lai
,
W. M.
, and
Mow
,
V. C.
,
1998
, “
A Mixture Theory for Charged Hydrated Soft Tissues Containing Multi-electrolytes: Passive Transport and Swelling Behaviors
,”
ASME J. Biomech. Eng.
,
102
, pp.
169
180
.
7.
Soulhat
,
J.
,
Buschmann
,
M. D.
, and
Shirazi-Adl
,
A.
,
1999
, “
A Fibril-Network Reinforced Model of Cartilage in Unconfined Compression
,”
ASME J. Biomech. Eng.
,
121
, pp.
340
347
.
8.
Cohen
,
B.
,
Lai
,
W. M.
, and
Mow
,
V. C.
,
1998
, “
A Transversely Isotropic Biphasic Model for Unconfined Compression of Growth Plate and Chondroepiphysis
,”
ASME J. Biomech. Eng.
,
120
, pp.
491
496
.
9.
Cohen
,
B.
,
Gardner
,
T. R.
, and
Ateshian
,
G. A.
,
1993
, “
The Influence of Transverse Isotropy on Cartilage Indentation Behavior—A Study of the Human Humeral Head
,”
Trans. Orthop. Res. Soc.
,
18
, p.
185
185
.
10.
Mow
,
V. C.
,
Good
,
P. M.
, and
Gardner
,
T. R.
,
2000
, “
A New Method to Determine the Tensile Properties of Articular Cartilage Using the Indentation Test
,”
Trans. Orthop. Res. Soc.
,
25
, p.
103
103
.
11.
Hayes
,
W. C.
, and
Mockros
,
L. F.
,
1971
, “
Viscoelastic Properties of Human Articular Cartilage
,”
J. Appl. Physiol.
,
31
, pp.
562
568
.
12.
Hayes
,
W. C.
, and
Bodine
,
A. J.
,
1978
, “
Flow-Independent Viscoelastic Properties of Articular Cartilage Matrix
,”
J. Biomech.
,
11
, pp.
407
419
.
13.
Mak
,
A. F.
,
1986
, “
The Apparent Viscoelastic Behavior of Articular Cartilage—The Contributions From the Intrinsic Matrix Viscoelasticity and Interstitial Fluid Flows
,”
ASME J. Biomech. Eng.
,
108
, pp.
123
130
.
14.
Setton
,
L. A.
,
Zhu
,
W.
, and
Mow
,
V. C.
,
1993
, “
The Biphasic Poroviscoelastic Behavior of Articular Cartilage: Role of the Surface Zone in Governing the Compressive Behavior
,”
J. Biomech.
,
26
, pp.
581
592
.
15.
Suh
,
J.-K.
, and
DiSilvestro
,
M. R.
,
1999
, “
Biphasic Poroviscoelastic Behavior of Hydrated Biological Soft Tissue
,”
ASME J. Appl. Mech.
,
66
, pp.
528
535
.
16.
Suh
,
J.-K.
, and
Bai
,
S.
,
1997
, “
Biphasic Poroviscoelastic Behavior of Articular Cartilage in Creep Indentation Test
,”
Trans. Orthop. Res. Soc.
,
22
, p.
823
823
.
17.
DiSilvestro, M. R., Zhu, Q., and Suh, J.-K., 1999, “Biphasic Poroviscoelastic Theory Predicts the Strain Rate Dependent Viscoelastic Behavior of Articular Cartilage,” Proc. 1999 Bioeng. Conf., ASME BED-Vol. 42, pp. 105–106.
18.
Soltz
,
M. A.
, and
Ateshian
,
G. A.
,
2000
, “
Interstitial Fluid Pressurization During Confined Compression Cyclical Loading of Articular Cartilage
,”
Ann. Biomed. Eng.
,
28
, pp.
150
159
.
19.
Zhu
,
W.
,
Mow
,
V. C.
,
Koob
,
T. J.
, and
Eyre
,
D. R.
,
1993
, “
Viscoelastic Shear Properties of Articular Cartilage and the Effects of Glycosidase Treatments
,”
J. Orthop. Res.
,
11
, pp.
771
781
.
20.
Setton
,
L. A.
,
Mow
,
V. C.
, and
Howell
,
D. S.
,
1995
, “
Mechanical Behavior of Articular Cartilage in Shear Is Altered by Transection of the Anterior Cruciate Ligament
,”
J. Orthop. Res.
,
13
, pp.
473
482
.
21.
Mak
,
A. F.
,
1986
, “
Unconfined Compression of Hydrated Viscoelastic Tissues: A Biphasic Poroviscoelastic Analysis
,”
Biorheology
,
23
, pp.
371
383
.
22.
Soltz
,
M. A.
, and
Ateshian
,
G. A.
,
2000
, “
A Conewise Linear Elasticity Mixture Model for the Analysis of Tension-Compression Nonlinearity in Articular Cartilage
,”
ASME J. Biomech. Eng.
,
122
,
576
586
.
23.
Guilak
,
F.
,
Ratcliffe
,
A.
, and
Mow
,
V. C.
,
1995
, “
Chondrocyte Deformation and Local Tissue Strain in Articular Cartilage: A Confocal Microscopy Study
,”
J. Orthop. Res.
,
13
, pp.
410
421
.
24.
Schinagl
,
R. M.
,
Gurskis
,
D.
,
Chen
,
A. C.
, and
Sah
,
R. L.
,
1997
, “
Depth-Dependent Confined Compression Modulus of Full-Thickness Bovine Articular Cartilage
,”
J. Orthop. Res.
,
15
, pp.
499
506
.
25.
Wang
,
C. C.-B.
,
Soltz
,
M. A.
,
Mauck
,
R. L.
,
Valhmu
,
W. B.
,
Ateshian
,
G. A.
, and
Hung
,
C. T.
,
2000
, “
Comparison of Equilibrium Axial Strain Distribution in Articular Cartilage Explants and Cell-Seeded Alginate Disks Under Unconfined Compression
,”
Trans. Orthop. Res. Soc.
,
25
, p.
131
131
.
26.
Wang
,
C. C.-B.
,
Hung
,
C. T.
, and
Mow
,
V. C.
,
2001
, “
An Analysis of the Effects of Depth-Dependent Aggregate Modulus on Articular Cartilage Stress-Relaxation Behavior in Compression
,”
J. Biomech.
,
34
,
75
84
.
27.
Li
,
L. P.
,
Buschmann
,
M. D.
, and
Shirazi-Adl
,
A.
,
2000
, “
A Fibril Reinforced Nonhomogeneous Poroelastic Model for Articular Cartilage: Inhomogeneous Response in Unconfined Compression
,”
J. Biomech.
,
33
, pp.
1533
1541
.
28.
Holmes
,
M. H.
, and
Mow
,
V. C.
,
1990
, “
The Nonlinear Characteristics of Soft Gels and Hydrated Connective Tissues in Ultrafiltration
,”
J. Biomech.
,
23, pp.
1145
1156
.
29.
Soltz
,
M. A.
, and
Ateshian
,
G. A.
,
1998
, “
Experimental Verification and Theoretical Prediction of Cartilage Interstitial Fluid Pressurization at an Impermeable Contact Interface in Confined Compression
,”
J. Biomech.
,
31
, pp.
927
934
.
30.
Armstrong
,
C. G.
,
Mow
,
V. C.
, and
Lai
,
W. M.
,
1984
, “
An Analysis of Unconfined Compression of Articular Cartilage
,”
ASME J. Biomech. Eng.
,
106
, pp.
165
173
.
31.
Curnier
,
A.
,
He
,
Q.-C.
, and
Zysset
,
P.
,
1995
, “
Conewise Linear Elastic Materials
,”
J. Elast.
,
37
, pp.
1
38
.
32.
Kempson
,
G. E.
,
Freeman
,
M. A.
, and
Swanson
,
S. A.
,
1968
, “
Tensile Properties of Articular Cartilage
,”
Nature (London)
,
220
, pp.
1127
1128
.
33.
Woo
,
S. L.-Y.
,
Akeson
,
W. H.
, and
Jemmott
,
G. F.
,
1976
, “
Measurements of Nonhomogeneous, Directional Mechanical Properties of Articular Cartilage in Tension
,”
J. Biomech.
,
9
, pp.
785
791
.
34.
Armstrong
,
C. G.
, and
Mow
,
V. C.
,
1982
, “
Variations in the Intrinsic Mechani-cal Properties of Human Articular Cartilage With Age, Degeneration, and Water Content
,”
J. Bone Jt. Surg., Am. Vol.
,
64A
, pp.
88
94
.
35.
Akizuki
,
S.
,
Mow
,
V. C.
,
Muller
,
F.
,
Pita
,
J. C.
,
Howell
,
D. S.
, and
Manicourt
,
D. H.
,
1986
, “
Tensile Properties of Human Knee Joint Cartilage: I. Influence of Ionic Conditions, Weight Bearing, and Fibrillation on the Tensile Modulus
,”
J. Orthop. Res.
,
4
, pp.
379
-
392
.
36.
Akizuki
,
S.
,
Mow
,
V. C.
,
Muller
,
F.
,
Pita
,
J. C.
, and
Howell
,
D. S.
,
1987
, “
Tensile Properties of Human Knee Joint Cartilage. II. Correlations Between Weight Bearing and Tissue Pathology and the Kinetics of Swelling
,”
J. Orthop. Res.
,
5
, pp.
173
-
186
.
37.
Schmidt
,
M. B.
,
Mow
,
V. C.
,
Chun
,
L. E.
, and
Eyre
,
D. R.
,
1990
, “
Effects of Proteoglycan Extraction on the Tensile Behavior of Articular Cartilage
,”
J. Orthop. Res.
,
8
, pp.
353
363
.
38.
Huang, C.-Y., Stankiewicz, A., Ateshian, G. A., Flatow, E. L., Bigliani, L. U., and Mow, V. C., 1999, “Tensile and Compressive Stiffness of Human Glenohumeral Cartilage Under Finite Deformation,” Proc. 1999 Bioeng. Conf., ASME BED-Vol. 42, pp. 469–470.
39.
Soltz
,
M. A.
,
Palma
,
C.
,
Barsoumian
,
S.
,
Wang
,
C. C.-B.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
,
2000
, “
Multi-Axial Loading of Bovine Articular Cartilage in Unconfined Compression
,”
Trans. Orthop. Res. Soc.
,
25
, p.
888
888
.
40.
Woo
,
S. L.-Y
,
Simon
,
B. R.
,
Kuei
,
S. C.
, and
Akeson
,
W. H.
,
1980
, “
Quasi-Linear Viscoelastic Properties of Normal Articular Cartilage
,”
ASME J. Biomech. Eng.
,
102
, pp.
85
90
.
41.
Ahmed
,
A. M.
, and
Burke
,
D. L.
,
1983
, “
In-Vitro Measurement of Static Pressure Distribution in Synovial Joints—Part I: Tibial Surface of the Knee
,”
ASME J. Biomech. Eng.
,
105
, pp.
216
-
225
.
42.
Huberti
,
H. H.
, and
Hayes
,
W. C.
,
1984
, “
Patellofemoral Contact Pressures. The Influence of Q-Angle and Tendofemoral Contact
,”
J. Bone Jt. Surg., Am. Vol.
,
66A
, pp.
715
724
.
43.
Fung, Y. C., 1981, Biomechanics: Mechanical Properties of Living Tissues, Springer-Verlag, New York.
44.
Mansour
,
J. M.
, and
Mow
,
V. C.
,
1976
, “
The Permeability of Articular Cartilage Under Compressive Strain and at High Pressures
,”
J. Bone Jt. Surg., Am. Vol.
,
58A
, pp.
509
516
.
45.
Khalsa
,
P. S.
, and
Eisenberg
,
S. R.
,
1997
, “
Compressive Behavior of Articular Cartilage Is Not Completely Explained by Proteoglycan Osmotic Pressure
,”
J. Biomech.
,
30
, pp.
589
594
.
46.
Mak, A. F., 1985, “Uniaxial Tension of Hydrated Viscoelastic Tissues,” ASME Adv. Bioengng, N. A. Langrana, ed., pp. 18–19.
47.
LeRoux
,
M. A.
,
Ateshian
,
G. A.
,
Vail
,
T. P.
, and
Setton
,
L. A.
,
2001
, “
Effects of Collagen Fiber Anisotropy on the Hydraulic Permeability of the Meniscus
,”
Trans. Orthop. Res. Soc.
,
26
, p.
45
45
.
48.
Hodge
,
W. A.
,
Carlson
,
K. L.
,
Fijan
,
R. S.
,
Burgess
,
R. G.
,
Riley
,
P. O.
,
Harris
,
W. H.
, and
Mann
,
R. W.
,
1989
, “
Contact Pressures From an Instrumented Hip Endoprosthesis
,”
J. Bone Jt. Surg., Am. Vol.
,
71A
, pp.
1378
1386
.
49.
Lee
,
R. C.
,
Frank
,
E. H.
,
Grodzinsky
,
A. J.
, and
Roylance
,
D. K.
,
1981
, “
Oscillatory Compressional Behavior of Articular Cartilage and Its Associated Electromechanical Properties
,”
ASME J. Biomech. Eng.
,
103
, pp.
280
292
.
50.
Kim
,
Y. J.
,
Bonassar
,
L. J.
, and
Grodzinsky
,
A. J.
,
1995
, “
The Role of Cartilage Streaming Potential, Fluid Flow and Pressure in the Stimulation of Chondrocyte Biosynthesis During Dynamic Compression
,”
J. Biomech.
,
28
, pp.
1055
1066
.
51.
Buschmann
,
M. D.
,
Kim
,
Y. J.
,
Wong
,
M.
,
Frank
,
E.
,
Hunziker
,
E. B.
, and
Grodzinsky
,
A. J.
,
1999
, “
Stimulation of Aggrecan Synthesis in Cartilage Explants by Cyclic Loading Is Localized to Regions of High Interstitial Fluid Flow
,”
Arch. Biochem. Biophys.
,
366
, pp.
1
7
.
You do not currently have access to this content.