Osmotic pressure and associated residual stresses play important roles in cartilage development and biomechanical function. The curling behavior of articular cartilage was believed to be the combination of results from the osmotic pressure derived from fixed negative charges on proteoglycans and the structural and compositional and material property inhomogeneities within the tissue. In the present study, the in vitro swelling and curling behaviors of thin strips of cartilage were analyzed with a new structural model using the triphasic mixture theory with a collagen-proteoglycan solid matrix composed of a three-layered laminate with each layer possessing a distinct set of orthotropic properties. A conewise linear elastic matrix was also incorporated to account for the well-known tension-compression nonlinearity of the tissue. This model can account, for the first time, for the swelling-induced curvatures found in published experimental results on excised cartilage samples. The results suggest that for a charged-hydrated soft tissue, such as articular cartilage, the balance of proteoglycan swelling and the collagen restraining within the solid matrix is the origin of the in situ residual stress, and that the layered collagen ultrastructure, e.g., relatively dense and with high stiffness at the articular surface, play the dominate role in determining curling behaviors of such tissues.

1.
Toole
,
B. P.
, 1972, “
Hyaluronate Turnover During Chondrogenesis in the Developing Chick Limb and Axial Skeleton
,”
Dev. Biol.
0012-1606,
29
(
3
), pp.
321
329
.
2.
Feinberg
,
R. N.
, and
Beebe
,
D. C.
, 1983, “
Hyaluronate in Vasculogenesis
,”
Science
0036-8075,
220
(
4602
), pp.
1177
1179
.
3.
Oster
,
G. F.
,
Murray
,
J. D.
, and
Maini
,
P. K.
, 1985, “
A Model for Chondrogenic Condensations in the Developing Limb: The Role of Extracellular Matrix and Cell Tractions
,”
J. Embryol. Exp. Morphol.
0022-0752,
89
, pp.
93
112
.
4.
Mow
,
V. C.
,
Gu
,
W. Y.
, and
Chen
,
F. H.
, 2005, “
Structure and Function of Articular Cartilage and Meniscus
,”
Basic Orthopaedic Biomechanics and Mechano-Biology
,
Lippincott
,
Philadelphia
.
5.
Bian
,
L.
,
Crivello
,
K. M.
,
Ng
,
K. W.
,
Xu
,
D.
,
Williams
,
D. Y.
,
Ateshian
,
G. A.
, and
Hung
,
C. T.
, 2009, “
Influence of Temporary Chondroitinase ABC-Induced Glycosaminoglycan Suppression on Maturation of Tissue-Engineered Cartilage
,”
Tissue Eng., Part A
,
15
(
8
), pp.
2065
2072
.
6.
Natoli
,
R.
,
Revell
,
C. M.
, and
Athanasiou
,
K.
, 2009, “
Chondroitinase ABC Treatment Results in Increased Tensile Properties of Self-Assembled Tissue Engineered Articular Cartilage
,”
Tissue Eng., Part A
,
15
(
10
), pp.
3119
3128
.
7.
Fry
,
H.
, and
Robertson
,
W. V.
, 1967, “
Interlocked Stresses in Cartilage
,”
Nature (London)
0028-0836,
215
, pp.
53
54
.
8.
Setton
,
L. A.
,
Gu
,
W. Y.
,
Mow
,
V. C.
, and
Lai
,
W. M.
, 1995, “
Predictions of the Swelling-Induced Pre-Stress in Articular Cartilage
,”
Mechanics of Porous Media
,
Kluwer Academic
,
Dordrecht, The Netherlands
.
9.
Maroudas
,
A. I.
, 1976, “
Balance Between Swelling Pressure and Collagen Tension in Normal and Degenerate Cartilage
,”
Nature (London)
0028-0836,
260
(
5554
), pp.
808
809
.
10.
Heinegard
,
D.
,
Bayliss
,
M.
, and
Lorenzo
,
P.
, 2003, “
Biochemistry and Metabolism of Normal and Osteoarthritic Cartilage
,”
Osteoarthritis
,
Oxford University Press
,
New York
.
11.
Ehrlich
,
S.
,
Wolff
,
N.
,
Schneiderman
,
R.
,
Maroudas
,
A.
,
Parker
,
K. H.
, and
Winlove
,
C. P.
, 1998, “
The Osmotic Pressure of Chondroitin Sulphate Solutions: Experimental Measurements and Theoretical Analysis
,”
Biorheology
0006-355X,
35
(
6
), pp.
383
397
.
12.
Kovach
,
I. S.
, 1995, “
The Importance of Polysaccharide Configurational Entropy in Determining the Osmotic Swelling Pressure of Concentrated Proteoglycan Solution and the Bulk Compressive Modulus of Articular Cartilage
,”
Biophys. Chem.
0301-4622,
53
(
3
), pp.
181
187
.
13.
Urban
,
J. P.
,
Maroudas
,
A.
,
Bayliss
,
M. T.
, and
Dillon
,
J.
, 1979, “
Swelling Pressures of Proteoglycans at the Concentrations Found in Cartilaginous Tissues
,”
Biorheology
0006-355X,
16
(
6
), pp.
447
464
.
14.
Clark
,
J. M.
, 1990, “
The Organisation of Collagen Fibrils in the Superficial Zones of Articular Cartilage
,”
J. Anat.
0021-8782,
171
, pp.
117
130
.
15.
Clark
,
J. M.
, 1991, “
Variation of Collagen Fiber Alignment in a Joint Surface: A Scanning Electron Microscope Study of the Tibial Plateau in Dog, Rabbit, and Man
,”
J. Orthop. Res.
0736-0266,
9
(
2
), pp.
246
257
.
16.
Buschmann
,
M. D.
, and
Grodzinsky
,
A. J.
, 1995, “
A Molecular Model of Proteoglycan-Associated Electrostatic Forces in Cartilage Mechanics
,”
ASME J. Biomech. Eng.
0148-0731,
117
(
2
), pp.
179
192
.
17.
Eisenberg
,
S. R.
, and
Grodzinsky
,
A. J.
, 1985, “
Swelling of Articular Cartilage and Other Connective Tissues: Electromechanochemical Forces
,”
J. Orthop. Res.
0736-0266,
3
(
2
), pp.
148
159
.
18.
Myers
,
E. R.
,
Lai
,
W. M.
, and
Mow
,
V. C.
, 1984, “
A Continuum Theory and an Experiment for the Ion-Induced Swelling Behavior of Articular Cartilage
,”
ASME J. Biomech. Eng.
0148-0731,
106
(
2
), pp.
151
158
.
19.
Wilson
,
W.
,
Van Donkelaar
,
C. C.
,
Van Rietbergen
,
B.
, and
Huiskes
,
R.
, 2005, “
A Fibril-Reinforced Poroviscoelastic Swelling Model for Articular Cartilage
,”
J. Biomech.
0021-9290,
38
(
6
), pp.
1195
1204
.
20.
Setton
,
L. A.
,
Lai
,
W. M.
, and
Mow
,
V. C.
, 1993, “
Swelling-Induced Residual Stress and the Mechanism of Curling in Articular Cartilage in Vitro
,”
Advances in Bioengineering
, Vol.
26
, pp.
58
62
.
21.
Setton
,
L. A.
,
Tohyama
,
H.
, and
Mow
,
V. C.
, 1998, “
Swelling and Curling Behaviors of Articular Cartilage
,”
ASME J. Biomech. Eng.
0148-0731,
120
(
3
), pp.
355
361
.
22.
Olsen
,
S.
, and
Oloyede
,
A.
, 2002, “
A Finite Element Analysis Methodology for Representing the Articular Cartilage Functional Structure
,”
Comput. Methods Biomech. Biomed. Eng.
1025-5842,
5
(
6
), pp.
377
386
.
23.
Chahine
,
N. O.
,
Chen
,
F. H.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
, 2005, “
Direct Measurement of Osmotic Pressure of Glycosaminoglycan Solutions by Membrane Osmometry at Room Temperature
,”
Biophys. J.
0006-3495,
89
(
3
), pp.
1543
1550
.
24.
Lu
,
X. L.
,
Sun
,
D. D.
,
Guo
,
X. E.
,
Chen
,
F. H.
,
Lai
,
W. M.
, and
Mow
,
V. C.
, 2004, “
Indentation Determined Mechanoelectrochemical Properties and Fixed Charge Density of Articular Cartilage
,”
Ann. Biomed. Eng.
0090-6964,
32
(
3
), pp.
370
379
.
25.
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.
0148-0731,
113
(
3
), pp.
245
258
.
26.
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.
0148-0731,
120
(
2
), pp.
169
180
.
27.
Jones
,
R. M.
, 1975,
Mechanics of Composite Material
,
Scripta
,
Washington, DC
.
28.
Ateshian
,
G. A.
,
Chahine
,
N. O.
,
Basalo
,
I. M.
, and
Hung
,
C. T.
, 2004, “
The Correspondence Between Equilibrium Biphasic and Triphasic Material Properties in Mixture Models of Articular Cartilage
,”
J. Biomech.
0021-9290,
37
(
3
), pp.
391
400
.
29.
Wan
,
L. Q.
,
Miller
,
C.
,
Guo
,
X. E.
, and
Mow
,
V. C.
, 2004, “
Fixed Electrical Charges and Mobile Ions Affect the Measuable Mechano-Electrochemical Properties of Charged-Hydrated Biological Tissues: The Articular Cartilage Paradigm
,”
Mech. Chem. Biosyst.
1546-2048,
1
(
1
), pp.
81
99
.
30.
Lu
,
X. L.
,
Miller
,
C.
,
Chen
,
F. H.
,
Guo
,
X. E.
, and
Mow
,
V. C.
, 2007, “
The Generalized Triphasic Correspondence Principle for Simultaneous Determination of the Mechanical Properties and Proteoglycan Content of Articular Cartilage by Indentation
,”
J. Biomech.
0021-9290,
40
(
11
), pp.
2434
2441
.
31.
Sun
,
D. D.
,
Guo
,
X. E.
,
Likhitpanichkul
,
M.
,
Lai
,
W. M.
, and
Mow
,
V. C.
, 2004, “
The Influence of the Fixed Negative Charges on Mechanical and Electrical Behaviors of Articular Cartilage Under Unconfined Compression
,”
ASME J. Biomech. Eng.
0148-0731,
126
(
1
), pp.
6
16
.
32.
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.
0736-0266,
4
(
4
), pp.
379
392
.
33.
Roth
,
V.
, and
Mow
,
V. C.
, 1980, “
The Intrinsic Tensile Behavior of the Matrix of Bovine Articular Cartilage and Its Variation with Age
,”
J. Bone Jt. Surg., Am. Vol.
0021-9355,
62
(
7
), pp.
1102
1117
.
34.
Huang
,
C. Y.
,
Stankiewicz
,
A.
,
Ateshian
,
G. A.
, and
Mow
,
V. C.
, 2005, “
Anisotropy, Inhomogeneity, and Tension-Compression Nonlinearity of Human Glenohumeral Cartilage in Finite Deformation
,”
J. Biomech.
0021-9290,
38
(
4
), pp.
799
809
.
35.
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.
0148-0731,
122
(
6
), pp.
576
586
.
36.
Reddy
,
J. N.
, 2004,
Mechanics of Laminated Composite Plates and Shells: Theory and Analysis
,
CRC
,
Boca Raton
.
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