An automated approach for measuring in situ two-dimensional strain fields was developed and validated for its application to cartilage mechanics. This approach combines video microscopy, optimized digital image correlation (DIC), thin-plate spline smoothing (TPSS) and generalized cross-validation (GCV) techniques to achieve the desired efficiency and accuracy. Results demonstrate that sub-pixel accuracies can be achieved for measuring tissue displacements with this methodology with a measurement uncertainty ranging from 0.25 to 0.30 pixels. The deformational gradients (from which the strains are determined) can be evaluated directly using the optimized DIC, with a measurement uncertainty of 0.0170.032. In actual measurements of strain in cartilage, TPSS and differentiation can be used to achieve a more accurate measurement of the gradients from the displacement data. Using this automated approach, the two-dimensional strain fields inside immature bovine carpometacarpal joint cartilage specimens under unconfined compression were characterized n=21. The depth-dependent apparent elastic modulus and Poisson’s ratio were also determined and found to be smallest at the articular surface and increasing with depth. The apparent Poisson’s ratio is found to decrease with increasing compressive strain, with values as low as 0.01 observed near the articular surface at 25% compression. The variation of the apparent Poisson’s ratio with depth is found to be consistent with a theoretical model of cartilage which accounts for the disparity in its tensile and compressive moduli.

1.
Mow, V. C., and Ateshian, G. A., 1997, “Lubrication and Wear of Diarthrodial Joints,” Basic Orthopaedic Biomechanics, V. C. Mow, and Hayes, W. C., ed., Lippincott-Raven, Philadelphia, pp. 273–315.
2.
Maroudas, A., 1979, “Physicochemical Properties of Articular Cartilage,” Adult Articular Cartilage, M. A. R. Freeman, eds., Pitman Medical, Kent, UK, pp. 215–290.
3.
Stockwell, R. S., 1979, Biology of Cartilage Cells, Cambridge Press, Cambridge.
4.
Aydelotte, M. B., Schumacher, B. L., and Kuettner, K. E., 1992, “Heterogeneity of Articular Chondrocytes,” Articular Cartilage and Osteoarthritis, K. E. Kuettner, eds., Raven Press, New York, pp. 237–249.
5.
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
422
.
6.
Grodzinsky, A. J., Frank, E. H., Kim, Y. J., and Buschmann, M. D., 1996, “The Role of Specific Macromolecules in Cell-Matrix Interactions and in Matrix Function: Physicochemical and Mechanical Mediators of Chondrocyte Biosynthesis,” Extracellular Matrix, W. D. Comper, eds., Harwood Academic Publishers, Melbourne, Australia, pp. 310–334.
7.
Lipshitz
,
H.
,
Etheredge
,
R.
, and
Glimcher
,
M. J.
,
1976
, “
Changes in the Hexosamine Content and Swelling Ratio of Articular Cartilage as Functions of Depth from the Surface
,”
J. Bone Jt. Surg., Am. Vol.
58A
, pp.
1149
1153
.
8.
Maroudas
,
A.
,
Muir
,
H.
, and
Wingham
,
J.
,
1969
, “
The Correlation of Fixed Negative Charge with Glycosaminoglycan Content of Human Articular Cartilage
,”
Biochim. Biophys. Acta
,
177
, pp.
492
500
.
9.
Venn
,
M.
, and
Maroudas
,
A.
,
1977
, “
Chemical Composition of Normal and Osteoarthritic Femoral Head Cartilage
,”
Ann. Rheum. Dis.
,
36
, pp.
121
129
.
10.
Weiss
,
C.
,
Rosenberg
,
L.
, and
Helfet
,
A. J.
,
1968
, “
An Ultrastructural Study of Normal Young Adult Human Articular Cartilage
,”
J. Bone Jt. Surg., Am. Vol.
50A
, pp.
663
674
.
11.
Redler
,
I.
, and
Zimny
,
M. L.
,
1970
, “
Scanning Electron Microscopy of Normal and Abnormal Articular Cartilage and Synovium
,”
J. Bone Jt. Surg., Am. Vol.
52A
, pp.
1395
1407
.
12.
Clark
,
I. C.
,
1971
, “
Articular Cartilage: A Review and Scanning Electron Microscopy Study—I. The Interterritorial Fibrillar Architecture
,”
J. Bone Jt. Surg., Am. Vol.
53B
, pp.
732
750
.
13.
Bullough
,
P. G.
, and
Jagannath
,
A.
,
1983
, “
The Morphology Ofthe Calcification Front in Articular Cartilage
,”
J. Bone Jt. Surg., Am. Vol.
65B
, pp.
72
90
.
14.
Hunziker, E. B., 1992, “Articular Cartilage Structure in Humans and Experimental Animals,” Articular Cartilage and Osteoarthritis, K. E. Kuettner, Schleyerbach, R., Peyron, J. G., and Hascall, V. C., eds., Raven Press, New York, pp. 183–199.
15.
Brocklehurst
,
R.
,
Bayliss
,
M. T.
,
Maroudas
,
A.
,
Coysh
,
H. L.
,
Freeman
,
M. A.
,
Revell
,
P. A.
, and
Ali
,
S. Y.
,
1984
, “
The Composition of Normal and Osteoarthritic Articular Cartilage from Human Knee Joints
,”
J. Bone Jt. Surg., Am. Vol.
66A
, pp.
95
106
.
16.
Mow
,
V. C.
, and
Wang
,
C. C.-B.
,
1999
, “
Some Bioengineering Considerations for Tissue Engineering of Articular Cartilage
,”
Clin. Orthop.
,
367
 Suppl, pp.
S204–S223
S204–S223
.
17.
Mow
,
V. C.
,
Wang
,
C. C.-B.
, and
Hung
,
C. T.
,
1999
, “
The Extracellular Matrix, Interstitial Fluid and Ions as a Mechanical Signal Transducer in Articular Cartilage
,”
Osteoarthritis Cartilage
,
7
, pp.
41
59
.
18.
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
.
19.
Kempson, G. E., 1979, “Mechanical Properties of Articular Cartilage,” Adult Articular Cartilage, M. A. R. Freeman, ed., Pitman Medical, Kent, England, pp. 333–414.
20.
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.
,
62A
, pp.
1102
1117
.
21.
Schinagl
,
R. M.
,
Gurkis
,
D.
,
Chen
,
C. C.
, and
Sah
,
R. L.-Y.
,
1997
, “
Depth-Dependent Confined Compression Modulus of Full-Thickness Bovine Articular Cartilage
,”
J. Orthop. Res.
,
15
, pp.
499
506
.
22.
Schinagl
,
R. M.
,
Ting
,
M. K.
,
Price
,
J. H.
, and
Sah
,
R. L.
,
1996
, “
Video Microscopy to Quantitate the Inhomogeneous Equilibrium Strain within Articular Cartilage During Confined Compression
,”
Ann. Biomed. Eng.
,
24
, pp.
500
512
.
23.
Jurvelin
,
J. S.
,
Buschmann
,
M. D.
, and
Hunziker
,
E. B.
,
1997
, “
Optical and Mechanical Determination of Poisson’s Ratio of Adult Bovine Humeral Articular Cartilage
,”
J. Biomech.
,
30
, pp.
235
241
.
24.
Shin
,
D.
,
Lin
,
J. H.
,
Agrawal
,
C. M.
, and
Athanasiou
,
K. A.
,
1998
, “
Zonal Variations in Micro-Indentation Properties of Articular Artilage
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
23
, p.
903
903
.
25.
Wong
,
M.
,
Jurvelin
,
J. S.
,
Ponticiello
,
M.
,
Tammi
,
M.
,
Kovanen
,
V.
, and
Hunziker
,
E. B.
,
1998
, “
Simultaneous Determination of Poisson’s Ratio and Elastic Modulus of Mature and Immature Cartilage
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
23
, p.
489
489
.
26.
Chang
,
D. G.
,
Lottman
,
L. M.
,
Chen
,
A. C.
,
Schinagl
,
R. M.
,
Albrecht
,
D. R.
,
Pedowitz
,
R. A.
,
Brossmann
,
J.
,
Frank
,
L. R.
, and
Sah
,
R. L.-Y.
,
1999
, “
The Depth-Dependent, Multi-Axial Properties of Aged Human Patellar Cartilage in Tension
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
24
, p.
655
655
.
27.
Elliott
,
D. M.
,
Kydd
,
S. R.
,
Perry
,
C. H.
, and
Setton
,
L. A.
,
1999
, “
Direct Measurement of Poisson’s Ratio of Human Articular Cartilage in Tension
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
24
, p.
649
649
.
28.
Huang
,
C.-Y.
,
Stankiewiecz
,
A.
,
Ateshian
,
G. A.
,
Flatow
,
E. L.
,
Bigliani
,
L. U.
, and
Mow
,
V. C.
,
1999
, “
Anisotropy, Inhomogeneity, and Tension-Compression Nonlinearity of Human Glenohumeral Cartilage in Finite Deformation
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
24
, p.
95
95
.
29.
Narmoneva
,
D. A.
,
Wang
,
J. Y.
, and
Setton
,
L. A.
,
1999
, “
Nonuniform Swelling-Induced Residual Strains in Articular Cartilage
,”
J. Biomech.
,
32
, pp.
401
408
.
30.
Soltz
,
M. A.
,
Palma
,
C.
,
Barsoumian
,
S.
,
Wang
,
C. C.-B.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
,
1999
, “
Multi-Axial Loading of Bovine Articular Cartilage in Unconfined Compression
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
24
, p.
888
888
.
31.
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 Distributions in Articular Cartilage Explants and Cell-Seeded Alginate Disks under Unconfined Compression
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
25
, p.
131
131
.
32.
Wang
,
C. C.-B.
,
Guo
,
X. Z.
,
Sun
,
D.
,
Mow
,
V. C.
,
Ateshian
,
G. A.
, and
Hung
,
C. T.
,
2002
, “
The Functional Environment of Chondrocytes within Cartilage Subject to Compressive Loading: A Theoretical and Experimental Approach
,”
Biorheology
,
39
, pp.
11
25
.
33.
Chen
,
S. S.
, and
Sah
,
R. L.-Y.
,
2001
, “
Contribution of Collagen Network and Fixed Charge to the Confined Compression Modulus of Articular Cartilage
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
26
, p.
426
426
.
34.
Matyas
,
J.
,
Young
,
D.
,
Hulme
,
P.
, and
Duncan
,
N.
,
2001
, “
Zonal Distribution of Articular Cartilage Compressive Strain in a Model of Early Experimental Osteoarthritis
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
26
, p.
128
128
.
35.
Rieppo
,
J.
,
Laasanen
,
M. S.
,
Korhonen
,
R. K.
,
Toyras
,
J.
,
Nieminen
,
M. T.
,
Hirvonen
,
J.
,
Helminen
,
H. J.
, and
Jurvelin
,
J. S.
,
2001
, “
Depth-Dependent Mechanical Properties of Bovine Patellar Cartilage
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
26
, p.
440
440
.
36.
Chu
,
T. C.
,
Ranson
,
W. F.
,
Sutton
,
M. A.
, and
Peters
,
W. H.
,
1985
, “
Applications of Digital Image Correlation Techniques to Experimental Mechanics
,”
Exp. Mech.
,
25
, pp.
232
244
.
37.
Sutton
,
M. A.
,
Cheng
,
M.
,
Petters
III,
W. H.
,
Chao
,
Y. J.
, and
McNeill
,
S. R.
,
1986
, “
Application of an Optimized Digital Correlation Method to Planar Deformation Analysis
,”
Image Vis. Comput.
,
4
, pp.
143
150
.
38.
McNeill
,
S. R.
,
Peters
,
W. H.
, and
Sutton
,
M. A.
,
1987
, “
Estimation of Stress Intensity Factor by Digital Image Correlation
,”
Eng. Fract. Mech.
,
28
, pp.
101
112
.
39.
Sutton
,
M. A.
, and
Chao
,
Y. J.
,
1988
, “
Measurement of Strains in a Paper Tensile Specimen Using Computer Vision Digital Image Correlation
,”
Tappi J.
,
70
, pp.
153
156
.
40.
Bruck
,
H. A.
,
McNeill
,
S. R.
,
Sutton
,
M. A.
, and
Petters
III,
W. H.
,
1989
, “
Digital Image Correlation Using Newton-Raphson Method of Partial Differential Correction
,”
Exp. Mech.
,
46
, pp.
261
267
.
41.
Russell
,
S. S.
, and
Sutton
,
M. A.
,
1989
, “
Strain-Field Analysis Acquired Through Correlation of X-Ray Radiographs of a Fiber-Reinforced Composite Laminate
,”
Exp. Mech.
,
46
, pp.
237
240
.
42.
Bay
,
B. K.
,
1995
, “
Texture Correlation: A Method for the Measurement of Detailed Strain Distributions within Trabecular Bone
,”
J. Orthop. Res.
,
13
, pp.
258
267
.
43.
Gonzalez
,
J.
, and
Knauss
,
W. G.
,
1998
, “
Strain Inhomogeneity and Discontinuous Crack Growth in a Particulate Composite
,”
J. Mech. Phys. Solids
,
46
, pp.
1981
1995
.
44.
Bastawros
,
A.-F.
,
Bart-Smith
,
H.
, and
Evans
,
A. G.
,
2000
, “
Experimental Analysis of Deformation Mechanisms in a Closed-Cell Aluminum Alloy Foam
,”
J. Mech. Phys. Solids
,
48
, pp.
301
322
.
45.
Bey
,
M. J.
, and
Soslowsky
,
L. J.
,
2000
, “
Two-Dimensional Intratendinous Strains of the Human Rotator Cuff: Technique and Preliminary Results
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
25
, p.
405
405
.
46.
Soltz
,
M. A.
, and
Ateshian
,
G. A.
,
2000
, “
A Conewise Linear Elasticity Mixture Model for the Analysis of Tension-Compression Nonlinearity in Articular Cartilage
,”
J. Biomech. Eng.
,
122
, pp.
576
586
.
47.
Soulhat
,
J.
,
Buschmann
,
M. D.
, and
Shirazi-Adl
,
A.
,
1999
, “
A Fibril-Network-Reinforced Biphasic Model of Cartilage in Unconfined Compression
,”
J. Biomech. Eng.
,
121
, pp.
340
347
.
48.
Fung, Y. C., 1965, Foundations of Solid Mechanics, Prentice Hall Inc., Englewood Cliffs.
49.
Lancaster, P., and Salkauskas, K., 1986, Curve and Space Fitting: An Introduction, Academic Press, London.
50.
Kelley, C. T., 1999, Iterative Methods for Optimization, Society for Industrial and Applied Mathematics, Philadelphia.
51.
Reinsch
,
C. H.
,
1967
, “
Smoothing by Spline Functions
,”
Numerische Mathematik
,
10
, pp.
177
183
.
52.
Wahba
,
G.
,
1975
, “
Smoothing Noisy Data with Spline Functions
,”
Numerische Mathematik
,
24
, pp.
383
393
.
53.
Woltring
,
H. J.
,
1985
, “
An Optimal Smoothing and Derivative Estimation from Noisy Displacement Data in Biomechanics
,”
Human Movement Science
,
4
, pp.
229
245
.
54.
Wahba, G., 1986, “Multivariate Thin Plate Spline Smoothing with Positivity and Other Linear Inequality Constraints,” Statistical Image Processing and Graphics, E. J. Wegman, and DePriest, D. J., eds., Dekker, New York, pp. 275–289.
55.
Dohrmann
,
C. R.
,
Busby
,
H. R.
, and
Trujillo
,
D. M.
,
1988
, “
Smoothing Noisy Data Using Dynamic Programming and Generalized Cross-Validation
,”
J. Biomech. Eng.
,
110
, pp.
37
41
.
56.
Ateshian
,
G. A.
,
1993
, “
A B-Spline Least-Squares Surface-Fitting Method for Articular Surface of Diarthrodial Joints
,”
J. Biomech. Eng.
,
115
, pp.
366
373
.
57.
Bates
,
D. M.
,
Lindstrom
,
M. J.
,
Wahba
,
G.
, and
Yandell
,
B. S.
,
1987
, “
GCVpack-Routines for Generalized Cross Validation
,”
Communication of Statistics
,
16
, pp.
263
297
.
58.
Craven
,
P.
, and
Wahba
,
G.
,
1979
, “
Smoothing Noisy Data with Spline Functions
,”
Numerische Mathematik
,
31
, pp.
377
403
.
59.
Duchon, J., 1976, “Splines Minimizing Rotation-Invariant Semi-Norms in Sobolev Spaces,” Constructive Theory of Functions of Several Variables, W. Schempp, and Zeller, K., eds., Springer-Verlag, New York.
60.
Hill
,
D. L.
,
Batchelor
,
P. G.
,
Holden
,
M.
, and
Hawkes
,
D. J.
,
2001
, “
Medical Image Registration
,”
Phys. Med. Biol.
,
46
, pp.
1
45
.
61.
Wang
,
C. C.-B.
, and
Mow
,
V. C.
,
1998
, “
Inhomogeneity of Aggregate Modulus Affects Cartilage Compressive Stress-Relaxation Behavior
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
23
, p.
481
481
.
62.
Sun
,
D. N.
,
Gu
,
W. Y.
,
Guo
,
X. E.
,
Lai
,
W. M.
, and
Mow
,
V. C.
,
1998
, “
The Influence of Inhomogeneous Fixed Charge Density of Cartilage Mechano-Electrochemical Behaviors
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
23
, p.
484
484
.
63.
Wang
,
C. C.-B.
,
Hung
,
C. T.
, and
Mow
,
V. C.
,
2000
, “
Analysis of the Effects of Depth-Dependent Aggregate Modulus on Articular Cartilage Stress-Relaxation Behavior in Compression
,”
J. Biomech.
,
34
, pp.
75
84
.
64.
Sutton
,
M. A.
,
Babai
,
M.
,
Jang
,
J.
, and
McNeill
,
S. R.
,
1988
, “
Effects of Subpixel Image Restoration on Digital Correlation Error Estimates
,”
Opt. Eng.
,
27
, pp.
870
877
.
65.
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 Concentrations, Weight Bearing and Fibrillation on the Tensile Modulus
,”
Trans. Annu. Meet. — Orthop. Res. Soc.
,
4
, pp.
379
392
.
66.
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
.
67.
Athanasiou
,
K. A.
,
Rosenwasser
,
M. P.
,
Buckwalter
,
J. A.
,
Malinin
,
T. I.
, and
Mow
,
V. C.
,
1991
, “
Interspecies Comparisons of in Situ Intrinsic Mechanical Properties of Distal Femoral Cartilage
,”
J. Orthop. Res.
,
9
, pp.
330
340
.
68.
Ateshian
,
G. A.
,
Wang
,
H.
, and
Lai
,
W. M.
,
1998
, “
The Role of Interstitial Fluid Pressurization and Surface Porosities on the Boundary Friction of Articular Cartilage
,”
J. Tribol.
,
120
, pp.
241
248
.
69.
Bursac
,
P. M.
,
Obitz
,
T. W.
,
Eisenberg
,
S. R.
, and
Stamenovic
,
D.
,
1999
, “
Confined and Unconfined Stress Relaxation of Cartilage: Appropriateness of a Transversely Isotropic Analysis
,”
J. Biomech.
,
32
, pp.
1125
1130
.
70.
Wang, C. C.-B., Chahine, N. O., Kelly, T. N., Lai, W. M., Hung, C. T., and Ateshian, G. A., 2001, “The Strain-Softening of Bovine Articular Cartilage under Infinitesimal Deformation in Unconfined Compression,” Advance of Bioengineering, ASME BED, 51, Abstract# 23061.
71.
Bursac
,
P. M.
,
McGrath
,
C. V.
,
Eisenberg
,
S. R.
, and
Stamenovic
,
D.
,
2000
, “
A Microstructural Model of Elastostatic Properties of Articular Cartilage in Confined Compression
,”
J. Biomech. Eng.
,
122
, pp.
347
353
.
72.
Wang, C. C.-B., Chahine, N. O., Kelly, T. N., Valhmu, W. B., Hung, C. T., and Ateshian, G. A., 2001, “Optical Determination of Anisotropic Material Properties of Bovine Articular Cartilage in Compression,” Advance of Bioengineering, ASME BED, 50, pp. 729–730.
You do not currently have access to this content.