There is increasing evidence that the regional spatial variations in the biological and mechanical properties of articular cartilage are an important consideration in the pathogenesis of knee osteoarthritis (OA) following kinematic changes at the knee due to joint destabilizing events (such as an anterior cruciate ligament (ACL) injury). Thus, given the sensitivity of chondrocytes to the mechanical environment, understanding the internal mechanical strains in knee articular cartilage under macroscopic loads is an important element in understanding knee OA. The purpose of this study was to test the hypothesis that cartilage from the central and peripheral regions of the tibial plateau has different internal strain distributions under the same applied load. The internal matrix strain distribution for each specimen was measured on osteochondral blocks from the tibial plateau of mature ovine stifle joints. Each specimen was loaded cyclically for 20 min, after which the specimen was cryofixed in its deformed position and freeze fractured. The internal matrix was viewed in a scanning electron microscope (SEM) and internal strains were measured by quantifying the deformation of the collagen fiber network. The peak surface tensile strain, maximum principal strain, and maximum shear strain were compared between the regions. The results demonstrated significantly different internal mechanical strain distributions between the central and peripheral regions of tibial plateau articular cartilage under both the same applied load and same applied nominal strain. These differences in the above strain measures were due to differences in the deformation patterns of the collagen network between the central and peripheral regions. Taken together with previous studies demonstrating differences in the biochemical response of chondrocytes from the central and peripheral regions of the tibial plateau to mechanical load, the differences in collagen network deformation observed in this study help to provide a fundamental basis for understanding the association between altered knee joint kinematics and premature knee OA.

References

References
1.
Quinn
,
T. M.
,
Hunziker
,
E. B.
, and
Häuselmann
,
H. J.
,
2005
, “
Variation of Cell and Matrix Morphologies in Articular Cartilage Among Locations in the Adult Human Knee
,”
Osteoarthritis Cartilage
,
13
(
8
), pp.
672
678
.
2.
Buschmann
,
M. D.
,
Gluzband
,
Y. A.
,
Grodzinsky
,
A. J.
, and
Hunziker
,
E. B.
,
1995
, “
Mechanical Compression Modulates Matrix Biosynthesis in Chondrocyte/Agarose Culture
,”
J. Cell Sci.
,
108
(
4
), pp.
1497
1508
.
3.
Vanderploeg
,
E. J.
,
Imler
,
S. M.
,
Brodkin
,
K. R.
,
Garcia
,
A. J.
, and
Levenston
,
M. E.
,
2004
, “
Oscillatory Tension Differentially Modulates Matrix Metabolism and Cytoskeletal Organization in Chondrocytes and Fibrochondrocytes
,”
J. Biomech.
,
37
(
12
), pp.
1941
1952
.
4.
Jin
,
M.
,
Frank
,
E. H.
,
Quinn
,
T. M.
,
Hunziker
,
E. B.
, and
Grodzinsky
,
A. J.
,
2001
, “
Tissue Shear Deformation Stimulates Proteoglycan and Protein Biosynthesis in Bovine Cartilage Explants
,”
Arch. Biochem. Biophys.
,
395
(
1
), pp.
41
48
.
5.
Quinn
,
T. M.
,
Grodzinsky
,
A. J.
,
Buschmann
,
M. D.
,
Kim
,
Y. J.
, and
Hunziker
,
E. B.
,
1998
, “
Mechanical Compression Alters Proteoglycan Deposition and Matrix Deformation Around Individual Cells in Cartilage Explants
,”
J. Cell Sci.
,
111
(
5
), pp.
573
583
.
6.
Smith
,
R. L.
,
Trindade
,
M. C. D.
,
Ikenoue
,
T.
,
Mohtai
,
M.
,
Das
,
P.
,
Carter
,
D. R.
,
Goodman
,
S. B.
, and
Schurman
,
D. J.
,
2000
, “
Effects of Shear Stress on Articular Chondrocyte Metabolism
,”
Biorheology
,
37
, pp.
95
107
.
7.
Bevill
,
S. L.
,
Briant
,
P. L.
, and
Levenston
,
M. E.
,
2009
, “
Central and Peripheral Region Tibial Plateau Chondrocytes Respond Differently to In Vitro Dynamic Compression
,”
Osteoarthritis Cartilage
,
17
(
8
), pp.
980
987
.
8.
Deneweth
,
J. M.
,
Newman
,
K. E.
,
Sylvia
,
S. M.
,
McLean
,
S. G.
, and
Arruda
,
E. M.
,
2013
, “
Heterogeneity of Tibial Plateau Cartilage in Response to a Physiological Compressive Strain Rate
,”
J. Orthop. Res.
,
31
(
3
), pp.
370
375
.
9.
Koo
,
S.
,
Rylander
,
J. H.
, and
Andriacchi
,
T. P.
,
2011
, “
Knee Joint Kinematics During Walking Influences the Spatial Cartilage Thickness Distribution in the Knee
,”
J. Biomech.
,
44
(
7
), pp.
1405
1409
.
10.
Scanlan
,
S. F.
,
Favre
,
J.
, and
Andriacchi
,
T. P.
,
2013
, “
The Relationship Between Peak Knee Extension at Heel-Strike of Walking and the Location of Thickest Femoral Cartilage in ACL Reconstructed and Healthy Contralateral Knees
,”
J. Biomech.
,
46
(
5
), pp.
849
854
.
11.
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
(
3
), pp.
216
225
.
12.
Andriacchi
,
T. P.
,
Mündermann
,
A.
,
Smith
,
R. L.
,
Alexander
,
E. J.
,
Dyrby
,
C. O.
, and
Koo
,
S.
,
2004
, “
A Framework for the In Vivo Pathomechanics of Osteoarthritis at the Knee
,”
Ann. Biomed. Eng.
,
32
(
3
), pp.
447
457
.
13.
Andriacchi
,
T. P.
,
Favre
,
J.
,
Erhart-Hledik
,
J. C.
, and
Chu
,
C. R.
,
2015
, “
A Systems View of Risk Factors for Knee Osteoarthritis Reveals Insights Into the Pathogenesis of the Disease
,”
Ann. Biomed. Eng.
,
43
(
2
), pp.
376
387
.
14.
Wu
,
J. Z.
,
Herzog
,
W.
, and
Epstein
,
M.
,
2000
, “
Joint Contact Mechanics in the Early Stages of Osteoarthritis
,”
Med. Eng. Phys.
,
22
(
1
), pp.
1
12
.
15.
Bullough
,
P. G.
,
Yawitz
,
P. S.
,
Tafra
,
L.
, and
Boskey
,
A. L.
,
1985
, “
Topographical Variations in the Morphology and Biochemistry of Adult Canine Tibial Plateau Articular Cartilage
,”
J. Orthop. Res.
,
3
(
1
), pp.
1
16
.
16.
Clark
,
J. M.
,
1990
, “
The Organisation of Collagen Fibrils in the Superficial Zones of Articular Cartilage
,”
J. Anat.
,
171
, pp.
117
130
.
17.
Broom
,
N. D.
,
1982
, “
Abnormal Softening in Articular Cartilage: Its Relationship to the Collagen Framework
,”
Arthritis Rheum.
,
25
(
10
), pp.
1209
1216
.
18.
Appleyard
,
R. C.
,
Burkhardt
,
D.
,
Ghosh
,
P.
,
Read
,
R.
,
Cake
,
M.
,
Swain
,
M. V.
, and
Murrell
,
G. A.
,
2003
, “
Topographical Analysis of the Structural, Biochemical and Dynamic Biomechanical Properties of Cartilage in an Ovine Model of Osteoarthritis
,”
Osteoarthritis Cartilage
,
11
(
1
), pp.
65
77
.
19.
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.
,
9
(
2
), pp.
246
257
.
20.
Clark
,
J. M.
,
Norman
,
A.
, and
Notzli
,
H.
,
1997
, “
Postnatal Development of the Collagen Matrix in Rabbit Tibial Plateau Articular Cartilage
,”
J. Anat.
,
191
(
2
), pp.
215
221
.
21.
Dunham
,
J.
,
Shackleton
,
D. R.
,
Billingham
,
M. E.
,
Bitensky
,
L.
,
Chayen
,
J.
, and
Muir
,
I. H.
,
1988
, “
A Reappraisal of the Structure of Normal Canine Articular Cartilage
,”
J. Anat.
,
157
, pp.
89
99
.
22.
Arokoski
,
J. P.
,
Hyttinen
,
M. M.
,
Lapveteläinen
,
T.
,
Takács
,
P.
,
Kosztáczky
,
B.
,
Módis
,
L.
,
Kovanen
,
V.
, and
Helminen
,
H.
,
1996
, “
Decreased Birefringence of the Superficial Zone Collagen Network in the Canine Knee (Stifle) Articular Cartilage After Long Distance Running Training, Detected by Quantitative Polarised Light Microscopy
,”
Ann. Rheum. Dis.
,
55
(
4
), pp.
253
264
.
23.
LeRoux
,
M. A.
,
Arokoski
,
J.
,
Vail
,
T. P.
,
Guilak
,
F.
,
Hyttinen
,
M. M.
,
Kiviranta
,
I.
, and
Setton
,
L. A.
,
2000
, “
Simultaneous Changes in the Mechanical Properties, Quantitative Collagen Organization, and Proteoglycan Concentration of Articular Cartilage Following Canine Meniscectomy
,”
J. Orthop. Res.
,
18
(
3
), pp.
383
392
.
24.
Song
,
Y.
,
Greve
,
J. M.
,
Carter
,
D. R.
,
Koo
,
S.
, and
Giori
,
N. J.
,
2006
, “
Articular Cartilage MR Imaging and Thickness Mapping of a Loaded Knee Joint Before and After Meniscectomy
,”
Osteoarthritis Cartilage
,
14
(
8
), pp.
728
737
.
25.
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
(
4
), pp.
500
512
.
26.
Wang
,
C. C.
,
Deng
,
J. M.
,
Ateshian
,
G. A.
, and
Hung
,
C. T.
,
2002
, “
An Automated Approach for Direct Measurement of Two-Dimensional Strain Distributions Within Articular Cartilage Under Unconfined Compression
,”
ASME J. Biomech. Eng.
,
124
(
5
), pp.
557
567
.
27.
Silverberg
,
J. L.
,
Dillavou
,
S.
,
Bonassar
,
L.
, and
Cohen
,
I.
,
2013
, “
Anatomic Variation of Depth-Dependent Mechanical Properties in Neonatal Bovine Articular Cartilage
,”
J. Orthop. Res.
,
31
(
5
), pp.
686
691
.
28.
Buckley
,
M. R.
,
Bonassar
,
L. J.
, and
Cohen
,
I.
,
2013
, “
Localization of Viscous Behavior and Shear Energy Dissipation in Articular Cartilage Under Dynamic Shear Loading
,”
ASME J. Biomech. Eng.
,
135
(
3
), p.
031002
.
29.
Wong
,
B. L.
, and
Sah
,
R. L.
,
2010
, “
Effect of Focal Articular Defect on Cartilage Deformation During Patello-Femoral Articulation
,”
J. Orthop. Res.
,
28
(
12
), pp.
1554
1561
.
30.
Motavalli
,
M.
,
Akkus
,
O.
, and
Mansour
,
J. M.
,
2014
, “
Depth-Dependent Shear Behavior of Bovine Articular Cartilage: Relationship to Structure
,”
J. Anat.
,
225
(
5
), pp.
519
526
.
31.
Kobayashi
,
S.
,
Yonekubo
,
S.
, and
Kurogouchi
,
Y.
,
1995
, “
Cryoscanning Electron Microscopic Study of the Surface Amorphous Layer of Articular Cartilage
,”
J. Anat.
,
187
(
2
), pp.
429
444
.
32.
Thambyah
,
A.
, and
Broom
,
N.
,
2006
, “
Micro-Anatomical Response of Cartilage-on-Bone to Compression: Mechanisms of Deformation Within and Beyond the Directly Loaded Matrix
,”
J. Anat.
,
209
(
5
), pp.
611
622
.
33.
Clark
,
J. M.
,
Norman
,
A. G.
,
Kääb
,
M. J.
, and
Nötzli
,
H. P.
,
1999
, “
The Surface Contour of Articular Cartilage in an Intact, Loaded Joint
,”
J. Anat.
,
195
(
1
), pp.
45
56
.
34.
Kääb
,
M. J.
,
Ito
,
K.
,
Rahn
,
B.
,
Clark
,
J. M.
, and
Nötzli
,
H. P.
,
2000
, “
Effect of Mechanical Load on Articular Cartilage Collagen Structure: A Scanning Electron-Microscopic Study
,”
Cells Tissues Organs
,
167
, pp.
106
120
.
35.
Kääb
,
M. J.
,
Richards
,
R. G.
,
Ito
,
K.
,
ap Gwynn
,
I.
, and
Nötzli
,
H. P.
,
2003
, “
Deformation of Chondrocytes in Articular Cartilage Under Compressive Load: A Morphological Study
,”
Cells Tissues Organs
,
175
, pp.
133
139
.
36.
Nötzli
,
H.
, and
Clark
,
J.
,
1997
, “
Deformation of Loaded Articular Cartilage Prepared for Scanning Electron Microscopy With Rapid Freezing and Freeze-Substitution Fixation
,”
J. Orthop. Res.
,
15
(
1
), pp.
76
86
.
37.
Bevill
,
S. L.
,
Thambyah
,
A.
, and
Broom
,
N. D.
,
2010
, “
New Insights Into the Role of the Superficial Tangential Zone in Influencing the Microstructural Response of Articular Cartilage to Compression
,”
Osteoarthritis Cartilage
,
18
(
10
), pp.
1310
1318
.
38.
Humphreys
,
W.
,
Spurlock
,
B.
, and
Johnson
,
J.
,
1974
, “
Critical Point Drying of Ethanol-Infiltrated Cryofractured Biological Specimens for Scanning Electron Microscopy
,”
Scanning Microsc.
,
7
, pp.
275
282
.
39.
Beaupre
,
G. S.
,
Stevens
,
S. S.
, and
Carter
,
D. R.
,
2000
, “
Mechanobiology in the Development, Maintenance, and Degeneration of Articular Cartilage
,”
J. Rehab. Res. Dev.
,
37
(
2
), pp.
145
151
.
40.
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
(
3
), pp.
330
340
.
41.
Vanderploeg
,
E. J.
,
Imler
,
S. M.
,
Brodkin
,
K. R.
,
Garcia
,
A. J.
, and
Levenston
,
M. E.
,
2004
, “
Oscillatory Tension Differentially Modulates Matrix Metabolism and Cytoskeletal Organization in Chondrocytes and Fibrochondrocytes
,”
J. Biomech.
,
37
(
12
), pp.
1941
1952
.
42.
Lee
,
M. S.
,
Trindade
,
M. C.
,
Ikenoue
,
T.
,
Goodman
,
S. B.
,
Schurman
,
D. J.
, and
Smith
,
R. L.
,
2003
, “
Regulation of Nitric Oxide and bcl-2 Expression by Shear Stress in Human Osteoarthritic Chondrocytes In Vitro
,”
J. Cell. Biochem.
,
90
(
1
), pp.
80
86
.
43.
Kääb
,
M. J.
,
Ito
,
K.
,
Clark
,
J. M.
, and
Nötzli
,
H. P.
,
1998
, “
Deformation of Articular Cartilage Collagen Structure Under Static and Cyclic Loading
,”
J. Orthop. Res.
,
16
(
6
), pp.
743
751
.
44.
Buckwalter
,
J. A.
, and
Brown
,
T. D.
,
2004
, “
Joint Injury, Repair, and Remodeling: Roles in Post-Traumatic Osteoarthritis
,”
Clin. Orthop. Relat. Res.
,
423
, pp.
7
16
.
45.
Akizuki
,
S.
,
Mow
, V
. C.
,
Müller
,
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
(
4
), pp.
379
392
.
46.
Kääb
,
M.
,
Richards
,
R.
,
Walther
,
P.
,
ap Gwynn
,
I.
, and
Nötzli
,
H.
,
1999
, “
A Comparison of Four Preparation Methods for the Morphological Study of Articular Cartilage for Scanning Electron Microscopy
,”
Scanning Microsc.
,
13
, pp.
61
69
.
You do not currently have access to this content.