Research Papers

Cartilage Strain Distributions Are Different Under the Same Load in the Central and Peripheral Tibial Plateau Regions

[+] Author and Article Information
Paul Briant

Stanford University,
496 Lomita Mall,
Durand Building 204 MC: 4040,
Stanford, CA 94305;
149 Commonwealth Drive,
Menlo Park, CA 94025
e-mail: pbriant@exponent.com

Scott Bevill

Colorado Mesa University,
1100 North Avenue,
Grand Junction, CO 81501
e-mail: sbevill@coloradomesa.edu

Thomas Andriacchi

Stanford University,
496 Lomita Mall,
Durand Building 227 MC: 4040,
Stanford, CA 94305
e-mail: tandriac@stanford.edu

1Corresponding author.

Manuscript received May 31, 2015; final manuscript received October 16, 2015; published online November 6, 2015. Assoc. Editor: Tammy L. Haut Donahue.

J Biomech Eng 137(12), 121009 (Nov 06, 2015) (7 pages) Paper No: BIO-15-1271; doi: 10.1115/1.4031849 History: Received May 31, 2015; Revised October 16, 2015

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.

Copyright © 2015 by ASME
Your Session has timed out. Please sign back in to continue.


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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Clark, J. M. , 1990, “ The Organisation of Collagen Fibrils in the Superficial Zones of Articular Cartilage,” J. Anat., 171, pp. 117–130. [PubMed]
Broom, N. D. , 1982, “ Abnormal Softening in Articular Cartilage: Its Relationship to the Collagen Framework,” Arthritis Rheum., 25(10), pp. 1209–1216. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.
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.
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
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.


Grahic Jump Location
Fig. 1

Location of peripheral (dotted) and (dashed) specimen harvest location and freeze fracture plane (long dashed)

Grahic Jump Location
Fig. 2

Deformed matrix orientation traced on SEM image. Deformed cartilage can be viewed under the arrow, which was directly loaded by the indenter. Images across the entire specimen were obtained and combined to form a single panorama using the position data from the SEM.

Grahic Jump Location
Fig. 3

Comparison of estimated initial collagen orientation (solid lines) and deformed collagen orientation (X-marked lines) for (a) peripheral and (b) central region specimens

Grahic Jump Location
Fig. 4

Representative strain distributions calculated from the displacement fields for (a) the peripheral region and (b) the central region

Grahic Jump Location
Fig. 5

Bending deformation pattern in the central region in (a) full thickness view and (b) higher magnificent image near surface

Grahic Jump Location
Fig. 6

Peripheral low-load specimen under load. (a) Full thickness profile and (b) zoom-in at deep/transitional zone interface. No bending occurred during loading.

Grahic Jump Location
Fig. 7

Comparison of strain components under same applied load (a) and same applied nominal strain (b). The central region tended to have higher strains under same load and same nominal strain. The dashed lines on each bar show the average precision error associated with the initial position estimation for each region.



Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In