0
Technical Brief

Cartilage Nominal Strain Correlates With Shear Modulus and Glycosaminoglycans Content in Meniscectomized Joints

[+] Author and Article Information
Yongnam Song

Department of Mechanical Engineering,
Korea University,
Seoul 136-713, Korea;
Bone and Joint Center,
VA Palo Alto Healthcare System,
Palo Alto, CA 94304
e-mail: kurtbain@korea.ac.kr

Dennis R. Carter

Bone and Joint Center,
VA Palo Alto Healthcare System,
Palo Alto, CA 94304;
Department of Mechanical Engineering,
Stanford University,
Stanford, CA 94305

Nicholas J. Giori

Bone and Joint Center,
VA Palo Alto Healthcare System,
Palo Alto, CA 94304;
Department of Orthopedic Surgery,
Stanford University,
Stanford, CA 94305

1Corresponding author.

2Present address: Innovation Hall, Room 306, Anam-dong, Seongbuk-gu, Seoul 136-713, Korea.

Manuscript received November 22, 2012; final manuscript received March 10, 2014; accepted manuscript posted March 26, 2014; published online May 6, 2014. Assoc. Editor: James C. Iatridis.

J Biomech Eng 136(6), 064503 (May 06, 2014) (6 pages) Paper No: BIO-12-1577; doi: 10.1115/1.4027298 History: Received November 22, 2012; Revised March 10, 2014; Accepted March 26, 2014

Postmeniscectomy osteoarthritis (OA) is hypothesized to be the consequence of abnormal mechanical conditions, but the relationship between postsurgical alterations in articular cartilage strain and in vivo biomechanical/biochemical changes in articular cartilage is unclear. We hypothesized that spatial variations in cartilage nominal strain (percentile thickness change) would correlate with previously reported in vivo articular cartilage property changes following meniscectomy. Cadevaric sheep knees were loaded in cyclic compression which was previously developed to mimic normal sheep gait, while a 4.7 T magnetic resonance imaging (MRI) imaged the whole joint. 3D cartilage strain maps were compared with in vivo sheep studies that described postmeniscectomy changes in shear modulus, phase lag, proteoglycan content and collagen organization/content in the articular cartilage. The area of articular cartilage experiencing high (overloaded) and low (underloaded) strain was significantly increased in the meniscectomized tibial compartment by 10% and 25%, respectively, while no significant changes were found in the nonmeniscectomized compartment. The overloaded and underloaded regions of articular cartilage in our in vitro specimens correlated with regions of in vivo shear modulus reduction. Glycosaminoglycans (GAG) content only increased at the underloaded articular cartilage but decreased at the overloaded articular cartilage. No significant correlation was found in phase lag and collagen organization/content changes with the strain variation. Comparisons between postsurgical nominal strain and in vivo cartilage property changes suggest that both overloading and underloading after meniscectomy may directly damage the cartilage matrix stiffness (shear modulus). Disruption of superficial cartilage by overloading might be responsible for the proteoglycan (GAG) loss in the early stage of postmeniscectomy OA.

FIGURES IN THIS ARTICLE
<>
Copyright © 2014 by ASME
Your Session has timed out. Please sign back in to continue.

References

Roos, H., Lauren, M., Adalberth, T., Roos, E. M., Jonsson, K., and Lohmander, L. S., 1998, “Knee Osteoarthritis After Meniscectomy: Prevalence of Radiographic Changes After Twenty-One Years, Compared With Matched Controls,” Arthritis Rheum., 41(4), pp. 687–693. [CrossRef] [PubMed]
Jorgensen, U., Sonne-Holm, S., Lauridsen, F., and Rosenklint, A., 1987, “Long-Term Follow-Up of Meniscectomy in Athletes. A Prospective Longitudinal Study,” J. Bone Jt. Surg. Br., 69(1), pp. 80–83.
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]
Oakley, S. P., Lassere, M. N., Portek, I., Szomor, Z., Ghosh, P., Kirkham, B. W., Murrell, G. A., Wulf, S., and Appleyard, R. C., 2004, “Biomechanical, Histologic and Macroscopic Assessment of Articular Cartilage in a Sheep Model of Osteoarthritis,” Osteoarthritis Cartilage, 12(8), pp. 667–679. [CrossRef] [PubMed]
Chatain, F., Adeleine, P., Chambat, P., Neyret, P., and Societe Francaise, D. A., 2003, “A Comparative Study of Medial Versus Lateral Arthroscopic Partial Meniscectomy on Stable Knees: 10-Year Minimum Follow-Up,” Arthroscopy, 19(8), pp. 842–849. [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. 383–92. [CrossRef] [PubMed]
Borel, M., Pastoureau, P., Papon, J., Madelmont, J. C., Moins, N., Maublant, J., and Miot-Noirault, E., 2009, “Longitudinal Profiling of Articular Cartilage Degradation in Osteoarthritis by High-Resolution Magic Angle Spinning 1h Nmr Spectroscopy: Experimental Study in the Meniscectomized Guinea Pig Model,” J. Proteome Res., 8(5), pp. 2594–2600. [CrossRef] [PubMed]
Mckinley, T. O., English, D. K., and Bay, B. K., 2003, “Trabecular Bone Strain Changes Resulting from Partial and Complete Meniscectomy,” Clin. Orthop. Relat. Res., 407, pp. 259–267. [CrossRef] [PubMed]
Wilson, W., Van Rietbergen, B., Van Donkelaar, C. C., and Huiskes, R., 2003, “Pathways of Load-Induced Cartilage Damage Causing Cartilage Degeneration in the Knee After Meniscectomy,” J. Biomech., 36(6), pp. 845–851. [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]
Song, Y., Greve, J. M., Carter, D. R., and Giori, N. J., 2008, “Meniscectomy Alters the Dynamic Deformational Behavior and Cumulative Strain of Tibial Articular Cartilage in Knee Joints Subjected to Cyclic Loads,” Osteoarthritis Cartilage, 16(12), pp. 1545–1554. [CrossRef] [PubMed]
Burkhardt, D., Hwa, S. Y., and Ghosh, P., 2001, “A Novel Microassay for the Quantitation of the Sulfated Glycosaminoglycan Content of Histological Sections: Its Application to Determine the Effects of Diacerhein on Cartilage in an Ovine Model of Osteoarthritis,” Osteoarthritis Cartilage, 9(3), pp. 238–247. [CrossRef] [PubMed]
Appleyard, R. C., Ghosh, P., and Swain, M. V., 1999, “Biomechanical, Histological and Immunohistological Studies of Patellar Cartilage in an Ovine Model of Osteoarthritis Induced by Lateral Meniscectomy,” Osteoarthritis Cartilage, 7(3), pp. 281–294. [CrossRef] [PubMed]
Hoch, D. H., Grodzinsky, A. J., Koob, T. J., Albert, M. L., and Eyre, D. R., 1983, “Early Changes in Material Properties of Rabbit Articular Cartilage After Meniscectomy,” J. Orthop. Res., 1(1), pp. 4–12. [CrossRef] [PubMed]
Chen, A. C., Klisch, S. M., Bae, W. C., Temple, M. M., Mcgowan, K. B., Gratz, K. R., Schumacher, B. L., and Sah, R. L., 2004, “Mechanical Characterization of Native and Tissue-Engineered Cartilage,” Methods Mol. Med., 101, pp. 157–190. [PubMed]
Appleyard, R., 2005, private communication.
Taylor, W. R., Ehrig, R. M., Heller, M. O., Schell, H., Seebeck, P., and Duda, G. N., 2006, “Tibio-Femoral Joint Contact Forces in Sheep,” J. Biomech., 39(5), pp. 791–798. [CrossRef] [PubMed]
Eckstein, F., Lemberger, B., Stammberger, T., Englmeier, K. H., and Reiser, M., 2000, “Patellar Cartilage Deformation In Vivo After Static Versus Dynamic Loading,” J. Biomech., 33(7), pp. 819–825. [CrossRef] [PubMed]
Herberhold, C., Faber, S., Stammberger, T., Steinlechner, M., Putz, R., Englmeier, K. H., Reiser, M., and Eckstein, F., 1999, “In Situ Measurement of Articular Cartilage Deformation in Intact Femoropatellar Joints Under Static Loading,” J. Biomech., 32(12), pp. 1287–1295. [CrossRef] [PubMed]
Mosher, T. J., Smith, H. E., Collins, C., Liu, Y., Hancy, J., Dardzinski, B. J., and Smith, M. B., 2005, “Change in Knee Cartilage T2 at Mr Imaging After Running: A Feasibility Study,” Radiology, 234(1), pp. 245–249. [CrossRef] [PubMed]
Andriacchi, T. P., 1994, “Dynamics of Knee Malalignment,” Orthop. Clin. North Am., 25(3), pp. 395–403. [PubMed]
Mundermann, A., Dyrby, C. O., Hurwitz, D. E., Sharma, L., and Andriacchi, T. P., 2004, “Potential Strategies to Reduce Medial Compartment Loading in Patients With Knee Osteoarthritis of Varying Severity: Reduced Walking Speed,” Arthritis Rheum., 50(4), pp. 1172–1178. [CrossRef] [PubMed]
Hurwitz, D. E., Ryals, A. B., Case, J. P., Block, J. A., and Andriacchi, T. P., 2002, “The Knee Adduction Moment During Gait in Subjects With Knee Osteoarthritis is More Closely Correlated With Static Alignment Than Radiographic Disease Severity, Toe Out Angle and Pain,” J. Orthop. Res., 20(1), pp. 101–107. [CrossRef] [PubMed]
Hurwitz, D. E., Ryals, A. R., Block, J. A., Sharma, L., Schnitzer, T. J., and Andriacchi, T. P., 2000, “Knee Pain and Joint Loading in Subjects With Osteoarthritis of the Knee,” J. Orthop. Res., 18(4), pp. 572–579. [CrossRef] [PubMed]
Hurwitz, D. E., Sumner, D. R., Andriacchi, T. P., and Sugar, D. A., 1998, “Dynamic Knee Loads During Gait Predict Proximal Tibial Bone Distribution,” J. Biomech., 31(5), pp. 423–430. [CrossRef] [PubMed]
Caligaris, M., Canal, C. E., Ahmad, C. S., Gardner, T. R., and Ateshian, G. A., 2009, “Investigation of the Frictional Response of Osteoarthritic Human Tibiofemoral Joints and the Potential Beneficial Tribological Effect of Healthy Synovial Fluid,” Osteoarthritis Cartilage, 17(10), pp. 1327–1332. [CrossRef] [PubMed]
Gleghorn, J. P., Jones, A. R., Flannery, C. R., and Bonassar, L. J., 2009, “Boundary Mode Lubrication of Articular Cartilage by Recombinant Human Lubricin,” J. Orthop. Res., 27(6), pp. 771–777. [CrossRef] [PubMed]
Schmidt, T. A., and Sah, R. L., 2007, “Effect of Synovial Fluid on Boundary Lubrication of Articular Cartilage,” Osteoarthritis Cartilage, 15(1), pp. 35–47. [CrossRef] [PubMed]
Wong, B. L., Bae, W. C., Gratz, K. R., and Sah, R. L., 2008, “Shear Deformation Kinematics During Cartilage Articulation: Effect of Lubrication, Degeneration, and Stress Relaxation,” Mol. Cell Biomech., 5(3), pp. 197–206. [PubMed]

Figures

Grahic Jump Location
Fig. 1

The front view schematic of the joint loading apparatus and a real picture of the device are shown

Grahic Jump Location
Fig. 2

Typical MR image of (a) articular cartilage deformation in an intact knee and (b) after meniscectomy at steady-state are shown (a black air bubble was present in the left side of the meniscectomized knee image between femur and tibia)

Grahic Jump Location
Fig. 3

Square grid patterns were applied to the medial (3 × 4 grid) and lateral (3 × 3 grid) tibial articular cartilage models. The medial side was divided in four columns and lateral side was divided in three columns similar to the grid pattern used in a previous in vivo sheep study. (Mo: Meniscectomy outer, Mmo: Meniscectomy middle-outer, Mmi: Meniscectomy middle-inner, Mi: Meniscectomy inner, Io: Intact outer, Im: Intact middle, Ii: Intact inner).

Grahic Jump Location
Fig. 4

Nominal strain maps for (a) a loaded intact and (b) loaded medially meniscectomized joint were produced. (c) Changes in nominal strain after meniscectomy were calculated by subtracting the meniscectomized strain map from the intact strain map.

Grahic Jump Location
Fig. 5

The areas of (a) high and (b) low strain (strain measurements outside the mean strain of the articular cartilage ± one standard deviation, or approximately the greatest and smallest 15% of the strain measurements in the intact joints) were significantly increased in the meniscectomized tibial condyle following medial meniscectomy

Grahic Jump Location
Fig. 6

Changes in the area of high + low strain is displayed. Changes in shear modulus, phase lag, proteoglycan (GAG) content, and collagen organization following meniscectomy from the work of Oakley et al. [4] are also compared. Stars indicate significant changes following meniscectomy in each property. The properties in meniscectomized knees were normalized by the properties of the unoperated contralateral knees in each intact and meniscectomized tibial condyle.

Grahic Jump Location
Fig. 7

Nominal strain changes in each column after medial meniscectomy. (Mo: Meniscectomy outer, Mmo: Meniscectomy middle-outer, Mmi: Meniscectomy middle-inner, Mi: Meniscectomy inner, Io: Intact outer, Im: Intact middle, Ii: Intact inner).

Grahic Jump Location
Fig. 8

Correlation between postmeniscectomy changes in (a) shear modulus and compressive strain, (b) phase lag and compressive strain, (c) GAG content and compressive strain, and (d) collagen content and compressive strain. Shear modulus, phase lag, GAG content, and collagen content data were employed from an in vivo sheep study by Appleyard et al. [3].

Tables

Errata

Discussions

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