0
Research Papers

Patterns of Femoral Cartilage Thickness are Different in Asymptomatic and Osteoarthritic Knees and Can be Used to Detect Disease-Related Differences Between Samples

[+] Author and Article Information
Julien Favre

e-mail: jfavre@stanford.edu

Sean F. Scanlan

e-mail: scanlansean@gmail.com
Department of Mechanical Engineering,
Stanford University,
Durand Building 061,
496 Lomita Mall,
Stanford, CA 94305-4308

Jenifer C. Erhart-Hledik

e-mail: jerhart@stanford.edu

Katerina Blazek

e-mail: kblazek@stanford.edu
Department of Mechanical Engineering,
Stanford University,
Durand Building 061,
496 Lomita Mall,
Stanford, CA 94305-4308;
Center for Tissue Regeneration,
Repair, and Restoration,
Veterans Administration Hospital,
3801 Miranda Avenue,
Palo Alto, CA 94304-1207

Thomas P. Andriacchi

Department of Mechanical Engineering,
Stanford University,
Durand Building 227,
496 Lomita Mall,
Stanford, CA 94305-4308;
Center for Tissue Regeneration,
Repair, and Restoration,
Veterans Administration Hospital,
3801 Miranda Avenue,
Palo Alto, CA 94304-1207;
Department of Orthopedic Surgery,
Stanford University,
Durand Building 227,
496 Lomita Mall,
Stanford, CA 94305-4308,
e-mail: tandriac@stanford.edu

Contributed by the Bioengineering Division of ASME for publication in the Journal of Biomechanical Engineering. Manuscript received December 7, 2012; final manuscript received May 16, 2013; accepted manuscript posted May 22, 2013; published online September 13, 2013. Assoc. Editor: Tammy Haut Donahue.

J Biomech Eng 135(10), 101002 (Sep 13, 2013) (10 pages) Paper No: BIO-12-1601; doi: 10.1115/1.4024629 History: Received December 07, 2012; Revised May 16, 2013; Accepted May 22, 2013

Measures of mean cartilage thickness over predefined regions in the femoral plate using magnetic resonance imaging have provided important insights into the characteristics of knee osteoarthritis (OA), however, this quantification method suffers from the limited ability to detect OA-related differences between knees and loses potentially important information regarding spatial variations in cartilage thickness. The objectives of this study were to develop a new method for analyzing patterns of femoral cartilage thickness and to test the following hypotheses: (1) asymptomatic knees have similar thickness patterns, (2) thickness patterns differ with knee OA, and (3) thickness patterns are more sensitive than mean thicknesses to differences between OA conditions. Bi-orthogonal thickness patterns were extracted from thickness maps of segmented magnetic resonance images in the medial, lateral, and trochlea compartments. Fifty asymptomatic knees were used to develop the method and establish reference asymptomatic patterns. Another subgroup of 20 asymptomatic knees and three subgroups of 20 OA knees each with a Kellgren/Lawrence grade (KLG) of 1, 2, and 3, respectively, were selected for hypotheses testing. The thickness patterns were similar between asymptomatic knees (coefficient of multiple determination between 0.8 and 0.9). The thickness pattern alterations, i.e., the differences between the thickness patterns of an individual knee and reference asymptomatic thickness patterns, increased with increasing OA severity (Kendall correlation between 0.23 and 0.47) and KLG 2 and 3 knees had significantly larger thickness pattern alterations than asymptomatic knees in the three compartments. On average, the number of significant differences detected between the four subgroups was 4.5 times greater with thickness pattern alterations than mean thicknesses. The increase was particularly marked in the medial compartment, where the number of significant differences between subgroups was 10 times greater with thickness pattern alterations than mean thickness measurements. Asymptomatic knees had characteristic regional thickness patterns and these patterns were different in medial OA knees. Assessing the thickness patterns, which account for the spatial variations in cartilage thickness and capture both cartilage thinning and swelling, could enhance the capacity to detect OA-related differences between knees.

FIGURES IN THIS ARTICLE
<>
Copyright © 2013 by ASME
Your Session has timed out. Please sign back in to continue.

References

Andriacchi, T. P., Mundermann, A., Smith, R. L., Alexander, E. J., Dyrby, C. O., and Koo, S., 2004, “A Framework for the in Vivo Pathomechanics of Osteoarthritis of the Knee,” Ann. Biomed. Eng., 32, pp. 447–457. [CrossRef] [PubMed]
Adam, C., Eckstein, F., Milz, S., and Putz, R., 1998, “The Distribution of Cartilage Thickness Within the Joints of the Lower Limb of Elderly Individuals,” J. Anat., 193, pp. 203–214. [CrossRef] [PubMed]
Cohen, Z. A., Mow, V. C., Henry, J. H., Levine, W. N., and Ateshian, G. A., 2003, “Templates of the Cartilage Layers of the Patellofemoral Joint and Their Use in the Assessment of Osteoarthritis Cartilage Damage,” Osteoarthritis Cartilage, 11, pp. 569–579. [CrossRef] [PubMed]
Wirth, W., and Eckstein, F., 2008, “A Technique for Regional Analysis of Femorotibial Cartilage Thickness Based on Quantitative Magnetic Resonance Imaging,” IEEE Trans. Med. Imaging, 27, pp. 737–744. [CrossRef] [PubMed]
Koo, S., Gold, G. E., and Andriacchi, T. P., 2005, “Considerations in Measuring Cartilage Thickness Using MRI: Factors Influencing Reproducibility and Accuracy,” Osteoarthritis Cartilage, 13, pp. 782–789. [CrossRef] [PubMed]
Eckstein, F., and Wirth, W., 2011, “Quantitative Cartilage Imaging in Knee Osteoarthritis,” Arthritis, 2011, 19 pages. [CrossRef]
Buck, R. J., Wyman, B. T., Hellio Le Graverand, M. P., Wirth, W., and Eckstein, F., 2010, “An Efficient Subset of Morphological Measures for Articular Cartilage in the Healthy and Diseased Human Knee,” Magn. Reson. Med., 63, pp. 680–690. [CrossRef] [PubMed]
Buck, R. J., Wyman, B. T., Hellio Le Graverand, M. P., Hudelmaier, M., Wirth, W., and Eckstein, F., 2010, “Osteoarthritis May Not be a One-Way-Road of Cartilage Loss—Comparison of Spatial Patterns of Cartilage Change Between Osteoarthritic and Healthy Knees,” Osteoarthritis Cartilage, 18, pp. 329–335. [CrossRef] [PubMed]
Pelletier, J. P., Raynauld, J. P., Berthiaume, M. J., Abram, F., Choquette, D., Haraoui, B., Beary, J., Cline, G. A., Meyer, J. M., and Martel-Pelletier, J., 2007, “Risk Factors Associated With the Loss of Cartilage Volume on Weight-Bearing Areas in Knee Osteoarthritis Patients Assessed by Quantitative Magnetic Resonance Imaging: A Longitudinal Study,” Arthritis Res. Ther., 9, p. R74. [CrossRef] [PubMed]
Eckstein, F., Cicuttini, F., Raynauld, J. P., Waterton, J. C., and Peterfly, C., 2006, “Magnetic Resonance Imaging (MRI) of Articular Cartilage in the Knee Osteoarthritis (OA): Morphological Assessment,” Osteoarthritis Cartilage, 12(Suppl.), pp. 46–75. [CrossRef]
Reichenbach, S., Yang, M., Eckstein, F., Niu, J., Hunter, D. J., McLennan, C. E., Guermazi, A., Roemer, F., Hudelmaier, M., Aliabadi, P., and Felson, D. T., 2010, “Does Cartilage Volume or Thickness Distinguish Knees With and Without Mild Radiographic Osteoarthritis? The Framingham Study,” Ann. Rheum. Dis., 69, pp. 143–149. [CrossRef] [PubMed]
Hunter, D. J., Li, L., Zhang, Y. Q., Totterman, S., Tamez, J., Kwohl, C. K., Eaton, C. B., Hellio Le Graverand, M. P., and Beals, C. R., 2010, “Region of Interest Analysis: By Selecting Regions With Denuded Areas Can We Detect Greater Amounts of Change?,” Osteoarthritis Cartilage, 18, pp. 175–183. [CrossRef] [PubMed]
Andriacchi, T. P., 2013, “Valgus Alignment and Lateral Compartment Knee OA: A Biomechanical Paradox or New Insight Into Knee OA?,” Arthritis Rheum., 65, pp. 310–313. [CrossRef]
Forbell, R. B., Nevitt, M. C., Hudelmaier, M., Wirth, W., Wyman, B. T., Benichou, O., Dreher, D., Davies, R., Lee, J. H., Baribaud, F., Gimona, A., and Eckstein, F., 2010, “Femorotibial Subchondral Bone Area and Regional Cartilage Thickness: A Cross-Sectional Description in Healthy Reference Cases and Various Radiographic Stages of Osteoarthritis in 1,003 Knees From the Osteoarthritis Initiative,” Arthritis Care Res., 62, pp. 1612–1623. [CrossRef]
Eckstein, F., Winzheimer, M., Hohe, J., Englmeier, K. H., and Reiser, M., 2001, “Interindividual Variability and Correlation Among Morphological Parameters of Knee Joint Cartilage Plates: Analysis With Three-Dimensional MR Imaging,” Osteoarthritis Cartilage, 9, pp. 101–111. [CrossRef] [PubMed]
Eckstein, F., Yang, M., Guermazi, A., Roemer, F. W., Hudelmaier, M., Picha, K., Baribaud, F., Wirth.W., and Felson, D. T., 2010, “Reference Values and Z-scores for Subregional Femorotibial Cartilage Thickness—Results From a Large Population-Based Sample (Framingham) and Comparison With the Non-Exposed Osteoarthritis Initiative Reference Cohort,” Osteoarthritis Cartilage, 18, pp. 1275–1283. [CrossRef] [PubMed]
Eckstein, F., Gavazzeni, A., Sittek, H., Haubner, M., Lösch, A., Milz, S., Englmeier, K. H., Schulte, E., Putz, R., and Reiser, M., 1996, “Determination of Knee Joint Cartilage Thickness Using Three-Dimensional Magnetic Resonance Chondro-Crassometry (3D MR-CCM),” Magn. Reson. Med., 36, pp. 256–265. [CrossRef] [PubMed]
Connolly, A., FitzPatrick, D., Moulton, J., Lee, J., and Lerner, A., 2008, “Tibiofemoral Cartilage Thickness Distribution and Its Correlation With Anthropometric Variables,” Proc. Inst, Mech. Eng., Part H: J. Eng. Med., 222, pp. 29–39. [CrossRef]
Li, G., Park, S. E., Defrate, L. E., Schutzer, M. E., Ji, L., Gill, T. J., and Rubash, H. E., 2005, “The Cartilage Thickness Distribution in the Tibiofemoral Joint and its Correlation With Cartilage-to-Cartilage Contact,” Clin. Biomech. (Bristol, Avon), 20, pp. 736–744. [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, 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, pp. 849–854. [CrossRef]
Favre, J., Blazek, K., Erhart, J. C., and Andriacchi, T. P., 2012, “Characterization of the Spatial Cartilage Thickness Distribution on the Distal Femur in Healthy Knees,” Proceedings of the Annual Meeting of the Orthopeadic Research Society, San-Francisco, CA, pp. 1795.
Chaudhari, A. M. W., Briant, P. L., Bevill, S. L., Koo, S., and Andriacchi, T. P., 2008, “Knee Kinematics, Cartilage Morphology and Osteoarthritis After ACL Injury,” Med. Sci. Sports Exercise, 40, pp. 215–222. [CrossRef]
Bevill, S. L., Briant, P. L., Levenston, M. E., and Andriacchi, T. P., 2009, “Central and Peripheral Region Tibial Plateau Chondrocytes Respond Differently to in Vitro Dynamic Compression,” Osteoarthritis Cartilage, 17, pp. 980–987. [CrossRef] [PubMed]
Andriacchi, T. P., Koo, S., and Scanlan, S. F., 2009, “Gait Mechanics Influence Healthy Cartilage Morphology and Osteoarthritis of the Knee,” J. Bone Jt. Surg., Am., 91, pp. 95–101. [CrossRef]
Creaby, M. W., Wang, Y., Bennell, K. L., Hinman, R. S., Metcalf, B. R., Bowles, K. A., and Cicuttini, F. M., 2010, “Dynamic Knee Loading is Related to Cartilage Defects and Tibial Plateau Bone Area in Medial Knee Osteoarthritis,” Osteoarthritis Cartilage, 18, pp. 1380–1388. [CrossRef] [PubMed]
Sharma, L., Hurwitz, D. E., Thonar, E. J., Sum, J. A., Lenz, M. E., Dunlop, D. D., Schnitzer, T. J., Kirwan-Mellis, G., and Andriacchi, T. P., 1998, “Knee Adduction Moment, Serum Hyaluronan Level, and Disease Severity in Medial Tibiofemoral Osteoarthritis,” Arthritis Rheum., 41, pp. 1233–1240. [CrossRef] [PubMed]
Favre, J., Hayoz, M., Erhart-Hledik, J. C., and Andriacchi, T. P., 2012, “A Neural Network Model to Predict Knee Adduction Moment During Walking Based on Ground Reaction Force and Anthropometric Measurements,” J. Biomech., 45, pp. 692–698. [CrossRef] [PubMed]
Miyazaki, T., Wada, M., Kawahara, H., Sato, M., Baba, H., and Shimada, S., 2002, “Dynamic Load at Baseline Can Predict Radiographic Disease Severity in Medial Compartment Knee Osteoarthritis,” Ann. Rheum. Dis., 61, pp. 617–622. [CrossRef] [PubMed]
Wirth, W., Benichou, O., Kwoh, C. K., Guermazi, A., Hunter, D., Putz, R., and Eckstein, F., 2010, “Spatial Patterns of Cartilage Loss in the Medial Femoral Condyle in Osteoarthritic Knees: Data From the Osteoarthritis Initiative,” Magn. Reson. Med., 63, pp. 574–581. [CrossRef] [PubMed]
Ahmad, C. S., Cohen, Z. A., Levine, W. N., Ateshian, G. A., and Mow, V. C., 2001, “Biomechanical and Topographic Considerations for Autologous Osteochondral Grafting in the Knee,” Am. J. Sports Med., 29, pp. 201–206. [PubMed]
Gulati, A., Chau, R., Beard, D. J., Price, A. J., Gill, H. S., and Murray, D. W., 2009, “Localization of the Full-Thickness Cartilage Lesions in Medial and Lateral Unicompartmental Knee Osteoarthritis,” J. Orthop. Res., 27, pp. 1339–1346. [CrossRef] [PubMed]
Kellgren, J. H., and Lawrence, J. S., 1957, “Radiological Assessment of Osteoarthritis,” Ann. Rheum. Dis., 16, pp. 494–502. [CrossRef] [PubMed]
Kauffmann, C., Gravel, P., Godbout, B., Gravel, A., Beaudoin, G., Raynauld, J. P., Martel-Pelletier, J., Pelletier, J. P., and de Guise, J. A., 2003, “Computer-Aided Method for Quantification of Cartilage Thickness and Volume Changes Using MRI: Validation Study Using a Synthetic Model,” IEEE Trans. Biomed. Eng., 50, pp. 978–988. [CrossRef] [PubMed]
Neter, J., Wasserman, W., and Kunter, M. H., 1985, Applied Linear Statistical Models: Regression, Analysis of Variance, and Experimental Designs, Irwin series in statistics, Irwin, ed., Chicago, IL.
Ahlback, S., 1968, “Osteoarthrosis of the Knee. A Radiographic Investigation,” Acta Radiologica Diagnosis, 277(Suppl.), pp. 70–72.
Hellio Le Graverand, M. P., Buck, R. J., Wyman, B. T., Vignon, E., Mazzuca, S. A., Brandt, K. D., Piperno, M., Charles, H. C., Hudelmaier, M., Hunter, D. J., Jackson, C., Kraus, V. B., Link, M. T., Majumdar, S., Prasad, P. V., Schnitzer, T. J., Vaz, A., Wirth, W., Eckstein, F., 2009, “Subregional Femoral Cartilage Morphology in Women—Comparison Between Healthy Controls and Participants With Different Grades of Radiographic Knee Osteoarthritis,” Osteoarthritis Cartilage, 17, pp. 1177–1185. [CrossRef] [PubMed]
Eckstein, F., Nevitt, M., Gimona, A., Picha, K., Lee, J. H., Davies, R. Y., Dreher, D., Benichou, O., Hellio Le Graverand, M. P., Hudelmaier, M., Maschek, S., and Wirth, W., 2011, “Rates of Change and Sensitivity to Change in Cartilage Morphology in Healthy Knees and in Knees With Mild, Moderate, and End-Stage Radiographic Osteoarthritis: Results From 831 Participants From the Osteoarthritis Initiative,” Arthritis Care Res., 63, pp. 311–319. [CrossRef]

Figures

Grahic Jump Location
Fig. 1

Illustration of the method used to build the thickness map based MR images. (a) Segmentation of one MR image (solid line) and results from the segmentation of more medial images (dashed lines; 1 slice out of 6 is displayed). (b) Reconstruction of the three-dimensional cartilage model. The plane corresponding to the image segmented in (a) is indicated by a solid line. (c) Thickness map for the bone-cartilage layer. Again, the plane corresponding to the image segmented in (a) is indicated by a solid line.

Grahic Jump Location
Fig. 2

(a) Thickness map with superposition of the cylinder fit used to define the coordinate system. (b) Example of thickness cut extraction around a point located 60 deg posterior to the notch and at 25% of the medial-lateral width.

Grahic Jump Location
Fig. 3

Illustration of the thickness cut extraction method. (a) The algorithm searches for the point within the search regions which provides thickness cuts that best match reference thickness cuts. (b) Thickness cuts for the best-matching points in the thickness map displayed in (a) and the reference asymptomatic thickness cuts (obtained with the training dataset) used for the searches.

Grahic Jump Location
Fig. 4

Description of the sizes of the thickness cuts and the search regions as determined after the training phase. It is important to note that the best-matching points are located at the center of the search regions in this figure, but that these points can actually be anywhere in the search regions, depending on the individual thickness shape of the knee under analysis. It should also be noted that the search regions agree with the regions of thicker cartilage described in prior studies [20-22].

Grahic Jump Location
Fig. 5

Decomposition of a thickness cut into its relative (zero-mean) pattern and its mean value

Grahic Jump Location
Fig. 6

Illustration of the “thickness pattern alteration” (Δtp) metric used to evaluate the similarity between the thickness pattern of an individual knee and the corresponding asymptomatic reference thickness pattern. As depicted in the right plot, Δtp is sensitive to local cartilage thinning and/or thickening that modify the form of the thickness pattern. Note that global cartilage thinning or thickening (i.e., changes in the mean value of the thickness cut) does not affect Δtp.

Grahic Jump Location
Fig. 7

Illustration of the regions used for the secondary mean thickness measurements. (a) Ovoid regions defined by the size of the bi-orthogonal cuts and centered on the individual best-matching points. (b) A set of eight standard regions of interest [9].

Grahic Jump Location
Fig. 8

Thickness patterns for the four subgroups in the analysis dataset (n = 20 knees per subgroup). Each graph displays the average (black line) ± one standard deviation (gray area) of a subgroup along with the coefficients of multiple determination (CMD) for the subgroup. For comparison, the reference asymptomatic thickness patterns (obtained with the training dataset) are presented using a blue dashed line.

Grahic Jump Location
Fig. 9

Box plots of the thickness pattern alterations (Δtp) for the four subgroups in the analysis dataset. The bars at the top of the boxes indicate significant differences between the subgroups (p < 0.008). The values at the top of the graphs correspond to the Kendall correlation coefficients (τ); the following symbols indicate significant correlations (: p < 0.01, ¶¶: p < 0.001, ¶¶¶: p < 0.0001).

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