Abstract
Osteoarthritis is a common disease. However, its causes and morphological features of diseased cartilage surfaces are not well understood. The purposes of this research were (a) to develop quantitative surface characterization techniques to study human cartilages at a micron and submicron scale and (b) to investigate distinctive changes in the surface morphologies and biomechanical properties of the cartilages in different osteoarthritis grades. Diseased cartilage samples collected from osteoarthritis patients were prepared for image acquisition using two different techniques, that is, laser scanning microscopy at a micrometer scale and atomic force microscopy at a nanometer scale. Three-dimensional, digital images of human cartilages were processed and analyzed quantitatively. This study has demonstrated that high-quality three-dimensional images of human cartilage surfaces could be obtained in a hydrated condition using laser scanning microscopy and atomic force microscopy. Based on the numerical data extracted from improved image quality and quantity, it has been found that osteoarthritis evolution can be identified by specific surface features at the micrometer scale, and these features are amplitude and functional property related. At the submicron level, the spatial features of the surfaces were revealed to differ between early and advanced osteoarthritis grades. The effective indentation moduli of human cartilages effectively revealed the cartilage deterioration. The imaging acquisition and numerical analysis methods established allow quantitative studies of distinctive changes in cartilage surface characteristics and better understanding of the cartilage degradation process.
References
| 1. |
Grushko, G, Schneiderman, R, Maroudas, A. Some biochemical and biophysical parameters for the study of the pathogenesis of osteoarthritis: a comparison between the processes of ageing and degeneration in human hip cartilage. Connect Tissue Res 1989; 19: 149–176. Google Scholar | Crossref | Medline | ISI |
| 2. |
Hudelmaier, M, Glaser, C, Hohe, J. Age-related changes in the morphology and deformational behavior of knee joint cartilage. Arthritis Rheum 2001; 44(11): 2556–2561. Google Scholar | Crossref | Medline |
| 3. |
Altman, RD . Overview of osteoarthritis. Am J Med 1987; 83(4B): 65–69. Google Scholar | Crossref | Medline | ISI |
| 4. |
Uhl, M, Ihling, C, Allmann, KH. Human articular cartilage: in vitro correlation of MRI and histologic findings. Eur Radiol 1998; 8: 1123–1129. Google Scholar | Crossref | Medline | ISI |
| 5. |
Faber, S, Eckstein, F, Lukasz, S. Gender differences in knee joint cartilage thickness, volume and articular surface areas: assessment with quantitative three-dimensional MR imaging. Skeletal Radiol 2001; 30: 144–150. Google Scholar | Crossref | Medline | ISI |
| 6. |
Buck, RJ, Wyman, BT, Le Graverand, MP. An efficient subset of morphological measures for articular cartilage in the healthy and diseased human knee. Magn Reson Med 2010; 63: 680–690. Google Scholar | Crossref | Medline | ISI |
| 7. |
Johansson, A, Kuiper, JH, Sundqvist, T. Spectroscopic measurement of cartilage thickness in arthroscopy: ex vivo validation in human knee condyles. Arthroscopy 2012; 28: 1513–1523. Google Scholar | Crossref | Medline | ISI |
| 8. |
Alhadlaq, H, Xia, Y, Moody, J. Detecting structural changes in early experimental osteoarthritis of tibial cartilage by microscopic magnetic resonance imaging and polarised light microscopy. Ann Rheum Dis 2004; 63: 709–717. Google Scholar | Crossref | Medline | ISI |
| 9. |
Quinn, TM, Hunziker, EB, Häuselmann, HJ. Variation of cell and matrix morphologies in articular cartilage among locations in the adult human knee. Osteoarthritis Cartilage 2005; 13: 672–678. Google Scholar | Crossref | Medline | ISI |
| 10. |
Cohen, ZA, McCarthy, DM, Kwak, SD. Knee cartilage topography, thickness and contact areas from MRI: in-vitro calibration and in-vivo measurements. Osteoarthritis Cartilage 1999; 7: 95–109. Google Scholar | Crossref | Medline | ISI |
| 11. |
Tummala, S, Bay-Jensen, AC, Karsdal, MA. Diagnosis of osteoarthritis by cartilage surface smoothness quantified automatically from knee MRI. Cartilage 2011; 2(1): 50–59. Google Scholar | SAGE Journals | ISI |
| 12. |
Accardi, MA, Dini, D, Cann, PM. Experimental and numerical investigation of the behaviour of articular cartilage under shear loading—interstitial fluid pressurisation and lubrication mechanisms. Tribol Int 2011; 44: 565–578. Google Scholar | Crossref | ISI |
| 13. |
Verberne, G, Merkher, Y, Halperin, G. Techniques for assessment of wear between human cartilage surfaces. Wear 2009; 266: 1216–1223. Google Scholar | Crossref | ISI |
| 14. |
Chan, SMT, Neu, CP, DuRaine, G. Atomic force microscope investigation of the boundary-lubricant layer in articular cartilage. Osteoarthritis Cartilage 2010; 18: 956–963. Google Scholar | Crossref | Medline | ISI |
| 15. |
Coles, JM, Blum, JJ, Jay, GD. In situ friction measurement on murine cartilage by atomic force microscopy. J Biomech 2008; 41(3): 541–548. Google Scholar | Crossref | Medline | ISI |
| 16. |
Imer, R, Akiyama, T, Stolz, M. The measurement of biomechanical properties of porcine articular cartilage using AFM. Arch Histol Cytol 2009; 72(5): 251–259. Google Scholar | Crossref | Medline |
| 17. |
Ghosh, S, Bowen, J, Jiang, K. Investigation of techniques for the measurement of articular cartilage surface roughness. Micron 2013; 44: 179–184. Google Scholar | Crossref | Medline | ISI |
| 18. |
Tian, Y, Wang, J, Peng, Z. A new approach to numerical characterisation of wear particle surfaces in three-dimensions for wear study. Wear 2012; 282–283: 59–68. Google Scholar | Crossref | ISI |
| 19. |
Peng, Z, Wang, M. Three dimensional surface characterization of human cartilages at a micron and nanometre scale. Wear 2013; 301: 210–217. Google Scholar | Crossref | ISI |
| 20. |
Wang, M, Wang, J, Peng, Z. Wear characterisation of articular cartilage surfaces at a nano-scale using atomic force microscopy. Tribol Int 2013; 63: 235–242. Google Scholar | Crossref | ISI |
| 21. |
Outerbridge, R, Dunlop, J. The problem of chondromalacia patellae. Clin Orthop Relat Res 1975; 110: 177–196. Google Scholar | Crossref |
| 22. |
Shepherd, DET, Seedhom, BB. Thickness of human articular cartilage in joints of the lower limb. Ann Rheum Dis 1999; 58: 27–34. Google Scholar | Crossref | Medline | ISI |
| 23. |
Bilodeau, G . Regular pyramid punch problem. J Appl Mech 1992; 59: 519–523. Google Scholar | Crossref | ISI |
| 24. |
Hori, R, Mockros, L. Indentation tests of human articular cartilage. J Biomech 1976; 9: 259–268. Google Scholar | Crossref | Medline | ISI |
| 25. |
Kempson, GE, Freeman, MAR, Swanson, SAV. The determination of a creep modulus for articular cartilage from indentation tests on the human femoral head. J Biomech 1971; 4: 239–250. Google Scholar | Crossref | Medline | ISI |
| 26. |
ISO 25178-2:2006 . Geometrical product specifications (GPS)-surface texture: areal—part 2: terms, definitions and surface texture parameters. Google Scholar |
| 27. |
Blunt, L, Jiang, X. Advanced techniques for assessment surface topography, development of a basis for 3D surface texture standards “SURFSTAND”. London: Kogan Page Science, 2003. Google Scholar |
| 28. |
Leach, R . Chapter 8 - Surface topography characterisation. In: Leach, R (ed.) Fundamental principles of engineering nanometrology. 2nd ed. Oxford: William Andrew, 2014, pp.241–294. Google Scholar | Crossref |
| 29. |
Montgomery, DC, Runger, GC, Hubele, NF. Engineering statistics. 5th ed. Hoboken, NJ: John Wiley & Sons, 2011. Google Scholar |
| 30. |
Stolz, M, Gottardi, R, Raiteri, R. Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nat Nanotechnol 2009; 4: 186−192. Google Scholar | Crossref | Medline | ISI |
| 31. |
Florindo, JB, Bruno, OM. Fractal descriptors based on Fourier spectrum applied to texture analysis. Physica A 2012; 391: 4909–4922. Google Scholar | Crossref | ISI |
| 32. |
Buckwalter, JA, Mankin, HJ, Grodzinsky, AJ. Articular cartilage and osteoarthritis. Instr Course Lect 2005; 54: 465–480. Google Scholar | Medline |
| 33. |
Wen, CY, Wu, CB, Tang, B. Collagen fibril stiffening in osteoarthritic cartilage of human beings revealed by atomic force microscopy. Osteoarthritis Cartilage 2012; 20(8): 916–922. Google Scholar | Crossref | Medline | ISI |
| 34. |
Karvonen, RL, Negendank, WG, Teitge, RA. Factors affecting articular cartilage thickness in osteoarthritis and aging. J Rheumatol 1994; 21(7): 1310–1318. Google Scholar | Medline | ISI |
| 35. |
Jiang, Y, Mishima, H, Sakai, S. Gene expression analysis of major lineage-defining factors in human bone marrow cells: effect of aging, gender, and age-related disorders. J Orthop Res 2008; 26(7): 910–917. Google Scholar | Crossref | Medline | ISI |
| 36. |
Julkunen, P, Kiviranta, P, Wilson, W. Characterization of articular cartilage by combining microscopic analysis with a fibril-reinforced finite-element model. J Biomech 2007; 40: 1862–1870. Google Scholar | Crossref | Medline | ISI |
