Abstract
Articular cartilage is one of several biological tissues in which swelling effects are important in tissue mechanics and function, and may serve as an indicator of degenerative joint disease. This work presents a new approach to quantify swelling effects in articular cartilage, as well as to determine the material properties of cartilage from a simple free-swelling test. Samples of nondegenerate and degenerate human patellar cartilage were subjected to osmotic loading by equilibrating the tissue in solutions of varying osmolarity. The resulting swelling-induced strains were measured using a noncontacting optical method. A theoretical formulation of articular cartilage in a free-swelling configuration was developed based on an inhomogeneous, triphasic mechano-chemical model. Optimization of the model predictions to the experimental data was performed to determine two parameters descriptive of material stiffness at the surface and deeper cartilage layers, and a third parameter descriptive of thickness of the cartilage surface layer. These parameters were used to determine the thickness-averaged uniaxial modulus of cartilage, H(A). The obtained values for H(A) were similar to those for the tensile modulus of human cartilage reported in the literature. Degeneration resulted in an increase in thickness of the region of "apparent cartilage softening," and a decrease in the value for uniaxial modulus at this layer. These findings provide important evidence that collagen matrix disruption starts at the articular surface and progresses into the deeper layers with continued degeneration. These results suggest that the method provides a means to quantify the severity and depth of degenerative changes in articular cartilage. This method may also be used to determine material properties of cartilage in small joints in which conventional testing methods are difficult to apply.
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Selected References
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- Akizuki S., Mow V. C., Müller F., Pita J. C., Howell D. S., Manicourt D. H. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. J Orthop Res. 1986;4(4):379–392. doi: 10.1002/jor.1100040401. [DOI] [PubMed] [Google Scholar]
- Aspden R. M., Hukins D. W. Collagen organization in articular cartilage, determined by X-ray diffraction, and its relationship to tissue function. Proc R Soc Lond B Biol Sci. 1981 Jul 14;212(1188):299–304. doi: 10.1098/rspb.1981.0040. [DOI] [PubMed] [Google Scholar]
- Athanasiou K. A., Rosenwasser M. P., Buckwalter J. A., Malinin T. I., Mow V. C. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J Orthop Res. 1991 May;9(3):330–340. doi: 10.1002/jor.1100090304. [DOI] [PubMed] [Google Scholar]
- Bank R. A., Soudry M., Maroudas A., Mizrahi J., TeKoppele J. M. The increased swelling and instantaneous deformation of osteoarthritic cartilage is highly correlated with collagen degradation. Arthritis Rheum. 2000 Oct;43(10):2202–2210. doi: 10.1002/1529-0131(200010)43:10<2202::AID-ANR7>3.0.CO;2-E. [DOI] [PubMed] [Google Scholar]
- Basser P. J., Grodzinsky A. J. The Donnan model derived from microstructure. Biophys Chem. 1993 Feb;46(1):57–68. doi: 10.1016/0301-4622(93)87007-j. [DOI] [PubMed] [Google Scholar]
- Basser P. J., Schneiderman R., Bank R. A., Wachtel E., Maroudas A. Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique. Arch Biochem Biophys. 1998 Mar 15;351(2):207–219. doi: 10.1006/abbi.1997.0507. [DOI] [PubMed] [Google Scholar]
- Buschmann M. D., Grodzinsky A. J. A molecular model of proteoglycan-associated electrostatic forces in cartilage mechanics. J Biomech Eng. 1995 May;117(2):179–192. doi: 10.1115/1.2796000. [DOI] [PubMed] [Google Scholar]
- Clark J. M. The organisation of collagen fibrils in the superficial zones of articular cartilage. J Anat. 1990 Aug;171:117–130. [PMC free article] [PubMed] [Google Scholar]
- Clark J. M. 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. 1991 Mar;9(2):246–257. doi: 10.1002/jor.1100090213. [DOI] [PubMed] [Google Scholar]
- Ehrlich S., Wolff N., Schneiderman R., Maroudas A., Parker K. H., Winlove C. P. The osmotic pressure of chondroitin sulphate solutions: experimental measurements and theoretical analysis. Biorheology. 1998 Nov-Dec;35(6):383–397. doi: 10.1016/s0006-355x(99)80018-3. [DOI] [PubMed] [Google Scholar]
- Eisenberg S. R., Grodzinsky A. J. Swelling of articular cartilage and other connective tissues: electromechanochemical forces. J Orthop Res. 1985;3(2):148–159. doi: 10.1002/jor.1100030204. [DOI] [PubMed] [Google Scholar]
- Kovach I. S. The importance of polysaccharide configurational entropy in determining the osmotic swelling pressure of concentrated proteoglycan solution and the bulk compressive modulus of articular cartilage. Biophys Chem. 1995 Feb;53(3):181–187. doi: 10.1016/0301-4622(94)00100-x. [DOI] [PubMed] [Google Scholar]
- Lai W. M., Gu W. Y., Mow V. C. On the conditional equivalence of chemical loading and mechanical loading on articular cartilage. J Biomech. 1998 Dec;31(12):1181–1185. doi: 10.1016/s0021-9290(98)00099-2. [DOI] [PubMed] [Google Scholar]
- Lai W. M., Hou J. S., Mow V. C. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J Biomech Eng. 1991 Aug;113(3):245–258. doi: 10.1115/1.2894880. [DOI] [PubMed] [Google Scholar]
- Maroudas A. I. Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature. 1976 Apr 29;260(5554):808–809. doi: 10.1038/260808a0. [DOI] [PubMed] [Google Scholar]
- Maroudas A., Bannon C. Measurement of swelling pressure in cartilage and comparison with the osmotic pressure of constituent proteoglycans. Biorheology. 1981;18(3-6):619–632. doi: 10.3233/bir-1981-183-624. [DOI] [PubMed] [Google Scholar]
- Maroudas A. Biophysical chemistry of cartilaginous tissues with special reference to solute and fluid transport. Biorheology. 1975 Jun;12(3-4):233–248. doi: 10.3233/bir-1975-123-416. [DOI] [PubMed] [Google Scholar]
- Maroudas A., Venn M. Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. II. Swelling. Ann Rheum Dis. 1977 Oct;36(5):399–406. doi: 10.1136/ard.36.5.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Myers E. R., Lai W. M., Mow V. C. A continuum theory and an experiment for the ion-induced swelling behavior of articular cartilage. J Biomech Eng. 1984 May;106(2):151–158. doi: 10.1115/1.3138473. [DOI] [PubMed] [Google Scholar]
- Narmoneva D. A., Wang J. Y., Setton L. A. Nonuniform swelling-induced residual strains in articular cartilage. J Biomech. 1999 Apr;32(4):401–408. doi: 10.1016/s0021-9290(98)00184-5. [DOI] [PubMed] [Google Scholar]
- Roth V., Mow V. C. The intrinsic tensile behavior of the matrix of bovine articular cartilage and its variation with age. J Bone Joint Surg Am. 1980 Oct;62(7):1102–1117. [PubMed] [Google Scholar]
- Setton L. A., Tohyama H., Mow V. C. Swelling and curling behaviors of articular cartilage. J Biomech Eng. 1998 Jun;120(3):355–361. doi: 10.1115/1.2798002. [DOI] [PubMed] [Google Scholar]
- Urban J. P., Maroudas A., Bayliss M. T., Dillon J. Swelling pressures of proteoglycans at the concentrations found in cartilaginous tissues. Biorheology. 1979;16(6):447–464. doi: 10.3233/bir-1979-16609. [DOI] [PubMed] [Google Scholar]
- Venn M., Maroudas A. Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. I. Chemical composition. Ann Rheum Dis. 1977 Apr;36(2):121–129. doi: 10.1136/ard.36.2.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woo S. L., Akeson W. H., Jemmott G. F. Measurements of nonhomogeneous, directional mechanical properties of articular cartilage in tension. J Biomech. 1976;9(12):785–791. doi: 10.1016/0021-9290(76)90186-x. [DOI] [PubMed] [Google Scholar]
- Woo S. L., Lubock P., Gomez M. A., Jemmott G. F., Kuei S. C., Akeson W. H. Large deformation nonhomogeneous and directional properties of articular cartilage in uniaxial tension. J Biomech. 1979;12(6):437–446. doi: 10.1016/0021-9290(79)90028-9. [DOI] [PubMed] [Google Scholar]