Determining Tension–Compression Nonlinear Mechanical Properties of Articular Cartilage from Indentation Testing

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• 作者：Xingyu Chen ; Yilu Zhou ; Liyun Wang ; Michael H. Santare…
• 关键词：Biphasic ; Fiber ; reinforced ; Curve ; fitting ; Creep ; Optimization
• 刊名：Annals of Biomedical Engineering
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：44
• 期：4
• 页码：1148-1158
• 全文大小：1,509 KB
• 参考文献：1.Allen, K. D., and K. A. Athanasiou. Viscoelastic characterization of the porcine temporomandibular joint disc under unconfined compression. J. Biomech. 39:312–322, 2006.CrossRef PubMed
  2.Appleyard, R. C., P. Ghosh, and M. V. Swain. Biomechanical, histological and immunohistological studies of patellar cartilage in an ovine model of osteoarthritis induced by lateral meniscectomy. Osteoarthr. Cartil. 7:281–294, 1999.CrossRef PubMed
  3.Ateshian, G. A., V. Rajan, N. O. Chahine, C. E. Canal, and C. T. Hung. Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. J. Biomech. Eng. 131:061003, 2009.CrossRef PubMed PubMedCentral
  4.Athanasiou, K. A., A. Agarwal, and F. J. Dzida. Comparative study of the intrinsic mechanical properties of the human acetabular and femoral head cartilage. J. Orthop. Res. 12:340–349, 1994.CrossRef PubMed
  5.Athanasiou, K. A., M. P. Rosenwasser, J. A. Buckwalter, T. I. Malinin, and V. C. Mow. Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage. J. Orthop. Res. 9:330–340, 1991.CrossRef PubMed
  6.Bae, W. C., C. W. Lewis, M. E. Levenston, and R. L. Sah. Indentation testing of human articular cartilage: effects of probe tip geometry and indentation depth on intra-tissue strain. J. Biomech. 39:1039–1047, 2006.CrossRef PubMed
  7.Bae, W. C., M. M. Temple, D. Amiel, R. D. Coutts, G. G. Niederauer, and R. L. Sah. Indentation testing of human cartilage: sensitivity to articular surface degeneration. Arthritis Rheum. 48:3382–3394, 2003.CrossRef PubMed
  8.Chahine, N. O., C. C. Wang, C. T. Hung, and G. A. Ateshian. Anisotropic strain-dependent material properties of bovine articular cartilage in the transitional range from tension to compression. J. Biomech. 37:1251–1261, 2004.CrossRef PubMed PubMedCentral
  9.Chen, X., B. K. Zimmerman, and X. L. Lu. Determine the equilibrium mechanical properties of articular cartilage from the short-term indentation response. J. Biomech. 48:176–180, 2015.CrossRef PubMed
  10.Darling, E. M., S. Zauscher, and F. Guilak. Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthr. Cartil. 14:571–579, 2006.CrossRef PubMed
  11.Detamore, M. S., and K. A. Athanasiou. Tensile properties of the porcine temporomandibular joint disc. J. Biomech. Eng. 125:558–565, 2003.CrossRef PubMed
  12.DiSilvestro, M. R., Q. Zhu, M. Wong, J. S. Jurvelin, and J. K. Suh. Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: I-Simultaneous prediction of reaction force and lateral displacement. J. Biomech. Eng. 123:191–197, 2001.CrossRef PubMed
  13.Fortin, M., J. Soulhat, A. Shirazi-Adl, E. B. Hunziker, and M. D. Buschmann. Unconfined compression of articular cartilage: nonlinear behavior and comparison with a fibril-reinforced biphasic model. J. Biomech. Eng. 122:189–195, 2000.CrossRef PubMed
  14.Guo, H., and R. L. Spilker. An augmented Lagrangian finite element formulation for 3D contact of biphasic tissues. Comput. Methods Biomech. Biomed. Eng. 17:1206–1216, 2014.CrossRef
  15.Gupta, S., J. Lin, P. Ashby, and L. Pruitt. A fiber reinforced poroelastic model of nanoindentation of porcine costal cartilage: a combined experimental and finite element approach. J. Mech. Behav. Biomed. Mater. 2:326–337, 2009.CrossRef PubMed
  16.Han, L., E. H. Frank, J. J. Greene, H. Y. Lee, H. H. Hung, A. J. Grodzinsky, and C. Ortiz. Time-dependent nanomechanics of cartilage. Biophys. J. 100:1846–1854, 2011.CrossRef PubMed PubMedCentral
  17.Hayes, W. C., L. M. Keer, G. Herrmann, and L. F. Mockros. A mathematical analysis for indentation tests of articular cartilage. J. Biomech. 5:541–551, 1972.CrossRef PubMed
  18.Huang, C. Y., M. A. Soltz, M. Kopacz, V. C. Mow, and G. A. Ateshian. Experimental verification of the roles of intrinsic matrix viscoelasticity and tension-compression nonlinearity in the biphasic response of cartilage. J. Biomech. Eng. 125:84–93, 2003.CrossRef PubMed
  19.Huang, C. Y., A. Stankiewicz, G. A. Ateshian, and V. C. Mow. Anisotropy, inhomogeneity, and tension-compression nonlinearity of human glenohumeral cartilage in finite deformation. J. Biomech. 38:799–809, 2005.CrossRef PubMed PubMedCentral
  20.Julkunen, P., W. Wilson, H. Isaksson, J. S. Jurvelin, W. Herzog, and R. K. Korhonen. A review of the combination of experimental measurements and fibril-reinforced modeling for investigation of articular cartilage and chondrocyte response to loading. Comput. Math. Methods Med. 2013:326150, 2013.CrossRef PubMed PubMedCentral
  21.Jurvelin, J. S., M. D. Buschmann, and E. B. Hunziker. Optical and mechanical determination of Poisson’s ratio of adult bovine humeral articular cartilage. J. Biomech. 30:235–241, 1997.CrossRef PubMed
  22.Le, N. A., and B. C. Fleming. Measuring fixed charge density of goat articular cartilage using indentation methods and biochemical analysis. J. Biomech. 41:715–720, 2008.CrossRef PubMed PubMedCentral
  23.LeRoux, M. A., and L. A. Setton. Experimental and biphasic FEM determinations of the material properties and hydraulic permeability of the meniscus in tension. J. Biomech. Eng. 124:315–321, 2002.CrossRef PubMed
  24.Li, Q., B. Doyran, L. W. Gamer, X. L. Lu, L. Qin, C. Ortiz, A. J. Grodzinsky, V. Rosen, and L. Han. Biomechanical properties of murine meniscus surface via AFM-based nanoindentation. J. Biomech. 48:1364–1370, 2015.CrossRef PubMed
  25.Lu, X. L., and V. C. Mow. Biomechanics of articular cartilage and determination of material properties. Med. Sci. Sports Exerc. 40:193–199, 2008.CrossRef PubMed
  26.Lu, X. L., D. D. Sun, X. E. Guo, F. H. Chen, W. M. Lai, and V. C. Mow. Indentation determined mechanoelectrochemical properties and fixed charge density of articular cartilage. Ann. Biomed. Eng. 32:370–379, 2004.CrossRef PubMed
  27.Maas, S. A., B. J. Ellis, G. A. Ateshian, and J. A. Weiss. FEBio: finite elements for biomechanics. J. Biomech. Eng. 134:011005, 2012.CrossRef PubMed
  28.Mak, A. F., W. M. Lai, and V. C. Mow. Biphasic indentation of articular cartilage—I. Theoretical analysis. J Biomech. 20:703–714, 1987.CrossRef PubMed
  29.Makela, J. T., M. R. Huttu, and R. K. Korhonen. Structure-function relationships in osteoarthritic human hip joint articular cartilage. Osteoarthr. Cartil. 20:1268–1277, 2012.CrossRef PubMed PubMedCentral
  30.Mow, V. C., M. C. Gibbs, W. M. Lai, W. B. Zhu, and K. A. Athanasiou. Biphasic indentation of articular cartilage—II. A numerical algorithm and an experimental study. J. Biomech. 22:853–861, 1989.CrossRef PubMed
  31.Mow, V. C., W. Y. Gu, and F. H. Chen. Structure and function of articular cartilage and meniscus. In: Basic orthopaedic biomechanics and mechano-biology, edited by V. C. Mow, and R. Huiskes. Philadelphia: Lippincott Williams & Wilkins, 2005, pp. 181–258.
  32.Mow, V. C., S. C. Kuei, W. M. Lai, and C. G. Armstrong. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. J Biomech Eng. 102:73–84, 1980.CrossRef PubMed
  33.Moyer, J. T., A. C. Abraham, and T. L. Haut Donahue. Nanoindentation of human meniscal surfaces. J. Biomech. 45:2230–2235, 2012.CrossRef PubMed PubMedCentral
  34.Park, S., R. Krishnan, S. B. Nicoll, and G. A. Ateshian. Cartilage interstitial fluid load support in unconfined compression. J. Biomech. 36:1785–1796, 2003.CrossRef PubMed PubMedCentral
  35.Ruggiero, L., B. K. Zimmerman, M. Park, L. Han, L. Wang, D. L. Burris and X. L. Lu. Roles of the Fibrous Superficial Zone in the Mechanical Behavior of TMJ Condylar Cartilage. Ann. Biomed. Eng. PMID: 25893511, 2015.
  36.Simha, N. K., H. Jin, M. L. Hall, S. Chiravarambath, and J. L. Lewis. Effect of indenter size on elastic modulus of cartilage measured by indentation. J. Biomech. Eng. 129:767–775, 2007.CrossRef PubMed
  37.Soltz, M. A., and G. A. Ateshian. A conewise linear elasticity mixture model for the analysis of tension-compression nonlinearity in articular cartilage. J. Biomech. Eng. 122:576–586, 2000.CrossRef PubMed PubMedCentral
  38.Spilker, R. L., J. K. Suh, and V. C. Mow. A finite element analysis of the indentation stress-relaxation response of linear biphasic articular cartilage. J. Biomech. Eng. 114:191–201, 1992.CrossRef PubMed
  39.Taffetani, M., M. Griebel, D. Gastaldi, S. M. Klisch, and P. Vena. Poroviscoelastic finite element model including continuous fiber distribution for the simulation of nanoindentation tests on articular cartilage. J. Mech. Behav. Biomed. Mater. 32:17–30, 2014.CrossRef PubMed
  40.Wang, C. C., J. M. Deng, G. A. Ateshian, and C. T. Hung. An automated approach for direct measurement of two-dimensional strain distributions within articular cartilage under unconfined compression. J. Biomech. Eng. 124:557–567, 2002.CrossRef PubMed
  41.Williamson, A. K., A. C. Chen, K. Masuda, E. J. Thonar, and R. L. Sah. Tensile mechanical properties of bovine articular cartilage: variations with growth and relationships to collagen network components. J. Orthop. Res. 21:872–880, 2003.CrossRef PubMed
  42.Williamson, A. K., A. C. Chen, and R. L. Sah. Compressive properties and function-composition relationships of developing bovine articular cartilage. J. Orthop. Res. 19:1113–1121, 2001.CrossRef PubMed
  43.Wilson, W., C. C. van Donkelaar, B. van Rietbergen, and R. Huiskes. A fibril-reinforced poroviscoelastic swelling model for articular cartilage. J. Biomech. 38:1195–1204, 2005.CrossRef PubMed
  44.Wilson, W., C. C. van Donkelaar, B. van Rietbergen, K. Ito, and R. Huiskes. Stresses in the local collagen network of articular cartilage: a poroviscoelastic fibril-reinforced finite element study. J. Biomech. 37:357–366, 2004.CrossRef PubMed
  
• 作者单位：Xingyu Chen (1)
  Yilu Zhou (1)
  Liyun Wang (1)
  Michael H. Santare (1)
  Leo Q. Wan (2)
  X. Lucas Lu (1)
  
  1. Department of Mechanical Engineering, University of Delaware, 130 Academy Street SPL 126, Newark, DE, 19716, USA
  2. Department of Biomedical Engineering, Rensselaer Polytechnic Institute, Troy, NY, 12180, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Biomedicine
  Biomedical Engineering
  Biophysics and Biomedical Physics
  Mechanics
  Biochemistry
  
• 出版者：Springer Netherlands
• ISSN：1573-9686

文摘

The indentation test is widely used to determine the in situ biomechanical properties of articular cartilage. The mechanical parameters estimated from the test depend on the constitutive model adopted to analyze the data. Similar to most connective tissues, the solid matrix of cartilage displays different mechanical properties under tension and compression, termed tension–compression nonlinearity (TCN). In this study, cartilage was modeled as a porous elastic material with either a conewise linear elastic matrix with cubic symmetry or a solid matrix reinforced by a continuous fiber distribution. Both models are commonly used to describe the TCN of cartilage. The roles of each mechanical property in determining the indentation response of cartilage were identified by finite element simulation. Under constant loading, the equilibrium deformation of cartilage is mainly dependent on the compressive modulus, while the initial transient creep behavior is largely regulated by the tensile stiffness. More importantly, altering the permeability does not change the shape of the indentation creep curves, but introduces a parallel shift along the horizontal direction on a logarithmic time scale. Based on these findings, a highly efficient curve-fitting algorithm was designed, which can uniquely determine the three major mechanical properties of cartilage (compressive modulus, tensile modulus, and permeability) from a single indentation test. The new technique was tested on adult bovine knee cartilage and compared with results from the classic biphasic linear elastic curve-fitting program.