Evaluation of a post-processing approach for multiscale analysis of biphasic mechanics of chondrocytes

Understanding the mechanical behaviour of chondrocytes as a result of cartilage tissue mechanics has significant implications for both evaluation of mechanobiological function and to elaborate on damage mechanisms. A common procedure for prediction of chondrocyte mechanics (and of cell mechanics in general) relies on a computational post-processing approach where tissue-level deformations drive cell-level models. Potential loss of information in this numerical coupling approach may cause erroneous cellular-scale results, particularly during multiphysics analysis of cartilage. The goal of this study was to evaluate the capacity of first- and second-order data passing to predict chondrocyte mechanics by analysing cartilage deformations obtained for varying complexity of loading scenarios. A tissue-scale model with a sub-region incorporating representation of chondron size and distribution served as control. The post-processing approach first required solution of a homogeneous tissue-level model, results of which were used to drive a separate cell-level model (same characteristics as the sub-region of control model). The first-order data passing appeared to be adequate for simplified loading of the cartilage and for a subset of cell deformation metrics, for example, change in aspect ratio. The second-order data passing scheme was more accurate, particularly when asymmetric permeability of the tissue boundaries was considered. Yet, the method exhibited limitations for predictions of instantaneous metrics related to the fluid phase, for example, mass exchange rate. Nonetheless, employing higher order data exchange schemes may be necessary to understand the biphasic mechanics of cells under lifelike tissue loading states for the whole time history of the simulation.

[1]  W M Lai,et al.  A triphasic theory for the swelling and deformation behaviors of articular cartilage. , 1991, Journal of biomechanical engineering.

[2]  A. Gefen,et al.  Deformations, mechanical strains and stresses across the different hierarchical scales in weight-bearing soft tissues. , 2012, Journal of tissue viability.

[3]  V. Mow,et al.  The functional environment of chondrocytes within cartilage subjected to compressive loading: a theoretical and experimental approach. , 2002, Biorheology.

[4]  Harm Askes,et al.  Representative volume: Existence and size determination , 2007 .

[5]  Scott C. Sibole,et al.  Chondrocyte Deformations as a Function of Tibiofemoral Joint Loading Predicted by a Generalized High-Throughput Pipeline of Multi-Scale Simulations , 2012, PloS one.

[6]  E B Hunziker,et al.  Quantitative structural organization of normal adult human articular cartilage. , 2002, Osteoarthritis and cartilage.

[7]  Wei Sun,et al.  Three dimensional multi-scale modelling and analysis of cell damage in cell-encapsulated alginate constructs. , 2010, Journal of biomechanics.

[8]  Gerard A Ateshian,et al.  Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. , 2009, Journal of biomechanical engineering.

[9]  A. Grodzinsky,et al.  Cartilage tissue remodeling in response to mechanical forces. , 2000, Annual review of biomedical engineering.

[10]  V C Mow,et al.  The nonlinear characteristics of soft gels and hydrated connective tissues in ultrafiltration. , 1990, Journal of biomechanics.

[11]  T. Laursen,et al.  Finite Element Modeling Predictions of Region-specific Cell-matrix Mechanics in the Meniscus , 2006, Biomechanics and modeling in mechanobiology.

[12]  W Herzog,et al.  A novel method for determining articular cartilage chondrocyte mechanics in vivo. , 2011, Journal of biomechanics.

[13]  R. Fisher 014: On the "Probable Error" of a Coefficient of Correlation Deduced from a Small Sample. , 1921 .

[14]  Jukka S. Jurvelin,et al.  Composition of the pericellular matrix modulates the deformation behaviour of chondrocytes in articular cartilage under static loading , 2009, Medical & Biological Engineering & Computing.

[15]  Douglas G. Altman,et al.  Measurement in Medicine: The Analysis of Method Comparison Studies , 1983 .

[16]  G A Ateshian,et al.  Biomechanics of diarthrodial joints: a review of twenty years of progress. , 1993, Journal of biomechanical engineering.

[17]  R K Korhonen,et al.  Effect of superficial collagen patterns and fibrillation of femoral articular cartilage on knee joint mechanics-a 3D finite element analysis. , 2012, Journal of biomechanics.

[18]  M. Knight,et al.  Cell mechanics, structure, and function are regulated by the stiffness of the three-dimensional microenvironment. , 2012, Biophysical journal.

[19]  J. Urban,et al.  Present perspectives on cartilage and chondrocyte mechanobiology. , 2000, Biorheology.

[20]  Farshid Guilak,et al.  Three-dimensional finite element modeling of pericellular matrix and cell mechanics in the nucleus pulposus of the intervertebral disk based on in situ morphology , 2011, Biomechanics and modeling in mechanobiology.

[21]  A Shirazi-Adl,et al.  A fibril-network-reinforced biphasic model of cartilage in unconfined compression. , 1999, Journal of biomechanical engineering.

[22]  F. Guilak,et al.  Transfer of macroscale tissue strain to microscale cell regions in the deformed meniscus. , 2008, Biophysical journal.

[23]  Gerard A Ateshian,et al.  Equivalence between short-time biphasic and incompressible elastic material responses. , 2007, Journal of biomechanical engineering.

[24]  Benjamin J. Ellis,et al.  FEBio: finite elements for biomechanics. , 2012, Journal of biomechanical engineering.

[25]  W. Herzog,et al.  Mechanical behaviour of in-situ chondrocytes subjected to different loading rates: a finite element study , 2012, Biomechanics and Modeling in Mechanobiology.

[26]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[27]  V. Kouznetsova,et al.  Multi-scale second-order computational homogenization of multi-phase materials : a nested finite element solution strategy , 2004 .

[28]  V. G. Kouznetsova,et al.  Multi-scale computational homogenization: Trends and challenges , 2010, J. Comput. Appl. Math..

[29]  C. Spearman The proof and measurement of association between two things. , 2015, International journal of epidemiology.

[30]  E. Nauman,et al.  Multiscale strain analysis of tissue equivalents using a custom-designed biaxial testing device. , 2012, Biophysical journal.

[31]  A A Goldsmith,et al.  Application of finite elements to the stress analysis of articular cartilage. , 1996, Medical engineering & physics.

[32]  G A Ateshian,et al.  Experimental verification and theoretical prediction of cartilage interstitial fluid pressurization at an impermeable contact interface in confined compression. , 1998, Journal of biomechanics.

[33]  Jason P. Halloran,et al.  Multiscale Mechanics of Articular Cartilage: Potentials and Challenges of Coupling Musculoskeletal, Joint, and Microscale Computational Models , 2012, Annals of Biomedical Engineering.

[34]  Dan L. Bader,et al.  Anisotropic, Three-Dimensional Deformation of Single Attached Cells Under Compression , 2004, Annals of Biomedical Engineering.

[35]  Farshid Guilak,et al.  The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. , 2005, Acta biomaterialia.

[36]  V. Mow,et al.  The mechanical environment of the chondrocyte: a biphasic finite element model of cell-matrix interactions in articular cartilage. , 2000, Journal of biomechanics.

[37]  M. Schwartz Integrins and extracellular matrix in mechanotransduction. , 2010, Cold Spring Harbor perspectives in biology.