Towards Patient-Specific Computational Modelling of Articular Cartilage on the Basis of Advanced Multiparametric MRI Techniques

Cartilage degeneration is associated with tissue softening and represents the hallmark change of osteoarthritis. Advanced quantitative Magnetic Resonance Imaging (qMRI) techniques allow the assessment of subtle tissue changes not only of structure and morphology but also of composition. Yet, the relation between qMRI parameters on the one hand and microstructure, composition and the resulting functional tissue properties on the other hand remain to be defined. To this end, a Finite-Element framework was developed based on an anisotropic constitutive model of cartilage informed by sample-specific multiparametric qMRI maps, obtained for eight osteochondral samples on a clinical 3.0 T MRI scanner. For reference, the same samples were subjected to confined compression tests to evaluate stiffness and compressibility. Moreover, the Mankin score as an indicator of histological tissue degeneration was determined. The constitutive model was optimized against the resulting stress responses and informed solely by the sample-specific qMRI parameter maps. Thereby, the biomechanical properties of individual samples could be captured with good-to-excellent accuracy (mean R2 [square of Pearson’s correlation coefficient]: 0.966, range [min, max]: 0.904, 0.993; mean Ω [relative approximated error]: 33%, range [min, max]: 20%, 47%). Thus, advanced qMRI techniques may be complemented by the developed computational model of cartilage to comprehensively evaluate the functional dimension of non-invasively obtained imaging biomarkers. Thereby, cartilage degeneration can be perspectively evaluated in the context of imaging and biomechanics.

[1]  Stéphane Cotin,et al.  Real-Time Error Control for Surgical Simulation , 2016, IEEE Transactions on Biomedical Engineering.

[2]  C P Neu,et al.  Functional imaging in OA: role of imaging in the evaluation of tissue biomechanics. , 2014, Osteoarthritis and cartilage.

[3]  Sion Glyn-Jones,et al.  Non-invasive imaging of cartilage in early osteoarthritis. , 2013, The bone & joint journal.

[4]  W M Lai,et al.  Fluid transport and mechanical properties of articular cartilage: a review. , 1984, Journal of biomechanics.

[5]  J. M. Huyghe,et al.  Depth-dependent Compressive Equilibrium Properties of Articular Cartilage Explained by its Composition , 2007, Biomechanics and modeling in mechanobiology.

[6]  Serdar Göktepe,et al.  A micro-macro approach to rubber-like materials—Part I: the non-affine micro-sphere model of rubber elasticity , 2004 .

[7]  Sam F. Edwards,et al.  The theory of rubber elasticity , 1976, Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences.

[8]  Z. Suo,et al.  Inhomogeneous swelling of a gel in equilibrium with a solvent and mechanical load , 2009 .

[9]  P. Babyn,et al.  Osteoarthritis staging: comparison between magnetic resonance imaging, gross pathology and histopathology in the rhesus macaque. , 1995, Osteoarthritis and cartilage.

[10]  K. Fishbein,et al.  Sensitivity and specificity of univariate MRI analysis of experimentally degraded cartilage under clinical imaging conditions , 2015, Journal of magnetic resonance imaging : JMRI.

[11]  Johannes Thüring,et al.  T2 MR imaging vs. computational modeling of human articular cartilage tissue functionality. , 2017, Journal of the mechanical behavior of biomedical materials.

[12]  Luyao Cai,et al.  In vivo articular cartilage deformation: noninvasive quantification of intratissue strain during joint contact in the human knee , 2016, Scientific Reports.

[13]  B. Min,et al.  An in vitro comparative study of T2 and T2* mappings of human articular cartilage at 3-Tesla MRI using histology as the standard of reference , 2014, Skeletal Radiology.

[14]  Guigang Zhang,et al.  Deep Learning , 2016, Int. J. Semantic Comput..

[15]  T. Smith,et al.  Systematic review and meta-analysis of the reliability and discriminative validity of cartilage compositional MRI in knee osteoarthritis. , 2018, Osteoarthritis and cartilage.

[16]  A. E. Ehret,et al.  A polyconvex anisotropic strain–energy function for soft collagenous tissues , 2006, Biomechanics and modeling in mechanobiology.

[17]  C. Kuhl,et al.  Multiparametric MRI and Computational Modelling in the Assessment of Human Articular Cartilage Properties: A Comprehensive Approach , 2018, BioMed research international.

[18]  Mikhail Itskov,et al.  A polyconvex hyperelastic model for fiber-reinforced materials in application to soft tissues , 2007 .

[19]  Rüdiger Krauspe,et al.  T2* mapping for articular cartilage assessment: principles, current applications, and future prospects , 2014, Skeletal Radiology.

[20]  Mikhail Itskov,et al.  Tensor Algebra and Tensor Analysis for Engineers , 2009, Mathematical Engineering.

[21]  Edoardo Mazza,et al.  Inverse poroelasticity as a fundamental mechanism in biomechanics and mechanobiology , 2017, Nature Communications.

[22]  C. V. van Donkelaar,et al.  Relative contribution of articular cartilage’s constitutive components to load support depending on strain rate , 2016, Biomechanics and modeling in mechanobiology.

[23]  Steven R Goldring,et al.  Early knee osteoarthritis , 2015, RMD Open.

[24]  T. Vincent,et al.  Mechanoadaptation: articular cartilage through thick and thin , 2018, The Journal of physiology.

[25]  R. E. Outerbridge THE ETIOLOGY OF CHONDROMALACIA PATELLAE , 1961 .

[26]  Robert Schmitt,et al.  Polarization-sensitive optical coherence tomography-based imaging, parameterization, and quantification of human cartilage degeneration , 2016, Journal of biomedical optics.

[27]  Kim Henriksen,et al.  Which elements are involved in reversible and irreversible cartilage degradation in osteoarthritis? , 2010, Rheumatology International.

[28]  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.

[29]  Applications to Continuum Mechanics , 2015 .

[30]  K. Hjelle,et al.  Articular cartilage defects in 1,000 knee arthroscopies. , 2002, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[31]  S. Saarakkala,et al.  Imaging of Osteoarthritic Human Articular Cartilage using Fourier Transform Infrared Microspectroscopy Combined with Multivariate and Univariate Analysis , 2016, Scientific Reports.

[32]  B. M. Fulk MATH , 1992 .

[33]  M Tingart,et al.  Non-invasive T1ρ mapping of the human cartilage response to loading and unloading. , 2017, Osteoarthritis and cartilage.

[34]  H. Dorfman,et al.  Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. , 1971, The Journal of bone and joint surgery. American volume.

[35]  C. Kuhl,et al.  Ex vivo quantitative multiparametric MRI mapping of human meniscus degeneration , 2016, Skeletal Radiology.

[36]  Herve Delingette,et al.  Real-Time Elastic Deformations of Soft Tissues for Surgery Simulation , 1999, IEEE Trans. Vis. Comput. Graph..

[37]  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.

[38]  C. Kuhl,et al.  Functional in situ assessment of human articular cartilage using MRI: a whole-knee joint loading device , 2017, Biomechanics and modeling in mechanobiology.

[39]  S. Klein,et al.  Is T1ρ Mapping an Alternative to Delayed Gadolinium-enhanced MR Imaging of Cartilage in the Assessment of Sulphated Glycosaminoglycan Content in Human Osteoarthritic Knees? An in Vivo Validation Study. , 2016, Radiology.

[40]  Christiane Kuhl,et al.  Functional MR Imaging Mapping of Human Articular Cartilage Response to Loading. , 2017, Radiology.

[41]  T. Nishii,et al.  Comparison of load responsiveness of cartilage T1rho and T2 in porcine knee joints: an experimental loading MRI study. , 2015, Osteoarthritis and cartilage.

[42]  Jaynelle F Stichler,et al.  A comprehensive approach. , 2004, Marketing health services.

[43]  K. R. Clarke,et al.  A Method Of Linking Multivariate Community Structure To Environmental Variables , 1993 .

[44]  J M Huyghe,et al.  A composition-based cartilage model for the assessment of compositional changes during cartilage damage and adaptation. , 2006, Osteoarthritis and cartilage.

[45]  H J Helminen,et al.  Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. , 2002, Journal of biomechanics.

[46]  Thomas M. Link,et al.  Prestructural cartilage assessment using MRI , 2017, Journal of magnetic resonance imaging : JMRI.

[47]  R. Thuillier,et al.  Impact of Hypothermia and Oxygen Deprivation on the Cytoskeleton in Organ Preservation Models , 2018, BioMed research international.

[48]  A. Benninghoff,et al.  Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[49]  A. Guermazi,et al.  Compositional MRI techniques for evaluation of cartilage degeneration in osteoarthritis. , 2015, Osteoarthritis and cartilage.

[50]  C. Neu Functional imaging in OA: role of imaging in the evaluation of tissue biomechanics , 2022 .

[51]  Gerhard A. Holzapfel,et al.  Modeling the propagation of arterial dissection , 2006 .

[52]  Christiane Kuhl,et al.  Quantitative OCT and MRI biomarkers for the differentiation of cartilage degeneration , 2016, Skeletal Radiology.

[53]  P. Flory,et al.  Thermodynamic relations for high elastic materials , 1961 .

[54]  Alfio Grillo,et al.  Elasticity and permeability of porous fibre-reinforced materials under large deformations , 2012 .

[55]  T. Quinn,et al.  Anisotropic hydraulic permeability in compressed articular cartilage. , 2006, Journal of biomechanics.

[56]  R. C. Macridis A review , 1963 .

[57]  Ali Guermazi,et al.  Advances in imaging of osteoarthritis and cartilage. , 2011, Radiology.