Abstract
There is an increasing demand to develop predictive medicine through the creation of predictive models and digital twins of the different body organs. To obtain accurate predictions, real local microstructure, morphology changes and their accompanying physiological degenerative effects must be taken into account. In this article, we present a numerical model to estimate the long-term aging effect on the human intervertebral disc response by means of a microstructure-based mechanistic approach. It allows to monitor in-silico the variations in disc geometry and local mechanical fields induced by age-dependent long-term microstructure changes. Both lamellar and interlamellar zones of the disc annulus fibrosus are constitutively represented by considering the main underlying microstructure features in terms of proteoglycans network viscoelasticity, collagen network elasticity (along with content and orientation) and chemical-induced fluid transfer. With age, a noticeable increase in shear strain is especially observed in the posterior and lateral posterior regions of the annulus which is in correlation with the high vulnerability of elderly people to back problems and posterior disc hernia. Important insights about the relation between age-dependent microstructure features, disc mechanics and disc damage are revealed using the present approach. These numerical observations are hardly obtainable using current experimental technologies which makes our numerical tool useful for patient-specific long-term predictions.
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Andersson, G. B. Epidemiology of low back pain. Acta Orthop. Scand. 281:28–31, 1998.
Balzani, D., P. Neff, J. Schroder, and G. A. Holzapfel. A polyconvex framework for soft biological tissues. Adjustment to experimental data. Int. J. Solids Struct. 43:6052–6070, 2006.
Bergstrom, J. S., and M. C. Boyce. Constitutive modeling of the large strain time-dependent behavior of elastomers. J. Mech. Phys. Solids. 46:931–954, 1998.
Breivik, H., B. Collett, V. Ventafridda, R. Cohen, and D. Gallacher. Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur. J. Pain. 10:287–333, 2006.
Brickley-Parsons, D., and M. J. Glimcher. Is the chemistry of collagen in intervertebral discs an expression of Wolff’s Law? A study of the human lumbar spine. Spine. 9:148–163, 1984.
Cantournet, S., M. C. Boyce, and A. H. Tsou. Micromechanics and macromechanics of carbon nanotube-enhanced elastomers. J. Mech. Phys. Solids. 55:1321–1339, 2007.
Cortes, D. H., W. M. Han, L. J. Smith, and D. M. Elliott. Mechanical properties of the extra-fibrillar matrix of human annulus fibrosus are location and age dependent. J. Orthop. Res. 31:1725–1732, 2013.
Costi, J. J., I. A. Stokes, M. Gardner-Morse, J. P. Laible, H. M. Scoffone, and J. C. Iatridis. Direct measurement of intervertebral disc maximum shear strain in six degrees of freedom: motions that place disc tissue at risk of injury. J. Biomech. 40:2457–2466, 2007.
del Palomar, A. P., B. Calvo, and M. Doblare. An accurate finite element model of the cervical spine under quasi-static loading. J. Biomech. 41:523–531, 2008.
Derrouiche, A., F. Zaïri, and F. Zaïri. A chemo-mechanical model for osmo-inelastic effects in the annulus fibrosus. Biomech. Model. Mechanobiol. 18:1773–1790, 2019.
Derrouiche, A., A. Karoui, F. Zaïri, J. Ismail, Z. Qu, M. Chaabane, and F. Zaïri. The two Poisson’s ratios in annulus fibrosus: relation with the osmo-inelastic features. Mech. Soft Mater. 2:1, 2020.
Du, Y., S. Tavana, T. Rahman, N. Baxan, U. N. Hansen, and N. Newell. Sensitivity of intervertebral disc finite element models to internal geometric and non-geometric parameters. Front. Bioeng. Biotechnol. 9:509, 2021.
Ebara, S., J. C. Iatridis, L. A. Setton, R. J. Foster, V. C. Mow, and M. Weidenbaum. Tensile properties of nondegenerate human lumbar anulus fibrosus. Spine. 21:452–461, 1996.
Eberlein, R., G. Holzapfel, and M. Fröhlich. Multi-segment FEA of the human lumbar spine including the heterogeneity of the annulus fibrosus. Comput. Mech. 34:147–163, 2004.
Ehlers, W., N. Karajan, and B. Markert. An extended biphasic model for charged hydrated tissues with application to the intervertebral disc. Biomech. Model. Mechanobiol. 8:233–251, 2009.
Elliott, D. M., and L. A. Setton. Anisotropic and inhomogeneous tensile behavior of the human anulus fibrosus: experimental measurement and material model predictions. J. Biomech. Eng. 123:256–263, 2001.
Gent, A. N. A new constitutive relation for rubber. Rubber Chem. Technol. 69:59–61, 1996.
Ghezelbash, F., A. H. Eskandari, A. Shirazi-Adl, M. Kazempour, J. Tavakoli, M. Baghani, and J. J. Costi. Modeling of human intervertebral disc annulus fibrosus with complex multi-fiber networks. Acta Biomater. 123:208–221, 2021.
Gurtin, M. E., and L. Anand. The decomposition F=FeFp, material symmetry, and plastic irrotationality for solids that are isotropic-viscoplastic or amorphous. Int. J. Plast. 21:1686–1719, 2005.
Holzapfel, G. A., and T. C. Gasser. A viscoelastic model for fiber-reinforced composites at finite strains: continuum basis, computational aspects and applications. Comput. Methods Appl. Mech. Eng. 190:4379–4403, 2001.
Holzapfel, G. A., C. A. J. Schulze-Bauer, G. Feigl, and P. Regitnig. Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech. Model. Mechanobiol. 3:125–140, 2005.
Iatridis, J. C., and I. ap Gwynn. Mechanisms for mechanical damage in the intervertebral disc annulus fibrosus. J. Biomech. 37:1165–1175, 2004.
Iatridis, J. C., J. J. MacLean, M. O’Brien, and I. A. Stokes. Measurements of proteoglycan and water content distribution in human lumbar intervertebral discs. Spine. 32:1493–1497, 2007.
Jaramillo, H. E., L. Gomez, and J. J. Garcia. A finite element model of the L4-L5-S1 human spine segment including the heterogeneity and anisotropy of the discs. Acta Bioeng. Biomech. 17:15–24, 2015.
Kandil, K., F. Zaïri, A. Derrouiche, T. Messager, and F. Zaïri. Interlamellar-induced time-dependent response of intervertebral disc annulus: a microstructure-based chemoviscoelastic model. Acta Biomater. 100:75–91, 2019.
Kandil, K., F. Zaïri, T. Messager, and F. Zaïri. Interlamellar matrix governs human annulus fibrosus multiaxial behavior. Sci. Rep. 10:19292, 2020.
Kandil, K., F. Zaïri, T. Messager, and F. Zaïri. A microstructure-based modeling approach to assess aging-sensitive mechanics of human intervertebral disc. Comput. Methods Programs Biomed. 200:105890, 2021.
Kandil, K., F. Zaïri, T. Messager, and F. Zaïri. A microstructure-based model for a full lamellar–interlamellar displacement and shear strain mapping inside human intervertebral disc core. Comput. Biol. Med. 135:104629, 2021.
Koeller, W., F. Funke, and F. Hartmann. Biomechanical behaviour of human intervertebral discs subjected to long lasting axial loading. Biorheology. 21:675–686, 1984.
Markert, B., W. Ehlers, and N. Karajan. A general polyconvex strain energy function for fiber-reinforced materials. Proc. Appl. Math. Mech. 5:245–246, 2005.
O’Connell, G. D., S. Sen, and D. M. Elliott. Human annulus fibrosus material properties from biaxial testing and constitutive modeling are altered with degeneration. Biomech. Model. Mechanobiol. 11:493–503, 2012.
Osti, O. L., B. Vernon-Roberts, R. Moore, and R. D. Fraser. Annular tears and disc degeneration in the lumbar spine: a post-mortem study of 135 discs. J. Bone Jt. Surg. 74:678–682, 1992.
Parkkola, R., and M. Kormano. Lumbar disc and back muscle degeneration on MRI: correlation to age and body mass. J. Spinal Disord. 5:86–92, 1992.
Renner, S. M., R. N. Natarajan, A. G. Patwardhan, R. M. Havey, L. I. Voronov, B. Y. Guo, G. B. J. Andersson, and H. S. An. Novel model to analyze the effect of a large compressive follower pre-load on range of motions in a lumbar spine. J. Biomech. 40:1326–1332, 2007.
Rubin, D. I. Epidemiology and risk factors for spine pain. Neurol. Clin. 25:353–371, 2007.
Skaggs, D. L., M. Weidenbaum, J. C. Iatridis, A. Ratcliffe, and V. C. Mow. Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine. 19:1310–1319, 1994.
Tamoud, A., F. Zaïri, A. Mesbah, and F. Zaïri. Modeling multiaxial damage regional variation in human annulus fibrosus. Acta Biomater. 136:375–388, 2021.
Tamoud, A., F. Zaïri, A. Mesbah, and F. Zaïri. A microstructure-based model for time-dependent mechanics of multi-layered soft tissues and its application to intervertebral disc annulus. Meccanica. 56:585–606, 2021.
Tamoud, A., F. Zaïri, A. Mesbah, and F. Zaïri. A multiscale and multiaxial model for anisotropic damage and failure of human annulus fibrosus. Int. J. Mech. Sci. 205:106558, 2021.
Tavakoli, J., and J. J. Costi. New findings confirm the viscoelastic behaviour of the inter-lamellar matrix of the disc annulus fibrosus in radial and circumferential directions of loading. Acta Biomater. 71:411–419, 2018.
Tavakoli, J., D. M. Elliott, and J. J. Costi. Structure and mechanical function of the interlamellar matrix of the annulus fibrosus in the disc. J. Orthop. Res. 34:1307–1315, 2016.
Tavakoli, J., D. M. Elliott, and J. J. Costi. The ultra-structural organization of the elastic network in the intra- and inter-lamellar matrix of the intervertebral disc. Acta Biomater. 58:269–277, 2017.
Twomey, L., and J. Taylor. Age changes in lumbar intervertebral discs. Acta Orthop. Scand. 56:496–499, 1985.
van Loon, R., J. M. Huyghe, M. W. Wijlaars, and F. P. T. Baaijens. 3D FE implementation of an incompressible quadriphasic mixture model. Int. J. Numer. Methods Eng. 57:1243–1258, 2003.
Vernon-Roberts, B., R. J. Moore, and R. D. Fraser. The natural history of age-related disc degeneration: the pathology and sequelae of tears. Spine. 32:2797–2804, 2007.
Videman, T., S. Sarna, M. C. Battie, S. Koskinen, K. Gill, H. Paananen, and L. Gibbons. The long-term effect of physical loading and exercise lifestyles on back-related symptoms, disability, and spinal pathology among men. Spine. 20:699–709, 1995.
Vo, N. V., R. A. Hartman, P. R. Patil, M. V. Risbud, D. Kletsas, J. C. Iatridis, J. A. Hoyland, C. L. Le Maitre, G. A. Sowa, and J. D. Kang. Molecular mechanisms of biological aging in intervertebral discs. J. Orthop. Res. 34:1289–1306, 2016.
Wang, S., W. M. Park, H. R. Gadikota, J. Miao, Y. H. Kim, K. B. Wood, and G. Li. A combined numerical and experimental technique for estimation of the forces and moments in the lumbar intervertebral disc. Comput. Methods Biomech. Biomed. Eng. 16:1278–1286, 2013.
Wills, C. R., A. Malandrino, M. M. van Rijsbergen, D. Lacroix, K. Ito, and J. Noailly. Simulating the sensitivity of cell nutritive environment to composition changes within the intervertebral disc. J. Mech. Phys. Solids. 90:108–123, 2016.
Wilson, W., C. C. van Donkelar, and J. M. Huyghe. A comparison between mechano-electrochemical and biphasic swelling theories for soft hydrated tissues. J. Biomech. Eng. 127:158–165, 2005.
Zhou, C., T. Cha, W. Wang, R. Guo, and G. Li. Investigation of alterations in the lumbar disc biomechanics at the adjacent segments after spinal fusion using a combined in vivo and in silico approach. Ann. Biomed. Eng. 49:601–616, 2021.
Zhu, Q., X. Gao, and W. Gu. Temporal changes of mechanical signals and extracellular composition in human intervertebral disc during degenerative progression. J. Biomech. 47:3734–3743, 2014.
Zhu, Q., X. Gao, C. Chen, W. Gu, and M. D. Brown. Effect of intervertebral disc degeneration on mechanical and electric signals at the interface between disc and vertebra. J. Biomech.104:109756, 2020.
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Appendix A
Appendix A
In the continuum mechanics framework, the deformation gradient tensor \({\mathbf{F}} = {{\partial {\varvec{x}}} \mathord{\left/ {\vphantom {{\partial {\varvec{x}}} {\partial {\varvec{X}}}}} \right. \kern-0pt} {\partial {\varvec{X}}}}\) maps a material point from its initial position \({\varvec{X}}\) to the current position \({\varvec{x}}\). The time derivative is \({\dot{\mathbf{F}}} = {\mathbf{LF}}\) in which \({\mathbf{L}} = {{\partial {\varvec{v}}} \mathord{\left/ {\vphantom {{\partial {\varvec{v}}} {\partial {\varvec{x}}}}} \right. \kern-0pt} {\partial {\varvec{x}}}}\) is the spatial velocity gradient with \({\varvec{v}} = {{\partial {\varvec{x}}} \mathord{\left/ {\vphantom {{\partial {\varvec{x}}} {\partial t}}} \right. \kern-0pt} {\partial t}}\). Using the conceptual sequence of configurations, the deformation gradient tensor \({\mathbf{F}}\) can be decomposed via multiplicative forms:
where \({\mathbf{F}}_{{{\text{mech}}}}\) is the mechanical part related to the stress-producing contribution, in turn multiplicatively decomposed into an elastic part \({\mathbf{F}}_{{{\text{mech}}}}^{e}\) and a viscous part \({\mathbf{F}}_{{{\text{mech}}}}^{v}\), and \({\mathbf{F}}_{{{\text{chem}}}} = J^{{{1 \mathord{\left/ {\vphantom {1 3}} \right. \kern-0pt} 3}}} {\mathbf{I}}\) is the chemical-induced part related to the volumetric expansion in which the term \({\mathbf{I}}\) is the identity tensor and \(J = \det {\mathbf{F}}_{{{\text{chem}}}} > 0\) is the Jacobian.
The spatial velocity gradient \({\mathbf{L}}\) is described by:
in which \({\mathbf{L}}_{{{\text{mech}}}}\) is the stress-producing mechanical part, in turn decomposed into an elastic part \({\mathbf{L}}_{{{\text{mech}}}}^{e}\) and a viscous part \({\mathbf{L}}_{{{\text{mech}}}}^{v}\), and \({\mathbf{L}}_{{{\text{chem}}}}\) is the stress-free chemical-induced volumetric part.
The viscous spatial velocity gradient \({\mathbf{L}}_{{{\text{mech}}}}^{v}\) may be decomposed as the sum of symmetric and skew-symmetric parts:
in which \({\mathbf{D}}\) is the stretching rate (symmetric part) and \({\mathbf{W}}\) is the spin (skew-symmetric part):
It is assumed that the inelastic flow is irrotational,19 i.e. \({\mathbf{W}}_{{{\text{mech}}}}^{v} = {\mathbf{0}}\). The viscous deformation gradient \({\mathbf{F}}_{{{\text{mech}}}}^{v}\) is then extracted from:
The elastic component \({\mathbf{F}}_{{{\text{mech}}}}^{e} = {\mathbf{F}}_{{{\text{mech}}}} {\mathbf{F}}_{{{\text{mech}}}}^{{v^{ - 1} }}\) is then computed.
The tensor \({\mathbf{D}}_{{{\text{mech}}}}^{v}\) defining the specificity of the model is defined by the following general flow rule:
in which \(\dot{\gamma }_{{\text{v}}}\) is the accumulated viscous strain rate and \({\mathbf{N}}_{{\text{v}}}\) is the direction tensor of viscous flow aligned with the viscous Kirchhoff stress tensor \({{\varvec{\uptau}}}_{{\text{v}}}\).
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Kandil, K., Zaïri, F. & Zaïri, F. A Microstructure-Based Mechanistic Approach to Detect Degeneration Effects on Potential Damage Zones and Morphology of Young and Old Human Intervertebral Discs. Ann Biomed Eng 51, 1747–1758 (2023). https://doi.org/10.1007/s10439-023-03179-0
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DOI: https://doi.org/10.1007/s10439-023-03179-0