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BACKGROUND AND OBJECTIVE: The annulus fibrosus is an essential part of the intervertebral disc, critical for its structural integrity. Mechanical deterioration in this component can lead to complete disc failure, particularly through tears development, with radial tears being the most common. These tears are often the result of both mechanical and biological factors. This study aims to numerically investigate the mechanisms of radial failure in the annulus tissue, taking into account the mechanical and age-dependent biological damage origins. A newly developed microstructure-based model was upgraded to predict damage evolution in the different annulus regions. METHODS: The study employs a computational model to predict mechanical failures in various annulus regions, using experimental data for comparison. The model incorporates age-dependent microstructural changes to evaluate the effects of biological aging on the mechanical behavior. It specifically includes a detailed analysis of the temporal changes in circumferential rigidity and failure strain of the annulus. RESULTS: The model demonstrated a strong ability to replicate the experimental responses of the different annulus regions to failure. It revealed that age-related microstructural changes significantly impact the rigidity and failure response of the annulus, particularly in the posterior regions and as well the anterior inner side. These changes increase susceptibility to rupture with aging. A correlation was also observed between the composition of collagen fibers, water content, and the annulus transversal response in both radial and axial directions. CONCLUSION: The findings challenge previous assumptions, showing that age-dependent microstructural changes have a notable effect on the annulus mechanical properties. The computational model closely aligns with experimental observations, underscoring the determinant role of oriented collagen fibers in radial failure. This study enhances the understanding of annulus failure and provides a foundation for further research on the impact of aging on disc mechanical integrity and failure.

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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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The determinant role of the annulus fibrosus interlamellar zones in the intervertebral disc transversal and volumetric responses and hence on their corresponding three-dimensional conducts have been only revealed and appreciated recently. Their consideration in disc modeling strategies has been proven to be essential for the reproduction of correct local strain and displacement fields inside the disc especially in the unconstrained directions of the disc. In addition, these zones are known to be the starting areas of annulus fibrosus circumferential tears and disc delamination failure mode, which is often judged as one of the most dangerous disc failure modes that could evolve with time leading to disc hernia. For this latter reason, the main goal of the current contribution is to incorporate physically for the first time, the interlamellar zones, at the scale of a complete human lumbar intervertebral disc, in order to allow a correct local vision and replication of the different lamellar-interlamellar interactions and an identification of the interlamellar critical zones. By means of a fully tridimensional chemo-viscoelastic constitutive model, which we implemented into a finite element code, the physical, mechanical and chemical contribution of the interlamellar zones is added to the disc. The chemical-induced volumetric response is accounted by the model for both the interlamellar zones and the lamellae using experimentally-based fluid kinetics. Computational simulations are performed and critically discussed upon different simple and complex physiological movements. The disc core and the interlamellar zones are numerically accessed, allowing the observation of the displacement and shear strain fields that are compared to direct MRI experiments from the literature. Important conclusions about the correct lamellar-interlamellar-nucleus interactions are provided thanks to the developed model. The critical interlamellar spots with the highest delamination potentials are defined, analyzed and related to the local kinetics and microstructure.

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BACKGROUND AND OBJECTIVE: The human body soft tissues are hierarchic structures interacting in a complex manner with the surrounding biochemical environment. The loss of soft tissues functionality with age leads to more vulnerability regarding to the external mechanical loadings and increases the risk of injuries. As a main example of the human body soft tissues, the intervertebral disc mechanical response evolution with age is explored. Although the age-dependence of the intervertebral disc microstructure is a well-known feature, no noticeable age effect on the disc stiffness is evidenced in the in-vitro experimental studies of the literature. So, if the disc intrinsic mechanics remains constant, how to explain the correlation of disc degeneration and disc functionality loss with age. METHODS: A microstructure-based modeling approach was developed to assess in-silico the aging-sensitive mechanics of human intervertebral disc. The model considers the relationship between stress/volumetric macro-response and microstructure along with effective age effects acting at the lamellar and multi-lamellar scales. The stress-stretch and transversal responses of the different disc regions were computed for various age groups (13-18, 36, 58, 69 and 82 years old) and their evolution with age was studied. RESULTS: While matching with in-vitro experimental data, the predicted stiffness was found to increase while passing from adolescent young discs to mature older discs and then to remain almost constant for the rest of life. Important age-related changes in the disc transversal behavior were also predicted affecting the flexibility of the disc, changing its volumetric behavior, and modifying its dimensions. CONCLUSION: The developed approach was found able to bring new conclusions about age-dependent mechanical properties including regional dependency. The disc mechanics in terms of rigidity, radial and axial transversal responses were found to alter going from adolescent to middle age where the disc reaches a certain maturity. After reaching maturity, the mechanical properties undergo very slight changes until becoming almost constant with age.

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Establishing accurate structure-property relationships for intervertebral disc annulus fibrosus tissue is a fundamental task for a reliable computer simulation of the human spine but needs excessive theoretical-numerical-experimental works. The difficulty emanates from multiaxiality and anisotropy of the tissue response along with regional dependency of a complex hierarchic structure interacting with the surrounding environment. We present a new and simple hybrid microstructure-based experimental/modeling strategy allowing adaptation of animal disc model to human one. The trans-species strategy requires solely the basic knowledge of the uniaxial circumferential response of two different animal disc regions to predict the multiaxial response of any human disc region. This work demonstrates for the first time the determining role of the interlamellar matrix connecting the fibers-reinforced lamellae in the disc multiaxial response. Our approach shows encouraging multiaxial predictive capabilities making it a promising tool for human spine long-term prediction.

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STUDY DESIGN: Osmoviscoelastic behavior of cyclically loaded cervical intervertebral disc. OBJECTIVE: The aim of this study was to evaluate in vitro the effects of physiologic compressive cyclic loading on the viscoelastic properties of cervical intervertebral disc and, examine how the osmoviscoelastic coupling affects time-dependent recovery of these properties following a long period of unloading. SUMMARY OF BACKGROUND DATA: The human neck supports repetitive loadings during daily activities and recovery of disc mechanics is essential for normal mechanical function. However, the response of cervical intervertebral disc to cyclic loading is still not very well defined. Moreover, how loading history conditions could affect the time-dependent recovery is still unclear. METHODS: Ten thousand cycles of compressive loading, with different magnitudes and saline concentrations of the surrounding fluid bath, are applied to 8 motion segments (composed by 2 adjacent vertebrae and the intervening disc) extracted from the cervical spines of mature sheep. Subsequently, specimens are hydrated during 18 hours of unloading. The viscoelastic disc responses, after cyclic loading and recovery phase, are characterized by relaxation tests. RESULTS: Viscoelastic behaviors are significantly altered following large number of cyclic loads. Moreover, after 18-hour recovery period in saline solution at reference concentration (0.15 mol/L), relaxation behaviors were fully restored. Nonetheless, full recovery is not obtained whether the concentration of the surrounding fluid, that is, hypo-, iso-, or hyper-osmotic conditions. CONCLUSION: Cyclic loading effects and full recovery of viscoelastic behavior after hydration at iso-osmotic condition (0.15 mol/L) are governed by osmotic attraction of fluid content in the disc due to imbalance between the external load and the swelling pressure of the disc. After removal of the load, the disc recovers its viscoelastic properties following period of rest. Nevertheless, the viscoelastic recovery is a chemically activated process and its dependency on saline concentration is governed by fluid flow due to imbalance of ions between the disc tissues and the surrounding fluid. LEVEL OF EVIDENCE: 3.

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The annulus fibrosus of the intervertebral disc exhibits an unusual transversal behavior for which a constitutive representation that considers as well regional effect, chemical sensitivity and time-dependency has not yet been developed, and it is hence the aim of the present contribution. A physically-based model is proposed by introducing a free energy function that takes into account the actual disc annulus structure in relation with the surrounding biochemical environment. The response is assumed to be dominated by the viscoelastic contribution of the extracellular matrix, the elastic contribution of the oriented collagen fibers and the osmo-induced volumetric contribution of the internal fluid content variation. The regional dependence of the disc annulus response due to variation in fibers content/orientation allows a micromechanical treatment of the soft tissue. A finite element model of the annulus specimen is designed while taking into consideration the 'interlamellar' ground substance zone between lamellae of the layered soft tissue. The kinetics is designed using full-field strain measurements performed on specimens extracted from two disc annulus regions and tested under different osmotic conditions. The time-dependency of the tissue response is reported on stress-free volumetric changes, on hysteretic stress and transversal strains during quasi-static stretching at different strain-rates and on their temporal changes during an interrupted stretching. Considering the effective contributions of the internal fluid transfer and the extracellular matrix viscosity, the microstructure-based chemo-mechanical model is found able to successfully reproduce the significant features of the macro-response and the unusual transversal behavior including the strong regional dependency from inner to outer parts of the disc: Poisson's ratio lesser than 0 (auxetic) in lamellae plane, higher than 0.5 in fibers plane, and their temporal changes towards usual values (between 0 and 0.5) at chemo-mechanical equilibrium. The underlying time-dependent mechanisms occurring in the tissue are analyzed via the local numerical fields and important insights about the effective role of the interlamellar zone are revealed for the different disc localizations. STATEMENT OF SIGNIFICANCE: The structural complexity of the annulus fibrosus has only been appreciated through recent experimental contributions and a constitutive representation that considers as well regional effect, chemical sensitivity and time-dependency of the unusual transversal behavior has not yet been developed. Here, a microstructure-based chemo-viscoelastic model is developed to highlight the interlamellar-induced time-dependent response by means of a two-scale strategy. The model provides important insights about the origin of the time-dependent phenomena in disc annulus along with regional dependency, essential for understanding disc functionality.

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