Abstract The intervertebral disc is a complex structure that experiences multiaxial stresses regularly. Disc failure through herniation is a common cause of lower back pain, which causes reduced mobility and debilitating pain, resulting in heavy socioeconomic burdens. Unfortunately, herniation etiology is not well understood, partially due to challenges in replicating herniation in vitro. Previous studies suggest that flexion elevated risks of herniation. Thus, the objective of this study was to use a multiscale and multiphasic finite element model to evaluate the risk of failure under torque- or muscle-driven flexion. Models were developed to represent torque-driven flexion with the instantaneous center of rotation (ICR) located on the disc, and the more physiologically representative muscle-driven flexion with the ICR located anterior of the disc. Model predictions highlighted disparate disc mechanics regarding bulk deformation, stress-bearing mechanisms, and intradiscal stress–strain distributions. Specifically, failure was predicted to initiate at the bone-disc boundary under torque-driven flexion, which may explain why endplate junction failure, instead of herniation, has been the more common failure mode observed in vitro. By contrast, failure was predicted to initiate in the posterolateral annulus fibrosus under muscle-driven flexion, resulting in consistent herniation. Our findings also suggested that muscle-driven flexion combined with axial compression could be sufficient for provoking herniation in vitro and in silico. In conclusion, this study provided a computational framework for designing in vitro testing protocols that can advance the assessment of disc failure behavior and the performance of engineered disc implants.
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A Robust Multiscale and Multiphasic Structure-Based Modeling Framework for the Intervertebral Disc
A comprehensive understanding of multiscale and multiphasic intervertebral disc mechanics is crucial for designing advanced tissue engineered structures aiming to recapitulate native tissue behavior. The bovine caudal disc is a commonly used human disc analog due to its availability, large disc height and area, and similarities in biochemical and mechanical properties to the human disc. Because of challenges in directly measuring subtissue-level mechanics, such as in situ fiber mechanics, finite element models have been widely employed in spinal biomechanics research. However, many previous models use homogenization theory and describe each model element as a homogenized combination of fibers and the extrafibrillar matrix while ignoring the role of water content or osmotic behavior. Thus, these models are limited in their ability in investigating subtissue-level mechanics and stress-bearing mechanisms through fluid pressure. The objective of this study was to develop and validate a structure-based bovine caudal disc model, and to evaluate multiscale and multiphasic intervertebral disc mechanics under different loading conditions and with degeneration. The structure-based model was developed based on native disc structure, where fibers and matrix in the annulus fibrosus were described as distinct materials occupying separate volumes. Model parameters were directly obtained from experimental studies without calibration. Under the multiscale validation framework, the model was validated across the joint-, tissue-, and subtissue-levels. Our model accurately predicted multiscale disc responses for 15 of 16 cases, emphasizing the accuracy of the model, as well as the effectiveness and robustness of the multiscale structure-based modeling-validation framework. The model also demonstrated the rim as a weak link for disc failure, highlighting the importance of keeping the cartilage endplate intact when evaluating disc failure mechanisms in vitro . Importantly, results from this study elucidated important fluid-based load-bearing mechanisms and fiber-matrix interactions that are important for understanding disease progression and regeneration in intervertebral discs. In conclusion, the methods presented in this study can be used in conjunction with experimental work to simultaneously investigate disc joint-, tissue-, and subtissue-level mechanics with degeneration, disease, and injury.
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- Award ID(s):
- 1751212
- NSF-PAR ID:
- 10323640
- Date Published:
- Journal Name:
- Frontiers in Bioengineering and Biotechnology
- Volume:
- 9
- ISSN:
- 2296-4185
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)A comprehensive understanding of biological tissue mechanics is crucial for designing engineered tissues that aim to recapitulate native tissue behavior. Tensile mechanics of many fiber-reinforced tissues have been shown to depend on specimen geometry, which makes it challenging to compare data between studies. In this study, a validated multiscale, structure-based finite element model was used to evaluate the effect of specimen geometry on multiscale annulus fibrosus tensile mechanics through a fiber engagement analysis. The relationships between specimen geometry and modulus, Poisson’s ratio, tissue stress–strain distributions, and fiber reorientation behaviors were investigated at both tissue and sub-tissue levels. It was observed that annulus fibrosus tissue level tensile properties and stress transmission mechanisms were dependent on specimen geometry. The model also demonstrated that the contribution of fiber–matrix interactions to tissue mechanical response was specimen size- and orientation- dependent. The results of this study reinforce the benefits of structure-based finite element modeling in studies investigating multiscale tissue mechanics. This approach also provides guidelines for developing optimal combined computational-experimental study designs for investigating fiber-reinforced biological tissue mechanics. Additionally, findings from this study help explain the geometry dependence of annulus fibrosus tensile mechanics previously reported in the literature, providing a more fundamental and comprehensive understanding of tissue mechanical behavior. In conclusion, the methods presented here can be used in conjunction with experimental tissue level data to simultaneously investigate tissue and sub-tissue scale mechanics, which is important as the field of soft tissue biomechanics advances toward studies that focus on diminishing length scales.more » « less
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Background Water content is a key parameter for simulating tissue swelling and nutrient diffusion. Accurately measuring water content throughout the intervertebral disc (NP = nucleus pulposus; AF = annulus fibrosus) is important for developing patient‐specific models. Water content is measured using destructive techniques, Quantitative MRI has been used to estimate water content and detect early degeneration, but it is dependent on scan parameters, concentration of free water molecules, and fiber architecture.
Purpose To directly measure disc‐tissue water content using quantitative MRI and compare MRI‐based measurements with biochemical assays, and to quantify changes in disc geometry due to compression.
Study Type Basic science, controlled.
Specimen Twenty bone‐disc‐bone motion segments from skeletally mature bovines.
Field Strength/Sequence 7T/3D fast low angle shot (FLASH) pulse sequence and a T2rapid imaging with refocused echoes (RARE) sequence.
Assessment Disc volumes, NP and AF volumetric water content, and T2relaxation times were measured through MRI; NP and AF tissue gravimetric water content, mass density, and glycosaminoglycan content were measured through a biochemical assay.
Statistical Tests Correlations between MRI‐based measurement and biochemical composition were evaluated using Pearson's linear regression.
Results Mechanical dehydration resulted in a decrease in disc volume by up to 20% and a decrease in disc height by up to 35%. Direct water content measurements for the NP was achieved by normalizing MRI‐based spin density by NP mass density (1.10 ± 0.03 g/cm3). However, the same approach underestimated water content in the AF by ~10%, which may be due to a higher concentration of collagen fibers and bound water molecules.
Data Conclusion Spin density or spin density normalized by mass density to estimate NP and AF water content was more accurate than correlations between water content and relaxation times. Mechanical dehydration decreased disc volume and disc height, and increased maximum cross‐sectional area.
Level of Evidence Technical Efficacy Stage J. Magn. Reson. Imaging 2020;52:1152–1162.
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Abstract Intervertebral disc research has sought to develop a deeper understanding of spine biomechanics, the complex relationship between disc health and back pain, and the mechanisms of spinal injury and repair. To do so, many researchers have focused on characterizing tissue-level properties of the disc, where the roles of tissue subcomponents can be more systematically investigated. Unfortunately, experimental challenges often limit the ability to measure important disc tissue- and subtissue-level behaviors, including fiber–matrix interactions, transient nutrient and electrolyte transport, and damage propagation. Numerous theoretical and numerical modeling frameworks have been introduced to explain, complement, guide, and optimize experimental research efforts. The synergy of experimental and computational work has significantly advanced the field, and these two aspects have continued to develop independently and jointly. Meanwhile, the relationship between experimental and computational work has become increasingly complex and interdependent. This has made it difficult to interpret and compare results between experimental and computational studies, as well as between solely computational studies. This paper seeks to explore issues of model translatability, robustness, and efficient study design, and to propose and motivate potential future directions for experimental, computational, and combined tissue-level investigations of the intervertebral disc.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fbioe.2021.685799
