Effect of collagen fibre orientation on intervertebral disc torsion mechanics

The intervertebral disc is a complex fibro-cartilaginous material, consisting of a pressurized nucleus pulposus surrounded by the annulus fibrosus, which has an angle-ply structure. Disc injury and degeneration are noted by significant changes in tissue structure and function, which significantly alters stress distribution and disc joint stiffness. Differences in fibre orientation are thought to contribute to changes in disc torsion mechanics. Therefore, the objective of this study was to evaluate the effect of collagen fibre orientation on internal disc mechanics under compression combined with axial rotation. We developed and validated a finite element model (FEM) to delineate changes in disc mechanics due to fibre orientation from differences in material properties. FEM simulations were performed with fibres oriented at \(\pm 30^{\circ }\) throughout the disc (uniform by region and fibre layer). The initial model was validated by published experimental results for two load conditions, including \(0.48\,\hbox {MPa}\) axial compression and \(10\,\hbox {Nm}\) axial rotation. Once validated, fibre orientation was rotated by \(4^{\circ }\) or \(8^{\circ }\) towards the horizontal plane, resulting in a decrease in disc joint torsional stiffness. Furthermore, we observed that axial rotation caused a sinusoidal change in disc height and radial bulge, which may be beneficial for nutrient transport. In conclusion, including anatomically relevant fibre angles in disc joint FEMs is important for understanding stress distribution throughout the disc and will be important for understanding potential causes for disc injury. Future models will include regional differences in fibre orientation to better represent the fibre architecture of the native disc.     

Three-dimensional inhomogeneous triphasic finite-element analysis of physical signals and solute transport in human intervertebral disc under axial compression

A 3D inhomogeneous finite-element model for charged hydrated soft tissues containing charged/uncharged solutes was developed and applied to analyze the mechanical, chemical, and electrical signals within the human intervertebral disc during an axial unconfined compression. The effects of tissue properties and boundary conditions on the physical signals and the transport of fluid and solute were investigated. The numerical simulation showed that, during disc compression, the fluid pressurization and the effective (von Misses) solid stress were more pronounced in the annulus fibrosus (AF) region near the interface between AF and nucleus pulposus (NP). In NP, the distributions of the fluid pressure, effective stress, and electrical potential were more uniform than those in AF. The electrical signals were very sensitive to fixed charge density. Changes in material properties of NP (water content, fixed charge density, and modulus) affected fluid pressure, electrical potential, effective stress, and solute transport in the disc. This study is important for understanding disc biomechanics, disc nutrition, and disc mechanobiology.     

Mechanisms for mechanical damage in the intervertebral disc annulus fibrosus

Intervertebral disc degeneration results in disorganization of the laminate structure of the annulus that may arise from mechanical microfailure. Failure mechanisms in the annulus were investigated using composite lamination theory and other analyses to calculate stresses in annulus layers, interlaminar shear stress, and the region of stress concentration around a fiber break. Scanning electron microscopy (SEM) was used to evaluate failure patterns in the annulus and evaluate novel structural features of the disc tissue. Stress concentrations in the annulus due to an isolated fiber break were localized to approximately 5 microm away from the break, and only considered a likely cause of annulus fibrosus failure (i.e., radial tears in the annulus) under extreme loading conditions or when collagen damage occurs over a relatively large region. Interlaminar shear stresses were calculated to be relatively large, to increase with layer thickness (as reported with degeneration), and were considered to be associated with propagation of circumferential tears in the annulus. SEM analysis of intervertebral disc annulus fibrosus tissue demonstrated a clear laminate structure, delamination, matrix cracking, and fiber failure. Novel structural features noted with SEM also included the presence of small tubules that appear to run along the length of collagen fibers in the annulus and a distinct collagenous structure representative of a pericellular matrix in the nucleus region.     

Statistical factorial analysis on the poroelastic material properties sensitivity of the lumbar intervertebral disc under compression,flexion and axial rotation

A statistical factorial analysis approach was conducted on a poroelastic finite element model of a lumbar intervertebral disc to analyse the influence of six material parameters (permeabilities of annulus, nucleus, trabecular vertebral bone, cartilage endplate and Young's moduli of annulus and nucleus) on the displacement, fluid pore pressure and velocity fields. Three different loading modes were investigated: compression, flexion and axial rotation. Parameters were varied considering low and high levels in agreement with values found in the literature for both healthy and degenerated lumbar discs. Results indicated that annulus stiffness and cartilage endplate permeability have a strong effect on the overall fluid- and solid-phase responses in all loading conditions studied. Nucleus stiffness showed its main relevance in compression while annulus permeability influenced mainly the annular pressure field. This study confirms the permeability's central role in biphasic modelling and highlights for the lumbar disc which experiments of material property characterization should be performed. Moreover, such sensitivity study gives important guidelines in poroelastic material modelling and finite element disc validation.     

Statistical factorial analysis on the material property sensitivity of the mechanical responses of the C4-C6 under compression, anterior and posterior shear

A systematic approach using factorial analysis was conducted on the C4-C6 finite element model to analyse the influence of six spinal components (cortical shell, vertebral body, posterior elements, endplate, disc annulus and disc nucleus) on the internal stresses and external biomechanical responses under compression, anterior and posterior shear. Results indicated that the material properties variation of the disc annulus has a significant influence on both the external biomechanical responses and internal stress of the disc annulus and its neighboring hard bones. The study reveals for the first time, the significant influence of the cancellous bone under compression, while variation in the cortical shell modulus has a high influence under anterior and posterior shear. The study also reveals that the effects of interaction between two main components are insignificant.     

Implantable MEMS compressive stress sensors: Design,fabrication and calibration with application to the disc annulus

Physiological stresses are fundamental to biomechanical testing, mechanobiological analyses, implant design, and tissue engineering. The purpose of this study was to design, fabricate, and evaluate compressive stress sensors packaged for extended, in vivo implantation in the annulus of the intervertebral disc. A commercial microelectromechanical systems (MEMS) pressure sensor die was selected as the active element for a custom stress sensor. The sensor die was modified and packaged to protect the electrical system from the biochemical and biomechanical environment. Completed sensors were calibrated under hydrostatic pressure and solid contact compression. Calibrations were performed before and after 8 weeks of in vivo implantation in a porcine disc. For the two reported sensors, stress and voltage were linearly correlated over a range of 0–1.8 MPa with less than 5% change in sensitivity. Sensitivity to solid contact stress was within 10% of that from hydrostatic pressure. In contrast to most previous studies, in which disc pressure was measured in the fluidic nucleus pulposus, these sensors may be used to measure in vivo dynamic compressive stresses in the annulus at magnitudes typical of the musculoskeletal system in a large animal over a relatively long post-operative time.     

Periostin is expressed by cells of the human and sand rat intervertebral discs

Abstract

Periostin, a matricellular protein in the fasciclin family, is expressed in tissues subjected to constant mechanical stress. Periostin modulates cell-to-extracellular matrix interactions and can bind to collagen, fibronectin, tenascin-C and several integrins. Our objective was to evaluate whether periostin is expressed in the human intervertebral disc. Immunohistochemical localization of periostin was carried out in tissue of human lumbar discs and lumbar discs of the sand rat (Psammomys obesus). Human discs also were examined for periostin gene expression. Immunohistochemical localization demonstrated periostin in the cytoplasm of annulus and nucleus cells, and occasionally in the surrounding pericellular and interterritorial extracellular matrix. Periostin distribution in the human disc was distinctive. Outer annulus contained the highest proportion of periostin-positive cells (88.8%), whereas inner annulus contained only 61.4%. The nucleus pulposus contained the fewest periostin-positive cells (18.5%). There was a significant negative correlation between the percentage of cells positive for periostin in the inner annulus and subject age. Periostin gene expression in the human disc also was confirmed using molecular microarray analysis. Because work by others has shown that periostin plays an important role in the biomechanical properties of other connective tissues (skin, tendon, heart valves), future research is needed to elucidate the role of periostin in disc, loading, aging and degeneration.     

Disc mechanics with trans-endplate partial nucleotomy are not fully restored following cyclic compressive loading and unloaded recovery

Mechanical function of the intervertebral disc is maintained through the interaction between the hydrated nucleus pulposus, the surrounding annulus fibrosus, and the superior and inferior endplates. In disc degeneration the normal transfer of load between disc substructures is compromised. The objective of this study was to explore the mechanical role of the nucleus pulposus in support of axial compressive loads over time. This was achieved by measuring the elastic slow ramp and viscoelastic stress-relaxation mechanical behaviors of cadaveric sheep motion segments before and after partial nucleotomy through the endplate (keeping the annulus fibrosus intact). Mechanics were evaluated at five conditions: Intact, intact after 10,000 cycles of compression, acutely after nucleotomy, following nucleotomy and 10,000 cycles of compression, and following unloaded recovery. Radiographs and magnetic resonance images were obtained to examine structure. Only the short time constant of the stress relaxation was altered due to nucleotomy. In contrast, cyclic loading resulted in significant and large changes to both the stiffness and stress relaxation behaviors. Moreover, the nucleotomy had little to no effect on the disc mechanics after cyclic loading, as there were no significant differences comparing mechanics after cyclic loading with or without the nucleotomy. Following unloaded recovery the mechanical changes that had occurred as a consequence of cyclic loading were restored, leaving only a sustained change in the short time constant due to the trans-endplate nucleotomy. Thus the swelling and redistribution of the remaining nucleus pulposus was not able to fully restore mechanical behaviors. This study reveals insights into the role of the nucleus pulposus in disc function, and provides new information toward the potential role of altered nucleus pulpous function in the degenerative cascade.     

Measurement of surface deformation of soft tissue

A method is described for measuring the surface shape and deformations of soft tissue in three dimensions. The method uses close range stereophotogrammetry to record the three-dimensional locations of miniature optical targets applied to the tissue surface. This has been applied to study of human lumbar intervertebral disc. Measurements of the strain along surface annular fibers have been made under varying loads. In this case the maximum expected errors are about 0.15 mm, which corresponds to a strain of less than 1%. Preliminary findings have differed from predictions made in published mathematical models for the disc in that they show very little strain of the annulus in compression loading, but confirm axial torsional loading as liable to produce mechanical disruption of the disc annulus.     

Osmosis and viscoelasticity both contribute to time-dependent behaviour of the intervertebral disc under compressive load: A caprine in vitro study

The mechanical behaviour of the intervertebral disc highly depends on the content and transport of interstitial fluid. It is unknown, however, to what extent the time-dependent behaviour can be attributed to osmosis. Here we investigate the effect of both mechanical and osmotic loading on water content, nucleus pressure and disc height. Eight goat intervertebral discs, immersed in physiological saline, were subjected to a compressive force with a pressure needle inserted in the nucleus. The loading protocol was: 10 N (6 h); 150 N (42 h); 10 N (24 h). Half-way the 150 N-phase (24 h), we eliminated the osmotic gradient by adding 26% poly-ethylene glycol to the surrounding fluid. For 62 additional discs, we determined the water content of both nucleus and annulus after 6, 24, 48, or 72 h. The compressive load was initially counterbalanced by the hydrostatic pressure in the nucleus. The load forced 4.3% of the water out of the nucleus, which reduced nucleus pressure by 44(±6)%. Reduction of the osmotic gradient disturbed the equilibrium disc height, and a significant loss of annulus water content was found. Remarkably, pressure and water content of the nucleus pulposus remained unchanged. This shows that annulus water content is important in the response to axial loading. After unloading, in the absence of an osmotic gradient, there was substantial viscoelastic recovery of 53(±11)% of the disc height, without a change in water content. However, for restoration of the nucleus pressure and for full restoration of disc height, restoration of the osmotic gradient was needed.     

Micromechanics of the human vertebral body for forward flexion

To provide mechanistic insight into the etiology of osteoporotic wedge fractures, we investigated the spatial distribution of tissue at the highest risk of initial failure within the human vertebral body for both forward flexion and uniform compression loading conditions. Micro-CT-based linear elastic finite element analysis was used to virtually load 22 human T9 vertebral bodies in either 5° of forward flexion or uniform compression; we also ran analyses replacing the simulated compliant disc (E=8 MPa) with stiff polymethylmethacrylate (PMMA, E=2500 MPa). As expected, we found that, compared to uniform compression, forward flexion increased the overall endplate axial load on the anterior half of the vertebra and shifted the spatial distribution of high-risk tissue within the vertebra towards the anterior aspect of the vertebral body. However, despite that shift, the high-risk tissue remained primarily within the central regions of the trabecular bone and endplates, and forward flexion only slightly altered the ratio of cortical-to-trabecular load sharing at the mid-vertebral level (mean±SD for n=22: 41.3±7.4% compression; 44.1±8.2% forward flexion). When the compliant disc was replaced with PMMA, the anterior shift of high-risk tissue was much more severe. We conclude that, for a compliant disc, a moderate degree of forward flexion does not appreciably alter the spatial distribution of stress within the vertebral body.     

Numerical analysis of the influence of nucleus pulposus removal on the biomechanical behavior of a lumbar motion segment

Nucleus replacement was deemed to have therapeutic potential for patients with intervertebral disc herniation. However, whether a patient would benefit from nucleus replacement is technically unclear. This study aimed to investigate the influence of nucleus pulposus (NP) removal on the biomechanical behavior of a lumbar motion segment and to further explore a computational method of biomechanical characteristics of NP removal, which can evaluate the mechanical stability of pulposus replacement. We, respectively, reconstructed three types of models for a mildly herniated disc and three types of models for a severely herniated disc based on a L4–L5 segment finite element model with computed tomography image data from a healthy adult. First, the NP was removed from the herniated disc models, and the biomechanical behavior of NP removal was simulated. Second, the NP cavities were filled with an experimental material (Poisson's ratio = 0.3; elastic modulus = 3 MPa), and the biomechanical behavior of pulposus replacement was simulated. The simulations were carried out under the five loadings of axial compression, flexion, lateral bending, extension, and axial rotation. The changes of the four biomechanical characteristics, i.e. the rotation degree, the maximum stress in the annulus fibrosus (AF), joint facet contact forces, and the maximum disc deformation, were computed for all models. Experimental results showed that the rotation range, the maximum AF stress, and joint facet contact forces increased, and the maximum disc deformation decreased after NP removal, while they changed in the opposite way after the nucleus cavities were filled with the experimental material.     

Region Specific Response of Intervertebral Disc Cells to Complex Dynamic Loading: An Organ Culture Study Using a Dynamic Torsion-Compression Bioreactor

The spine is routinely subjected to repetitive complex loading consisting of axial compression, torsion, flexion and extension. Mechanical loading is one of the important causes of spinal diseases, including disc herniation and disc degeneration. It is known that static and dynamic compression can lead to progressive disc degeneration, but little is known about the mechanobiology of the disc subjected to combined dynamic compression and torsion. Therefore, the purpose of this study was to compare the mechanobiology of the intervertebral disc when subjected to combined dynamic compression and axial torsion or pure dynamic compression or axial torsion using organ culture. We applied four different loading modalities [1. control: no loading (NL), 2. cyclic compression (CC), 3. cyclic torsion (CT), and 4. combined cyclic compression and torsion (CCT)] on bovine caudal disc explants using our custom made dynamic loading bioreactor for disc organ culture. Loads were applied for 8 h/day and continued for 14 days, all at a physiological magnitude and frequency. Our results provided strong evidence that complex loading induced a stronger degree of disc degeneration compared to one degree of freedom loading. In the CCT group, less than 10% nucleus pulposus (NP) cells survived the 14 days of loading, while cell viabilities were maintained above 70% in the NP of all the other three groups and in the annulus fibrosus (AF) of all the groups. Gene expression analysis revealed a strong up-regulation in matrix genes and matrix remodeling genes in the AF of the CCT group. Cell apoptotic activity and glycosaminoglycan content were also quantified but there were no statistically significant differences found. Cell morphology in the NP of the CCT was changed, as shown by histological evaluation. Our results stress the importance of complex loading on the initiation and progression of disc degeneration.     

Failure strength of the bovine caudal disc under internal hydrostatic pressure

The structure of the disc is both complex and inhomogeneous, and it functions as a successful load-bearing organ by virtue of the integration of its various structural regions. These same features also render it impossible to assess the failure strength of the disc from isolated tissue samples, which at best can only yield material properties. This study investigated the intrinsic failure strength of the intact bovine caudal disc under a simple mode of internal hydrostatic pressure. Using a hydraulic actuator, coloured hydrogel was injected under monitored pressure into the nucleus through a hollow screw insert which passed longitudinally through one of the attached vertebrae. Failure did not involve vertebra/endplate structures. Rather, failure of the disc annulus was indicated by the simultaneous manifestation of a sudden loss of gel pressure, a flood of gel colouration appearing in the outer annulus and audible fibrous tearing. A mean hydrostatic failure pressure of 18+/-3 MPa was observed which was approximated as a thick-wall hoop stress of 45+/-7 MPa. The experiment provides a measurement of the intrinsic strength of the disc using a method of internal hydrostatic loading which avoids any disruption of the complex architecture of the annular wall. Although the disc in vivo is subjected to a much more complex pattern of loading than is achieved using simple hydrostatic pressurization, this latter mode provides a useful tool for investigating alterations in intrinsic disc strength associated with prior loading history or degeneration.     

Effect of disc degeneration on the muscle recruitment pattern in upright posture: a computational analysis

Based on the sensor driving control mechanism model, the effect of disc degeneration on the trunk muscle recruitment (TMR) pattern was analysed in erect standing posture. A previously developed computational model was used for this analysis, with modifications incorporating the T12-L1 motion segment and additional muscle fascicles. To generate disc degeneration at three different levels (L3–L4, L4–L5, or L5–S1), the material properties of the ground matrix of the annulus and bulk modulus of the nucleus were reduced. The finite element method combined with an optimization technique was applied to calculate the muscle forces. Minimization of deviations in the averaged tensile stress in the annulus fibres at the outermost layer in the five discs was selected for muscle force calculations. The results indicated that the disc degeneration noticeably increased the activation of the superficial muscle (IT and R) even though there was no clear change in the longissimus thoracis. Unlike some of the superficial muscles, activation in the deep muscles (multifidus (ML, MS, MT), LL and Q) was decreased. The change in TMR pattern generated an intervertebral disc angle difference and nucleus pressure increased in the upper level. These differences are expected to be functional in that they reduce the stress at the degenerated disc by changing the muscle activation, which slows down the progress of disc degeneration.     

Relationship between streaming potential and compressive stress in bovine intervertebral tissue

The intervertebral disc is formed by the nucleus pulposus (NP) and annulus fibrosus (AF), and intervertebral tissue contains a large amount of negatively charged proteoglycan. When this tissue becomes deformed, a streaming potential is induced by liquid flow with positive ions. The anisotropic property of the AF tissue is caused by the structural anisotropy of the solid phase and the liquid phase flowing into the tissue with the streaming potential. This study investigated the relationship between the streaming potential and applied stress in bovine intervertebral tissue while focusing on the anisotropy and loading location. Column-shaped specimens, 5.5 mm in diameter and 3 mm thick, were prepared from the tissue of the AF, NP and the annulus–nucleus transition region (AN). The loading direction of each specimen was oriented in the spinal axial direction, as well as in the circumferential and radial directions of the spine considering the anisotropic properties of the AF tissue. The streaming potential changed linearly with stress in all specimens. The linear coefficients k_e of the relationship between stress and streaming potential depended on the extracted positions. These coefficients were not affected by the anisotropy of the AF tissue. In addition, these coefficients were lower in AF than in NP specimens. Except in the NP specimen, the k_e values were higher under faster compression rate conditions. In cyclic compression loading the streaming potential changed linearly with compressive stress, regardless of differences in the tissue and load frequency.     

Penetrating annulus fibrosus injuries affect dynamic compressive behaviors of the intervertebral disc via altered fluid flow: an analytical interpretation

Extensive experimental work on the effects of penetrating annular injuries indicated that large injuries impact axial compressive properties of small animal intervertebral discs, yet there is some disagreement regarding the sensitivity of mechanical tests to small injury sizes. In order to understand the mechanism of injury size sensitivity, this study proposed a simple one dimensional model coupling elastic deformations in the annulus with fluid flow into and out of the nucleus through both porous boundaries and through a penetrating annular injury. The model was evaluated numerically in dynamic compression with parameters obtained by fitting the solution to experimental stress-relaxation data. The model predicted low sensitivity of mechanical changes to injury diameter at both small and large sizes (as measured by low and high ratios of injury diameter to annulus thickness), with a narrow range of high sensitivity in between. The size at which axial mechanics were most sensitive to injury size (i.e., critical injury size) increased with loading frequency. This study provides a quantitative hypothetical model of how penetrating annulus fibrosus injuries in discs with a gelatinous nucleus pulposus may alter disc mechanics by changing nucleus pulposus fluid pressurization through introduction of a new fluid transport pathway though the annulus. This model also explains how puncture-induced biomechanical changes depend on both injury size and test protocol.