Stepwise reduction of functional spinal structures increase disc bulge and surface strains

Previous studies postulated that an axial compression of lumbar intervertebral discs causes a complex strain pattern on the annulus. This pattern is not fully understood, since most studies measured only the uniaxial ultimate tensile strain of the annulus. The aim of this study was to investigate surface strains and their relation to disc bulging. This work was extended to study some defects that are relevant for the intermediate process of finite element modeling. Six specimens (L2-3) with a median age of 51 years were utilized for this in vitro study. Specimens were loaded with pure moments (2.5-7.5Nm) in the principal directions. The anatomy was subsequently reduced in three steps: (1) ligamentous and bony posterior structures, (2) anterior and posterior ligaments and (3) nucleus. Measured were ranges of motion, three-dimensional disc bulging and surface strains of the outer annulus. Lateral bending showed the largest axial strains (9.7%) for intact specimens, which increased to 15.1% after the removal of posterior structures. Disc bulging was largest in flexion with 1.56mm, which increased to 2.06mm after step (1). Defect (2) caused that flexion yielded the largest axial strains with 22.6% and 2.17mm of bulging. We could also determine a constriction effect of these ligaments. Nucleotomy did not essentially increase anterior disc bulging in flexion, but inward disc bulging increased by 0.55mm, in extension. Due to the increase in the complexity of finite element models, it is difficult to obtain data from the literature for validation purposes. This study presents new data, which assist in the development of such models.     

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.     

The micromechanical role of the annulus fibrosus components under physiological loading of the lumbar spine

To date, studies that have investigated the kinematics of spinal motion segments have largely focused on the contributions that the spinal ligaments play in the resultant motion patterns. However, the specific roles played by intervertebral disk components, in particular the annulus fibrosus, with respect to global motion is not well understood in spite of the relatively large literature base with respect to the local ex vivo mechanical properties of the tissue. The primary objective of this study was to implement the nonlinear and orthotropic mechanical behavior of the annulus fibrosus in a finite element model of an L4/L5 functional spinal unit in the form of a strain energy potential where the individual mechanical contributions of the ground substance and fibers were explicitly defined. The model was validated biomechanically under pure moment loading to ensure that the individual role of each soft tissue structure during load bearing was consistent throughout the physiologically relevant loading range. The fibrous network of the annulus was found to play critical roles in limiting the magnitude of the neutral zone and determining the stiffness of the elastic zone. Under flexion, lateral bending, and axial rotation, the collagen fibers were observed to bear the majority of the load applied to the annulus fibrosus, especially in radially peripheral regions where disk bulging occurred. For the first time, our data explicitly demonstrate that the exact fiber recruitment sequence is critically important for establishing the range of motion and neutral zone magnitudes of lumbar spinal motion segments.     

Effect of overload on changes in mechanical and structural properties of the annulus fibrosus of the intervertebral disc

The research focussed on analysing structural and mechanical properties in the intervertebral disc (IVD), caused by long-term cyclic loading. Spinal motion segments were divided into two groups: the control (C), and the group in which it was analysed the impact of posterior column in the load-bearing system of the spine—specimens with intact posterior column (IPC) and without posterior column (WPC). To evaluate the structural and mechanical changes, the specimens were tested with simulation of 100,000 compression-flexion load cycles after which it was performed macroscopic analysis. Mechanical properties of the annulus fibrosis (AF) from the anterior and posterior regions of the IVD were tested at the uniaxial tension test. The stiffness coefficient values were statistically 32% higher in the WPC group (110 N/mm) than in the IPC (79 N/mm). The dynamics of increase in this parameter does not correspond with the course of decrease in height loss. WPC segments revealed clear structural changes that mainly involve the posterior regions of the IVD (bulging and delamination with the effect of separation of collagen fibre bundles). Pathological changes also caused decreases in the value of stress in the AF. The greatest changes in the stress value about group C (7.43 ± 4.49 MPa) were observed in the front part of the fibrous ring, where this value was for IPC 4.49 ± 4.78 MPa and WPC 2.56 ± 1.01 MPa. The research indicates that the applied load model allows simulating damage that occurs in pathological IVD. And the posterior column’s presence affects this change’s dynamics, structural and mechanical properties of AF.

     

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.     

Influence of single-level lumbar degenerative disc disease on the behavior of the adjacent segments—A finite element model study

The current study investigated mechanical predictors for the development of adjacent disc degeneration. A 3-D finite element model of a lumbar spine was modified to simulate two grades of degeneration at the L4–L5 disc. Degeneration was modeled by changes in geometry and material properties. All models were subjected to follower preloads of 800 N and moment loads in the three principal directions of motion using a hybrid protocol. Degeneration caused changes in the loading and motion patterns of the segments above and below the degenerated disc. At the level (L3–L4) above the degenerated disc, the motion increased due to moderate degeneration by 21% under lateral bending, 26% under axial rotation and 28% under flexion/extension. At the level (L5-S1) below the degenerated disc, motion increased only during lateral bending by 20% due to moderate degeneration. Both the L3–L4 and L5-S1 segment showed a monotonic increase in both the maximum von Mises stress and shear stress in the annulus as degeneration progressed for all loading directions, expect extension at L3–L4. The most significant increase in stress was observed at the L5-S1 level during axial rotation with nearly a ten-fold increase in the maximum shear stress and 103% increase in the maximum von Mises stress. The L5-S1 segment also showed a progressive increase in facet contact force for all loading directions with degeneration. Nucleus pressure did not increase significantly for any loading direction at either the caudal or cephalic adjacent segment. Results suggest that single-level degeneration can increase the risk for injury at the adjacent levels.     

Degeneration affects the fiber reorientation of human annulus fibrosus under tensile load

The angled, lamellar structure of the annulus fibrosus is integral to its load-bearing function. Reorientation of this fiber structure with applied load may contribute to nonlinear mechanical behavior and to large increases in tensile modulus. Fiber reorientation has not yet been quantified for loaded non-degenerated and degenerated annulus fibrosus tissue. The objective of this study was to measure fiber reorientation and mechanical properties (toe- and linear-region modulus, transition strain, and Poisson's ratio) of loaded outer annulus fibrosus tissue using a new application of FFT image processing techniques. This method was validated for quantification of annulus fiber reorientation during loading in this study. We hypothesized that annulus fibrosus fibers would reorient under circumferential tensile load, and that fiber reorientation would be affine. Additionally, we hypothesized that degeneration would affect fiber reorientation, toe-region modulus and Poisson's ratio. Annulus fibrosus fibers were found to reorient toward the loading direction, and degeneration significantly decreased fiber reorientation (the fiber reorientation parameter, m(FFT)=-1.70 degrees /% strain for non-degenerated and -0.95 degrees /% strain for degenerated tissue). Toe-region modulus was significantly correlated with age (r=0.6). Paired t-tests showed no significant difference in the fiber reorientation parameter calculated experimentally with that calculated using an affine prediction. Thus, an affine prediction is a good approximation of fiber reorientation. The findings of this study add to the understanding of overall disc mechanical behavior and degeneration.     

Mechanical damage to the intervertebral disc annulus fibrosus subjected to tensile loading

Damage of the annulus fibrosus is implicated in common spinal pathologies. The objective of this study was to obtain a quantitative relationship between both the number of cycles and the magnitude of tensile strain resulting in damage to the annulus fibrosus. Four rectangular tensile specimens oriented in the circumferential direction were harvested from the outer annulus of 8 bovine caudal discs (n = 32) and subjected to one of four tensile testing protocols: (i) ultimate tensile strain (UTS) test; (ii) baseline cyclic test with 4 series of 400 cycles of baseline cyclic loading (peak strain = 20% UTS); (iii & iv) acute and fatigue damage cyclic tests consisting of 4 x 400 cycles of baseline cyclic loading with intermittent loading to 1 and 100 cycles, respectively, with peak tensile strain of 40%, 60%, and 80% UTS. Normalized peak stress for all mechanically loaded specimens was reduced from 0.89 to 0.11 of the baseline control levels, and depended on the magnitude of damaging strain and number of cycles at that damaging strain. Baseline, acute, and fatigue protocols resulted in permanent deformation of 3.5%, 6.7% and 9.6% elongation, respectively. Damage to the laminate structure of the annulus in the absence of biochemical activity in this study was assessed using histology, transmission electron microscopy, and biochemical measurements and was most likely a result of separation of annulus layers (i.e., delamination). Permanent elongation and stress reduction in the annulus may manifest in the motion segment as sub-catastrophic damage including increased neutral zone, disc bulging, and loss of nucleus pulposus pressure. The preparation of rectangular tensile strip specimens required cutting of collagen fibers and may influence absolute values of results, however, it is not expected to affect the comparisons between loading groups or dose-response reported.     

An accurate finite element model of the cervical spine under quasi-static loading

Cervical disc injury due to impact has been observed in clinical and biomechanical investigations; however, there is a lack of data that helps to elucidate the mechanisms of disc injury during these collisions. Therefore, it is necessary to understand the behavior of the cervical spine under different types of loading situations. A three dimensional finite element (FE) model for the multi-level cervical spine segment (C0-C7) was developed using computed tomography (CT) data and applied to study the internal stresses and strains of the intervertebral discs under quasi-static loading conditions. The intervertebral discs were treated as nonlinear, anisotropic and incompressible subjected to large deformations. The model accuracy was validated by comparing it with previously published experimental and numerical results for different movements. It was shown that the use of a fiber reinforced model to describe the behavior of the annulus of the discs would predict higher maximum shear strains than an isotropic one, being therefore important the use of complex constitutive models in order to be able to detect the appearance of injured zones, since those strains and stresses are supposed to be related with damage to soft tissues. Several movements were analyzed: flexion, extension and axial rotation, obtaining that the maximum shear stresses in the disc were higher for a flexo-extension movement.     

Collagen fibre orientation in the annulus fibrosus of intervertebral disc during bending and torsion measured by x-ray diffraction

X-ray diffraction has been used to measure the orientation of the collagen fibres in the ventral annulus fibrosus of intact L1/2 rabbit intervertebral disc during in vitro bending and torsion. Fibres are tilted with respect to the axis of the spine. As predicted by theory, fibre tilt decreases in those regions of the annulus which are stretched by bending but increases in the slackened regions. Good agreement with the quantitative predictions of bending theory was obtained in three of the six series of experiments, the predicted trend being found in all six. Tilt direction alternates in successive lamellae of the annulus. When discs were subjected to both clockwise and anticlockwise torsion of 5°, the two families of titled fibres reoriented in the expected directions.     

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.     

The influence of exogenous cross-linking and compressive creep loading on intradiscal pressure

This study involves a biomechanical evaluation of a prospective injectable treatment for degenerative discs. The high osmolarity of the non-degenerated nucleus pulposus attracts water contributing to the hydrostatic behavior of the tissue. This intradiscal pressure is known to drop as fluid is exuded from the matrix due to compressive loading. The objective of this study was to compare the changes in intradiscal pressure in control and genipin cross-linked intervertebral discs. Thirty bovine lumbar motion segments were randomly divided into a phosphate-buffered saline control group and a 0.33% genipin group and soaked at room temperature for 2 days. A needle pressure sensor was held in the center of the disc while short-term and static creep compressive loads were applied. The control group demonstrated a 25% higher average intradiscal pressure compared to genipin-treated discs under 750 N compressive load (p=0.029). Depressurization during static compressive creep was 56% higher in the control than in the genipin group (p=0.014). These results suggest cross-linking induced changes in the poroelastic properties of the involved tissues affected the mechanics of compressive load support in the disc with lower levels of nucleus pressure, a corresponding decrease in the elastic expansion of the annulus, and an increased axial compressive loading of the inner and outer annulus tissues. It is possible that concurrent changes in hydraulic permeability and proteoglycan retention known to be associated with genipin cross-linking were also contributors to poroelastic changes. Reduction of peak pressures and moderation of pressure fluctuations could be beneficial relative to discogenic pain.     

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.     

Stepwise reduction of functional spinal structures increase range of motion and change lordosis angle

Many investigators have performed studies on specific defect situations or determined the contribution on isolated structures. Investigating the contribution of functional structures requires obtaining the kinematic response directly on spinal segments. The purpose of this study was to quantify the function of anatomical components on lumbar segments for different loading magnitudes. Eight spinal segments (L4-5) with a median age of 52 years (ranging from 38 to 59 years) and a low degree of disc degeneration were utilized for the in vitro testing. Specimens were mounted in a custom-built spine tester and loaded with pure moments (1-10 N m) to move within three anatomical planes at a loading rate of 1.0 degrees /s. Anatomy was successively reduced by: ligaments, facet capsules, joints and nucleus. Data were evaluated for range of motion, neutral zone and lordosis angle. Transection of posterior ligaments predominantly increased specimen flexion for all bending moments applied. Supraspinous ligament also indicated to resist in extension slightly, whereas the facet capsules did not. Facet joints contributed to axial rotation, but not in lateral bending. The anterior longitudinal ligament was found to slightly resist in axial rotation, but strongly in extension. Nucleotomy caused largest increase of all movements. The unloaded posture of the specimens changed after ligament dissection, indicating ligament pretension. The region of lumbar spine is interesting for finite element (FE) simulation due to the high evidence of disc degeneration and injuries. This study may help to understand the function of specific anatomical structures and assists in FE model calibration. We suggest to start a calibration procedure for such models with the smallest functional structure (annulus) and to cumulatively add further structures.     

Neural arch load-bearing in old and degenerated spines

We validate a technique for measuring neural arch load-bearing in cadaveric spines, and use it to test the hypothesis that such load-bearing rises to high levels in old and degenerated spines. Fifty-nine cadaveric lumbar motion segments, aged 19-92 yr, were subjected to compressive creep loading to reduce intervertebral disc water content and height to in vivo levels. The distribution of compressive "stress" within the disc was then measured by pulling a miniature pressure transducer, side-mounted in a 1.3mm-diameter needle, along its mid-sagittal diameter. During these measurements, the motion segment was subjected to a compressive load of 2 kN, and positioned in 2 degrees of extension to simulate erect standing. Measurements of compressive "stress" were integrated over disc area, and this force subtracted from the applied 2 kN to give the force resisted by the neural arch. An empirical calibration factor was applied to normalise results from each disc to values obtained under conditions when all of the compressive force could be assumed to pass through the disc. Disc degeneration was graded macroscopically on a scale of 1-4. Validation tests showed that calculated values of disc loading were proportional to actual applied load (r(2)>0.96) and predicted it with errors of 2-8%. Neural arch load-bearing in non-degenerated specimens was generally less than 20%, but averaged 49% for specimens aged over 70 yr. Multiple regression showed that neural arch load bearing (%)=14.4 x disc degeneration score+0.46 x age-35. These results indicate a substantial shift in vertebral load-bearing with increasing age and degeneration.     

Strain transfer in the annulus fibrosus under applied flexion

A detailed understanding of the anatomical and mechanical environment in the intervertebral disc at the scale of the cell is necessary for the design of tissue engineering repair strategies and to elucidate the role of mechanical factors in pathology. The objective of this study was to measure and compare the macroscale to microscale strains in the outer annulus fibrosus in various cellular regions of intact discs over a range of applied flexion. Macroscale strains were measured on the annulus fibrosus surface, and contrasted to in situ microscale strains using novel confocal microscopy techniques for dual labeling of the cell and the extracellular matrix. Fiber oriented surface strains were significantly higher than in situ fiber strains, which implies a mechanism of load redistribution that minimizes strain along the fibers. Non-uniformity of the strains and matrix distortion occurred immediately and most interestingly varied little with increase in flexion (3–16°), suggesting that inter-fiber shear is important in the initial stages of strain redistribution. Fiber oriented intercellular strains were significantly larger and compressive compared to in situ strains in other regions of the extracellular matrix indicating that the mechanical environment in this region may be unique. Further examination of the structural morphology in this pericellular region is needed to fully understand the pathway of strain transfer from the tissue to the cell. This study provides new knowledge on the complex in situ micro-mechanical environment of the annulus fibrosus that is essential to understanding the mechanobiological behavior of this tissue.     

Response analysis of the lumbar spine during regular daily activities—A finite element analysis

A non-linear poroelastic finite element model of the lumbar spine was developed to investigate spinal response during daily dynamic physiological activities. Swelling was simulated by imposing a boundary pore pressure of 0.25 MPa at all external surfaces. Partial saturation of the disc was introduced to circumvent the negative pressures otherwise computed upon unloading. The loading conditions represented a pre-conditioning full day followed by another day of loading: 8 h rest under a constant compressive load of 350 N, followed by 16 h loading phase under constant or cyclic compressive load varying in between 1000 and 1600 N. In addition, the effect of one or two short resting periods in the latter loading phase was studied.The model yielded fairly good agreement with in-vivo and in-vitro measurements. Taking the partial saturation of the disc into account, no negative pore pressures were generated during unloading and recovery phase. Recovery phase was faster than the loading period with equilibrium reached in only ～3 h. With time and during the day, the axial displacement, fluid loss, axial stress and disc radial strain increased whereas the pore pressure and disc collagen fiber strains decreased. The fluid pressurization and collagen fiber stiffening were noticeable early in the morning, which gave way to greater compression stresses and radial strains in the annulus bulk as time went by. The rest periods dampened foregoing differences between the early morning and late in the afternoon periods. The forgoing diurnal variations have profound effects on lumbar spine biomechanics and risk of injury.     

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.     

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.