The Influence of Concordant Complex Posture and Loading Rate on Motion Segment Failure: A Mechanical and Microstructural Investigation.

STUDY DESIGN: Microstructural investigation of compression-induced herniation of a lumbar disc held in a concordant complex posture. OBJECTIVE: To explore the significance of loading rate in a highly asymmetric concordant posture, comparing the mechanisms of failure to an earlier study using a nonconcordant complex posture. SUMMARY OF BACKGROUND DATA: A recent study with a nonconcordant complex posture (turning in the opposite direction to that which the load is applied) demonstrated the vulnerability of the disc to loading that is borne by one set of oblique-counter oblique fiber sets in the alternating lamellae of the annulus, and aggravated by an elevated loading rate. Given the strain rate-dependent properties of the disc it might be expected that the outcome differs if the posture is reversed. METHODS: Forty-one motion segments from ovine 16 spines were split into two cohorts; adopting the previously employed low rate (40 mm/min) and surprise rate (400 mm/min) of loading. Both groups of damaged discs were then analyzed microstructurally. RESULTS: With the lower rate loading the concordant posture significantly reduced the load required to cause disc failure than earlier described for nonconcordant posture (6.9 vs. 8.4 kN), with more direct tears and alternate lamella damage extending to the anterior disc. Contrary to this result, with a surprise rate, the load at failure was significantly increased with the concordant posture (8.08 vs. 6.96 kN), although remaining significantly less than that from a simple flexed posture (9.6 kN). Analysis of the damage modes and postures suggest facet engagement plays a significant role. CONCLUSION: This study confirms that adding shear to the posture lowers the load at failure, and causes alternate lamella rupture. Load at failure in a complex posture is not determined by loading rate alone. Rather, the strain rate-dependent properties of the disc influence which elements of the system are brought into play. LEVEL OF EVIDENCE: N/A.

A Microstructural Investigation of Disc Disruption Induced by Low Frequency Cyclic Loading.

STUDY DESIGN: Microstructural investigation of low frequency cyclic loading and flexing of the lumbar disc. OBJECTIVE: To explore micro-level structural damage in motion segments subjected to low frequency repetitive loading and flexing at sub-acute loads. SUMMARY OF BACKGROUND DATA: Cumulative exposure to mechanical load has been implicated in low back pain and injury. The mechanical pathways by which cyclic loading physically affects spine tissues remain unclear, in part due to the absence of high quality microstructural evidence. METHODS: The study utilized seven intact ovine lumbar spines and from each spine one motion segment was used as a control, two others were cyclically loaded. Ten motion segments were subjected to 5000 cycles at 0.5 Hz with a peak load corresponding to ∼30% of that required to achieve failure. An additional small group of segments subjected to 10,000 or 30,000 cycles was similarly analyzed. Following chemical fixation and decalcification samples were cryosectioned along one of the oblique fiber angles and imaged in their fully hydrated state using differential interference contrast optical microscopy. Structural damage obtained from the images was organized into an algebraic shell for analysis. RESULTS: At 5000 cycles the disc damage was limited to inner wall distortions, evidence of stress concentrations at bridging-lamellae attachments, and small delaminations. The high-cycle discs tested exhibited significant mid-wall damage. There was no evidence of nuclear material being displaced. CONCLUSION: At this low frequency and without the application of sustained loading or a more severe loading regime, or maintaining a constant flexion with repetitive loading, it seems unlikely that actual nuclear migration occurs. It is possible that the inner-annular damage shown in the low dose group could disrupt pathways for nutrient diffusion leading to earlier cell death and matrix degradation, thus contributing to a cascade of degeneration. LEVEL OF EVIDENCE: N/A.

A more realistic disc herniation model incorporating compression, flexion and facet-constrained shear: a mechanical and microstructural analysis. Part II: high rate or 'surprise' loading.

PURPOSE: Part I of this study explored mechanisms of disc failure in a complex posture incorporating physiological amounts of flexion and shear at a loading rate considerably lower than likely to occur in a typical in vivo manual handling situation. Given the strain-rate-dependent mechanical properties of the heavily hydrated disc, loading rate will likely influence the mechanisms of disc failure. Part II investigates the mechanisms of failure in healthy discs subjected to surprise-rate compression while held in the same complex posture. METHODS: 37 motion segments from 13 healthy mature ovine lumbar spines were compressed in a complex posture intended to simulate the situation arising when bending and twisting while lifting a heavy object at a displacement rate of 400 mm/min. Seven of the 37 samples reached the predetermined displacement prior to a reduction in load and were classified as early stage failures, providing insight to initial areas of disc disruption. Both groups of damaged discs were then analysed microstructurally using light microscopy. RESULTS: The average failure load under high rate complex loading was 6.96 kN (STD 1.48 kN), significantly lower statistically than for low rate complex loading [8.42 kN (STD 1.22 kN)]. Also, unlike simple flexion or low rate complex loading, direct radial ruptures and non-continuous mid-wall tearing in the posterior and posterolateral regions were commonly accompanied by disruption extending to the lateral and anterior disc. CONCLUSION: This study has again shown that multiple modes of damage are common when compressing a segment in a complex posture, and the load bearing ability, already less than in a neutral or flexed posture, is further compromised with high rate complex loading.

A more realistic disc herniation model incorporating compression, flexion and facet-constrained shear: a mechanical and microstructural analysis. Part I: Low rate loading.

PURPOSE: To date, the mechanisms of disc failure have been explored at a microstructural level in relatively simple postures. However, in vivo the disc is known to be subjected to complex loading in compression, bending and shear, and the influence of these factors on the mechanisms of disc failure is yet to be described at a microstructural level. The purpose of this study was to provide a microstructural analysis of the mechanisms of failure in healthy discs subjected to compression while held in a complex posture incorporating physiological amounts of flexion and facet-constrained shear. METHODS: 30 motion segments from 10 healthy mature ovine lumbar spines were compressed in a complex posture intended to simulate the situation arising when bending and twisting while lifting a heavy object, and at a displacement rate of 40 mm/min. Nine of the 30 samples reached the predetermined displacement prior to a reduction in load and were classified as early-stage failures, providing insight into initial areas of disc disruption. Both groups of damaged discs were then analysed microstructurally using light microscopy. RESULTS: Complex postures significantly reduced the load required to cause disc failure than earlier described for flexed postures [8.42 kN (STD 1.22 kN) compared to 9.69 kN (STD 2.56 kN)] and resulted in a very different failure morphology to that observed in either simple flexion or direct compression, involving infiltration of nucleus material in a circuitous path to the annular periphery. CONCLUSION: The complex posture as used in this study significantly reduced the load required to cause disc failure, providing further evidence that asymmetric postures while lifting should be avoided if possible.

ISSLS Prize Winner: Vibration Really Does Disrupt the Disc: A Microanatomical Investigation.

STUDY DESIGN: Microstructural investigation of vibration-induced disruption of the flexed lumbar disc. OBJECTIVE: The aim of the study was to explore micro-level structural damage in motion segments subjected to vibration at subcritical peak loads. SUMMARY OF BACKGROUND DATA: Epidemiological evidence suggests that cumulative whole body vibration may damage the disc and thus play an important role in low back pain. In vitro investigations have produced herniations via cyclic loading (and cyclic with added vibrations as an exacerbating exposure), but offered only limited microstructural analysis. METHODS: Twenty-nine healthy mature ovine lumbar motion segments flexed 7° and subjected to vibration loading (1300 ±â€Š500 N) in a sinusoidal waveform at 5 Hz to simulate moderately severe physiologic exposure. Discs were tested either in the range of 20,000 to 48,000 cycles (medium dose) or 70,000 to 120,000 cycles (high dose). Damaged discs were analyzed microstructurally. RESULTS: There was no large drop in displacement over the duration of both vibration doses indicating an absence of catastrophic failure in all tests. The tested discs experienced internal damage that included delamination and disruption to the inner and mid-annular layers as well as diffuse tracking of nucleus material, and involved both the posterior and anterior regions. Less frequent tearing between the inner disc and endplate was also observed. Annular distortions also progressed into a more severe form of damage, which included intralamellar tearing and buckling and obvious strain distortion around the bridging elements within the annular wall. CONCLUSION: Vibration loading causes delamination and disruption of the inner and mid-annular layers and limited diffuse tracking of nucleus material. These subtle levels of disruption could play a significant role in initiating the degenerative cascade via micro-level disruption leading to cell death and altered nutrient pathways. LEVEL OF EVIDENCE: 5.

ISSLS Prize Winner: A Detailed Examination of the Elastic Network Leads to a New Understanding of Annulus Fibrosus Organization.

STUDY DESIGN: Investigation of the elastic network in disc annulus and its function. OBJECTIVE: To investigate the involvement of the elastic network in the structural interconnectivity of the annulus and to examine its possible mechanical role. SUMMARY OF BACKGROUND DATA: The lamellae of the disc are now known to consist of bundles of collagen fibers organized into compartments. There is strong interconnectivity between adjacent compartments and between adjacent lamellae, possibly aided by a translamellar bridging network, containing blood vessels. An elastic network exists across the disc annulus and is particularly dense between the lamellae, and forms crossing bridges within the lamellae. METHODS: Blocks of annulus taken from bovine caudal discs were studied in either their unloaded or radially stretched state then fixed and sectioned, and their structure analyzed optically using immunohistology. RESULTS: An elastic network enclosed the collagen compartments, connecting the compartments with each other and with the elastic network of adjacent lamellae, formed an integrated network across the annulus, linking it together. Stretching experiments demonstrated the mechanical interconnectivities of the elastic fibers and the collagen compartments. CONCLUSION: The annulus can be viewed as a modular structure organized into compartments of collagen bundles enclosed by an elastic sheath. The elastic network of these sheaths is interconnected mechanically across the entire annulus. This organization is also seen in the modular structure of tendon and muscle. The results provide a new understanding annulus structure and its interconnectivity, and contribute to fundamental structural information relevant to disc tissue engineering and mechanical modeling. LEVEL OF EVIDENCE: N/A.

A detailed microscopic examination of alterations in normal anular structure induced by mechanical destabilization in an ovine model of disc degeneration.

STUDY DESIGN: Microstructural investigation of anular structure. OBJECTIVE: To reveal the effect of mechanical destabilization on the anular architecture both locally and distantly. SUMMARY OF BACKGROUND DATA: Several longitudinal ovine-induced disc degeneration studies have documented degenerative changes in disc components using histologic, biomechanical, and biochemical approaches; however, changes in intervertebral disc (IVD) microstructure have largely remained neglected. In recent years, the use of structurally relevant section planes has improved our understanding of disc microstructure, including the presence of significant bridging structures radially linking the lamellae. It has been suggested that the translamellar cross-bridges offer a mechanism by which the anular wall can adaptively remodel itself in response to a changing biomechanical microenvironment. METHODS: IVDs harvested from lesion and sham-operated groups of Merino wethers were subjected to en face oblique and vertical sectioning. The macrostructural effect of the destabilization was examined in the vertically sectioned group with conventional histologic techniques. The second group was serially sectioned into 30-µm slices allowing a global examination of the anular microstructure in its fully hydrated state using a differential interference contrast microscope. RESULTS: The previously described induced disc degeneration in the mid-inner anulus fibrosus (AF) and a spontaneous repair process in the outer AF was confirmed. Increased translamellar bridging was observed contralaterally to the lesion in the mechanically destabilized IVD and development of atypical broad bridging elements in the outer lamellae. Structural alterations in the lamellar anchorages to the cartilaginous endplates in destabilized IVDs, including lamellar branching and discontinuities atypical of normal lamellar attachments were also observed. CONCLUSION: The present investigation has offered a glimpse of an anular wall apparently capable of remodeling in response to perturbations in its normal mechanical environment. The translamellar cross-bridges undergo adaptations in structure, in response to altered stresses locally at the anular defect site but also distantly in the contralateral AF in the destabilized disc. It is currently not known whether such changes in anular microarchitecture, however, predispose the anulus to further mechanical damage or have a stabilizing role to play in this structure.

How age influences unravelling morphology of annular lamellae - a study of interfibre cohesivity in the lumbar disc.

Although age- and degeneration-related changes in the morphology and biochemistry of the annulus fibrosus have been extensively reported, studies of tensile strength changes show only a weak correlation with maturity. Given that the disc is a tissue system in which significant levels of deformation occur with normal physiological loading, there may be structure-related properties that provide a better indicator of the influence of ageing on its function. This study is a morphological investigation of lamellar interfibre cohesivity with respect to maturity. Anterior segments of ovine lumbar discs in two age groups were cut at one of two section angles to generate intralamellar and interlamellar slices. These slices of hydrated annular tissue were subjected separately to microtensile and swelling forces, and examined using differential interference contrast microscopy. There were distinct differences in microstructural responses to transverse extension between the immature and mature intralamellar slices. The immature tissue exhibited a diffuse expansion of the array to form a fine fibrous net. In contrast, the mature tissue displayed a discontinuous expansion with the development of clefts and localized fibre buckling. A difference was also observed in the free-swelling response; the immature slices remained planar, whereas the cropped lamellar fibres in the mature slices exhibited a folded, buckled morphology. Morphological evidence from these experiments infers differences in fibre cohesivity between the immature and mature tissues, consistent with biochemical and histological studies. More extreme levels of deformation in the mature tissue could result in discontinuous opening of the fibrous arrays, which might have the potential to lead to cleft formation. These clefts may, in turn, provide micropaths through which nuclear material could extrude. Importantly, with many animal studies carried out on immature discs, the results here suggest that some caution is required with respect to extrapolating annular behaviour beyond this age group.

A microstructural investigation of intervertebral disc lamellar connectivity: detailed analysis of the translamellar bridges.

Little is known about the complex forces acting on the deformable multi-layered annulus at a microstructural level as the spine is compressed, flexed and twisted. The recently described translamellar bridging network radially linking many lamellae at discrete locations around the disc wall could be expected to play a significant biomechanical role. In this study, segments of annular wall that were sectioned at a range of angles (oblique, in-plane, sagittal and transverse) were examined using differential interference contrast microscopy to fully elucidate the fibrous detail of the translamellar bridging structures. Typically encompassing a width of 300-600 microm, translamellar bridging fibres proceed radially in the interbundle space within an individual lamella. Upon traversing the lamella, the bulk of these radial fibres bend through 90 degrees to merge with the fibres of the adjacent lamellae. The central fibres of this bridging system continue into the equivalent bridging structures in the adjacent lamellae. As well as exposing structural details that underpin the biomechanical properties of the disc wall, this study has also exposed the limitations of using standard section planes commonly employed by disc researchers.

ISSLS prize winner: microstructure and mechanical disruption of the lumbar disc annulus: part I: a microscopic investigation of the translamellar bridging network.

STUDY DESIGN: Microstructural investigation of interlamellar connectivity. OBJECTIVE: To reveal the macro and micro structure of the translamellar bridging network in the lumbar annulus. SUMMARY OF BACKGROUND DATA: Contrary to the view that there is minimal interconnection between lamellar sheets, experimental data reveal a significant contribution to the material behavior of the annulus from interactions between fiber populations of alternating lamellae. Recent microstructural studies indicate a localized rather than a homogeneous or dispersed mode of interconnectivity between lamellae. METHODS: Anterior segments of ovine lumbar discs in 2 age groups were sectioned along the oblique fiber angle. A 3-dimensional picture of the translamellar bridging network is developed using structural information obtained from fully hydrated unstained serial sections imaged by differential interference contrast optics. RESULTS: A high level of connectivity between apparently disparate bridging elements was revealed. The extended form of the bridging network is that of occasional substantial radial connections spanning many lamellae with a subsidiary fine branching network. The fibrous bridging network is highly integrated with the lamellae architecture via a collagen-based system of interconnectivity. CONCLUSION: This study demonstrates a far greater complexity to the interlamellar architecture of the disc annulus than has previously been recognized. Our findings are clearly relevant to disc biomechanics. Significant degrading of the translamellar bridging network may result in annular weakening leading potentially to disc failure. Most importantly this work opens the way to a much clearer understanding of the microanatomy of the disc wall.