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

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Abstract

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 4×400 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.

Introduction

Damage of the annulus fibrosus is implicated in intervertebral disc degeneration and may be attributed to mechanical causes, biological remodeling, loss of nutrition, and accumulation of cellular waste products. Whole body vibration causes muscular fatigue, a latency in the muscular response, and viscoelastic creep of soft tissues which may predispose the spinal motion segment to injury (Yoganandan et al., 1988; Adams and Dolan, 1997; Pope et al., 1998; Solomonow et al. (1999), Solomonow et al. (2000)). Repetitive mechanical loading on motion segments can result in significant damage to the disc and vertebrae. Cadaveric lumbar motion segments subjected to flexion and fatigue resulted in distortions of the lamellae of the annulus fibrosus and occasional radial fissures (Adams and Hutton, 1983). Hyperflexion has long been known to result in disc prolapse (Adams and Hutton, 1982) but sub-catastrophic injuries can also occur at loads below failure (Nightingale et al., 2002). Cyclic axial compression of motion segments resulted in failure of the vertebral endplate and subchondral bone under subfailure load magnitudes (as low as 50% of failure load) with less than 1000 cycles of loading (Hansson et al. (1987), Hansson et al. (1988)). The dynamic axial stiffness of the motion segment decreased for aged and degenerated lumbar spinal segments suggesting progressive damage may be a factor in disc degeneration (Hansson et al., 1987).

Failure of the annulus fibrosus or damage to the collagenous network is a potential cause of disc herniation. Clinical failure of the annulus in the posterolateral region of the disc was attributed, in part, to a reduced tensile failure stress in that region relative to the anterior region in both single layer (Skaggs et al., 1994) and multiple layer annulus fibrosus specimens (Galante, 1967; Acaroglu et al., 1995). With disc degeneration, failure stresses were significantly reduced, however failure strains were relatively constant with values of approximately 20% in the circumferential direction (Acaroglu et al., 1995). Sub-catastrophic failure and damage accumulation and progression was also predicted using finite element models implicating peripheral tears of the annulus (Natarajan et al., 1994; Kim, 2000). In vertical slices of annulus and bone (approximately 5 mm thick×30 mm wide) subjected to axial tension, fatigue failure was measured in less than 10,000 cycles if the load exceeded 45% of the ultimate tensile strength (Green et al., 1993). However, this study did not report material properties of the annulus in the circumferential direction, nor did they demonstrate if sub-catastrophic failure could occur with fewer cycles. At the composition level, the percent of denatured (damaged) collagen increased with intervertebral disc degeneration (Antoniou et al., 1996).

Damage progression in the circumferential direction of the disc annulus is likely to occur in vivo in response to extreme loading with associated degradation in tensile material properties, yet the threshold when this damage initiates is not available in the literature. We hypothesized that damage of the annulus will increase with the number of cycles and magnitude of strain applied to the disc. Furthermore, damage will occur at the weakest mechanical link which we hypothesized to be the interlamellar connections and therefore result in delamination. The primary 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. A secondary objective was to assess how damage affected the laminate structure of the annulus using histology, transmission electron microscopy (TEM) and biochemical measurements. Mechanical damage to the annulus was assessed through measurement of the normalized peak tensile stress and permanent deformation (% elongation).

Section snippets

Methods

Four rectangular tensile specimens oriented in the circumferential direction were harvested from the outer annulus of 8 mature bovine caudal discs (n=32) that were approximately 4 years of age 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 cyclic tests consisting of 400 cycles of baseline cyclic loading with

Results

Quasistatic ramp tests demonstrated a nonlinear stress–strain response (characteristic of that reported for human annulus tissue) with mean±SD values for UTS of 21.3±2.1% corresponding to failure stresses of 2.94±1.05 MPa. Acute and fatigue damage loading caused significant decreases in the normalized steady-state peak stresses (Fig. 4). Acute and fatigue loading to 40% of UTS (i.e., strain of 8.52%) reduced the normalized stress to 0.81 and 0.55, respectively (corresponding to segment 2 in Fig.

Discussion

In order to evaluate mechanical damage to the intervertebral disc, annulus fibrosus specimens were tested in tension using 4 different protocols. Damage to the annulus was assessed through measurement of permanent deformation (% elongation) and normalized peak stress. A secondary objective was to assess how damage affected the laminate structure of the annulus using biochemical measurements, histology and TEM evaluation. The most significant results of this study were that tensile stress

Acknowledgements

Funded by NIH Grant 1K01AR02078 and The Whitaker Foundation Grant RG-03-0030. We thank Drs. Mauro Alini and Peter Roughley for their helpful suggestions and Nicole DeLance at the Microscopy Imaging Center of the University of Vermont for technical assistance with histology and transmission electron microscopy.

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