Mechanisms for mechanical damage in the intervertebral disc annulus fibrosus

Abstract

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.

Fig. 1.

(a) Schematic of fiber-reinforced laminate representation of the annulus fibrosus of the intervertebral disc demonstrating axial stress (σ_x) and in-plane shear stress (τ_xy). The x−y coordinate system is taken with the structure, i.e., x is in the direction of circumferential hoop stress, and y is in the axial direction. The 1–2 coordinate system is oriented with directions 1 and 2 parallel and perpendicular to the fibers, respectively, with fiber angle θ. (b) Partial free-body diagram demonstrating direction of axial stress, in-plane shear stress, and interlaminar shear stress τ_xz, as well as partial delamination, and free surfaces (which are absent of stresses for a uniaxial tension test). (c) Schematic representation of cross section of the eight-layer annulus layup (aspect ratio was modified for clarity).

Fig. 2.

(a) Schematic of a broken collagen fiber with adjacent unbroken fibers. Note that the distance between fibers, h; is taken as the fiber radius. (b) Free-body diagram for a segment of collagen fiber. Results of this analysis indicated that the stress in the broken fiber is back to 95% of its nominal value at 32 fiber diameters away from the break (~5 μm).

Fig. 3.

Stresses throughout the thickness (z-direction) on the annulus layers resulting from 10% strain in the circumferential (x-direction) for angle-ply laminate with eight layers and fiber angle θ = 39°. (a) In the global coordinate system stresses are given in the x-direction (σ_x), y-direction (σ_y), and for in-plane shear in the x−y direction (τ_xy) (i.e., where x, y, and z corresponds to the circumferential, axial, and radial anatomical directions, respectively). (b) In the material coordinate system, stresses are given in the longitudinal direction (σ₁), transverse direction (σ₂) and for in-plane shear (τ₁₂). The fiber orientation with z-position is superimposed on both graphs.

Fig. 4.

Interlaminar shear stresses for angle-ply laminate of eight-layer angle-ply laminate (circle) and four-layer angle-ply laminate (square) with same total thickness and fiber angles of 39°. The fiber orientation with z-position is superimposed for both the eight-layer simulation (top) and four-layer simulation (bottom). Note that a laminate with fewer layers has a larger magnitude of τ_xz than the laminate with thinner layers, and may be responsible for circumferential tears.

Fig. 5.

SEM of two different regions of interest in the rat tail intervertebral disc nucleus pulposus demonstrating: (a) fine collagenous structure of the rat nucleus pulposus; (b) cellular inclusion from nucleus pulposus cells demonstrating area where cell was present; and (c) high-magnification image of cellular inclusion demonstrating fine structure of pericellular matrix.

Fig. 6.

SEM of annulus fibrosus of rat tail intervertebral disc demonstrating: (a) angle-ply laminate structure with collagen fibers protruding from the fracture site. An additional view of the laminate structure with delamination and matrix failure is shown under low (b) and high (c) magnification, with (d) high-magnification image of microtubule structure in the collagen network.

Fig. 7.

Schematic representation of typical failure patterns in a fiber-reinforced layer of composite materials. At the laminate level (i.e., multiple layers), these patterns manifest themselves in the form of transverse cracks in planes parallel to the fibers, fiber-dominated failures perpendicular to the fibers, and delaminations.