Human annulus fibrosus material properties from biaxial testing and constitutive modeling are altered with degeneration

Abstract

The annulus fibrosus (AF) of the intervertebral disc undergoes large and multidirectional stresses and strains. Uniaxial tensile tests are limited for measuring AF material properties, because freely contracting edges can prevent fiber stretch and are not representative of in situ boundary conditions. The objectives of this study were to measure human AF biaxial tensile mechanics and to apply and validate a constitutive model to determine material properties. Biaxial tensile tests were performed on samples oriented along the circumferential-axial and the radial-axial directions. Data were fit to a structurally-motivated anisotropic hyperelastic model composed of isotropic extrafibrillar matrix, nonlinear fibers, and fiber-matrix interactions (FMI) normal to the fibers. The validated model was used to simulate shear and uniaxial tensile behavior, to investigate AF structure-function, and to quantify the effect of degeneration. The biaxial stress-strain response was described well by the model (R2>0.9). The model showed that the parameters for fiber nonlinearity and the normal FMI correlated with degeneration, resulting in an elongated toe region and lower stiffness with degeneration. The model simulations in shear and uniaxial tension successfully matched previously published circumferential direction Young’s modulus, provided an explanation for the low values in previously published axial direction Young’s modulus, and was able to simulate shear mechanics. The normal FMI were important contributors to stress and changed with degeneration, therefore, their microstructural and compositional source should be investigated. Finally, the biaxial mechanical data and constitutive model can be incorporated into a disc finite element model to provide improved quantification of disc mechanics.

Biaxial mechanics and inter‐lamellar shearing of stem‐cell seeded electrospun angle‐ply laminates for annulus fibrosus tissue engineering

“…18,33 In this study, we show that electrospun biologic laminates reach >60% of native tissue biaxial properties under these types of loads, and that these properties are dependent on the opposing lamellar structure. 4 These data 4 Results are shown as mean AE standard deviation.…”

“…4 Four hooks were attached to each edge of the samples, which were secured to pulleys on the biaxial device via 2-0 braided silk suture. 25 Fiber angle was measured from the X 1 axis (Fig.…”

“…2 With degeneration, structural organization, and mechanical properties of the AF decrease, resulting in abnormal function. 3,4 Current treatments options, including discectomy and spinal fusion, do not restore mechanical function to the disk, and as such, often result in degeneration of adjacent disks. 5 This indicates a need for regenerative strategies that restore mechanical function for all relevant loading regimes, ideally matching native tissue benchmarks.…”

Lamellar and fibre bundle mechanics of the annulus fibrosus in bovine intervertebral disc

“…For instance, uni-and bi-axial tests have been used to determine the stressstrain response of the annulus [10,11], down to the level of single lamella [12,13]. Most previous work has, however, inferred the mechanical behaviour of the tissue by tracking cells [14,15] or markers that were glued or photobleached on the tissue [10,[14][15][16], or alternatively relied on relatively low resolution tissue tracking (for instance, 0.2 mm 2 elements [16,17]). …”

Quantification of continuous in vivo flexion–extension kinematics and intervertebral strains

“…The annulus has been tested at strains ranging from 2.5 to 50 % in uniaxial tension [4,[6][7][8][9][10][11] and from 1.25 to 15 % in equibiaxial extension [12,13]. The wide range of strains utilized in these experiments makes the results difficult to interpret within a functional context.…”