Asymmetric in-plane shear behavior of isolated cadaveric lumbar facet capsular ligaments: Implications for subject specific biomechanical models

Abstract

The facet capsular ligaments (FCLs) flank the spinous process on the posterior aspect of the spine. The lumbar FCL is collagenous, with collagen fibers aligned primarily bone-to-bone (medial-lateral) and experiences significant shear, especially during spinal flexion and extension. We characterized the mechanical response of the lumbar FCL to in-plane shear, and we evaluated that response in the context of the fiber architecture. In-plane shear tests with both positive and negative shear (i.e., corresponding to flexion and to extension) were performed on eight cadaveric human L4-L5 FCLs. Our most striking observation was subject-dependent asymmetry in the response. All samples showed a toe region of low stiffness, transitioning to greater stiffness at higher strains, for both shear directions. Different samples showed profoundly different transition strains, with some samples stiffening more rapidly in positive shear and some in negative shear. This unpredictable asymmetry, which did not correlate with age, side, or degeneration state, suggesting that collagen fibers in the FCL are sometimes aligned at a slight positive angle from the bone-to-bone axis and sometimes at a negative angle. Fitting the experimental data to a fiber-composite-based finite element model supported this idea, yielding optimal fits with positive or negative off-axis fiber directions (−40° to +40°). Subsequent examination of selected FCLs by small-angle x-ray scattering (SAXS) showed a similar variability in fiber direction. We conclude that small individual differences in lumbar FCL architecture may have a significant effect on lumbar FCL mechanics, especially at moderate strains.

Introduction

Low back pain affects up to 80% of adults in the United States in their lifetime (Deyo et al., 2006). The facet (zygapophyseal) joint and its joint capsule, located along the posterior spine, have been the subject of much research as potential sources of spine pain (Dreyer and Dreyfuss, 1996, Jaumard et al., 2011). The joint is formed by the pairs of bony facet surfaces at the interface between adjacent vertebrae, flanking the spinous process. The facet capsular ligament (FCL) is a curved capsular ligament surrounding the facet surfaces and encasing the joint space. The ligament’s major structural components are elastin and collagen fiber bundles, and it is innervated by proprioceptive and nociceptive nerves (Ashton et al., 1992). As a capsular ligament, the FCL encloses the synovial fluid in the facet joint space, whereas its innervation suggests an additional mechanosensory role. Furthermore, the FCL contributes to spinal stability (Sharma et al., 1995). All of these roles – fluid containment, mechanosensation, and stabilization – involve mechanical functions, making FCL mechanics an important area of study.

Previous mechanical studies of the FCL have used uniaxial and biaxial loading (Claeson and Barocas, 2016, Little and Khalsa, 2005). Little and Khalsa showed that the FCL exhibits viscoelastic and anisotropic behavior (Little and Khalsa, 2005), the latter consistent with the ligament's structural anisotropy (Boden et al., 1996). We previously (Claeson and Barocas, 2016) used equibiaxial extension tests in conjunction with a 3D finite element model. To describe the tissue accurately, we needed to include in-plane shear forces in the model parameter optimization (Claeson and Barocas, 2016). This result suggested that the largely unquantified shear properties of the lumbar FCL could be important. The need for detailed, multidirectional studies is further emphasized by the complex geometry of the FCL in conjunction with the complex motions of the spine (Zehr et al., 2019). Therefore, the objective of this study was to characterize the mechanical response of the lumbar FCL during planar shear testing.