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Time-dependent Characterization of Fluid Flow into the Intervertebral Disc

  • Author(s): Bezci, Semih Ege
  • Advisor(s): O'Connell, Grace D
  • et al.
Abstract

The primary function of the intervertebral disc is to support large, multi-directional loads acting on the spine. The intervertebral disc has a heterogeneous structure, comprised of a gel-like nucleus pulposus (NP) and the annulus fibrosus (AF). The AF has a highly organized structure consisting of collagen fibers oriented in a criss-cross pattern in the alternating layers. Despite differences in composition and structure, water is the primary biochemical constituent of both tissues, accounting for greater than 65% of tissue’s wet weight. The water content of the intervertebral disc fluctuates throughout the day as the magnitude of compressive stress acting on the spine varies with changes in body posture, muscle activity, and external loads. The disc loses water during the day and absorbs water at night when loads are reduced.

Due to the avascular nature of the intervertebral disc, cell viability and metabolism rely on the exchange of nutrients and metabolic by-products via diffusion under biochemical gradients and fluid flow modulated by diurnal loading patterns. Hence, investigating fluid flow kinematics under simulated physiological loading conditions is important for understanding healthy disc function and mechanobiology. However, there is a lack of knowledge of fluid flow behavior and recovery mechanics during low loading conditions when disc absorbs water and increases its height. Hence, this dissertation aims to fill in this gap in the literature by evaluating the time-dependent recovery mechanics and fluid flow kinematics of the healthy intervertebral disc during low loading conditions that simulate bed-rest. To achieve this, this study tested bovine bone-disc-bone motion segments under a series of creep and recovery loading conditions. Results showed that time-dependent disc recovery behavior has contributions from both inherent fluid-independent viscoelasticity and fluid-dependent poroelasticity. Intrinsic viscoelastic effects are present at short time scales, providing partial recovery of disc height within minutes of unloading before poroelastic effects come into play. Poroelastic fluid flow dominates recovery at long time scales and is largely driven by the osmotic differential between tissue and its surrounding environment.

In vitro biomechanical tests on disc joints monitor changes in disc height to understand the direction, magnitude, and rate of fluid flow through the disc. However, these studies report displacements for the entire bone-disc-bone joint without the ability to identify the region-specific changes during swelling due to fluid flow. To improve our understanding of the complex fluid redistribution within the disc, the second part of this work characterized the time-dependent swelling behavior of the intervertebral disc ex situ. The first experiment monitored time-dependent changes in tissue mass to compare differences in the swelling capacities of the NP and AF explants under free swelling conditions. NP explants experienced a higher swelling rate and equilibrium swelling capacity than AF explants. Specifically, there was a 200% increase in the NP tissue mass and a 70% increase in the AF tissue mass under free swelling conditions. The second experiment used an optical, non-contact measurement method to evaluate the distribution of swelling-induced strains throughout intact discs and AF rings. Axial deformations were fixed to prevent out-of-plane motion during swelling. The first group consisted of AF rings in contact with saline at the outer periphery and the center of the annular ring. The second group included AF rings in contact with saline solution only at the outer periphery. The third group included intact discs in contact with saline at the outer periphery. Tissue swelling due to fluid flow was observed to be a slow process that strongly depends on tissue-specific biochemical properties and physical boundary constraints. For AF rings, negative circumferential strains were observed in the inner AF, while positive circumferential strains were observed in the outer AF. However, restricting fluid flow only to the outer periphery during swelling reduced the swelling capacity of the inner AF. The largest absolute radial strain was observed to be in the outer AF for Group 1 and the outer AF for Group 2. The swelling capacity of the NP was largely reduced when swelling was restricted to occur only in the radial direction or constrained by the surrounding AF. Results from intact discs showed that NP pressurization during swelling reduces peak radial strains in the AF and results in uniform strain distribution throughout the AF.

Together these findings provide a better understanding of intervertebral disc mechanics and function, particularly during low loading periods when disc absorbs water and increases its volume due to swelling. In conclusion, fluid flow is a slow, time-dependent process that depends on many factors, including biochemical properties, external osmotic pressure, loading history, and boundary constraints.

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