Poroelastic behaviour of the degenerating human intervertebral disc: a ten-day study in a loaded disc culture system

Abstract

The intervertebral disc (IVD) allows flexibility to the vertebral column, and transfers the predominant axial loads during daily activities. Its axial biomechanical behaviour is poroelastic, due to the water-binding and releasing capacity of the nucleus pulposus. Degeneration of the intervertebral disc presumably affects both the instantaneous elastic response to the load on the IVD and the subsequent interstitial flow of fluid. This study aims to quantify the poroelastic behaviour of the IVD and its change with degeneration, as defined by the magnetic resonance imaging-based Pfirrmann Score (PS). For a period of ten days, 36 human lumbar IVDs were loaded with a simulated physiological axial loading regime, while deformation was monitored. The IVDs responded to the loads with instantaneous elastic and slow poroelastic axial deformation. Several mechanical parameters changed throughout the first five days of the experiment, until the IVDs settled into a dynamic equilibrium. In this equilibrium, degeneration was significantly related to a decrease in disc height loss during the daytime high load phase (ρ = -0.49), and to a decrease in the rate of this deformation during the final half hour of each day (ρ = -0.53). These properties were related to the nucleus glycosaminoglycan/hydroxyproline (GAG/HYP) ratio, rather than GAG content alone, indicating that remodelling of the extracellular matrix reduces poroelastic properties of the IVD. This implies that the degenerated discs have a reduced capacity to bind water and/or a reduced resistance against fluid flow. The resulting loss in hydrostatic pressure may further change cell behaviour in the nucleus pulposus.Keywords: Intervertebral disc, degeneration, biomechanics, poroelastic behaviour, Pfirrmann, magnetic resonance imaging, glycosaminoglycan, biochemistry, loaded disc culture system, spine. IntroductionLow back pain (LBP) is one of the most frequent medical complaints in western society, with enormous socioeconomic impact (Katz, 2006). Lifetime prevalence of more than three months of LBP is 20 % (Hoy et al., 2012), and direct and indirect costs of LBP are estimated at 0.6 % of the gross national product in the Netherlands (Lambeek et al., 2011). Despite this, the scientific progress to improve prevention and cure has been limited so far (Balagué et al., 2012). Progress has been hampered, among others, by difficulties in pinpointing the aetiology of non-specific LBP (Andersson, 1999). In the past two decades, the relation between intervertebral disc (IVD) degeneration and LBP has been under debate (Adams et al., 2000;Balagué et al., 2012;van Tulder et al., 1997), but recent epidemiological studies show that IVD degeneration indeed is a significant predictor (Cheung et al., 2009;Livshits et al., 2011;Wang et al., 2012). Structure and function of the intervertebral discThe IVD is a "cushion-like structure" (Chan et al., 2011). Its core is the nucleus pulposus, a gel-like matrix rich in proteoglycans, which is contained by the annulus fibrosus, consisting o...

Osteoarthritis and intervertebral disc degeneration: Quite different, quite similar

“…The degradation of the ECM results in a decrease in the production of proteoglycans in the cartilaginous matrices . Consequently, less fluid is attracted, leading to a decrease in hydrostatic pressure . This causes reduced joint space and an increase in tissue deformation (ie, shear stresses).…”

“…Shear stress is a mechanical cue for the cells to shift from collagen type II to collagen type I production, resulting in a more fibrous tissue . This fibrous tissue has an inferior capacity to resist compressive loads, as there is a loss of the typical poro‐ and viscoelastic biomechanical properties . The disruption of ECM not only results in loss of joint space, but also causes subchondral sclerosis and the formation of osteophytes, which is a reaction of the bone to the changing mechanical environment …”

“…120 Consequently, less fluid is attracted, leading to a decrease in hydrostatic pressure. 121 This causes reduced joint space and an increase in tissue deformation (ie, shear stresses). Shear stress is a mechanical cue for the cells to shift from collagen type II to collagen type I production, resulting in a more fibrous tissue.…”

“…26,122,123 This fibrous tissue has an inferior capacity to resist compressive loads, as there is a loss of the typical poro-and viscoelastic biomechanical properties. 48,121,124 The disruption of ECM not only results in loss of joint space, but also causes subchondral sclerosis and the formation of osteophytes, which is a reaction of the bone to the changing mechanical environment. 4,16,129…”

Cartilage intermediate layer protein is regulated by mechanical stress and affects extracellular matrix synthesis

“…Once IDD is initiated, this homeostasis gradually breaks as an imbalance develops between the rates of production and breakdown of matrix components at early stages, leading to a series of events including alterations in the pH and osmotic pressure, thereby creating a harsh extracellular environment for resident cells in NP tissues. Furthermore, the ECM under healthy conditions is able to retain enough hydration to withstand and absorb the mechanical loading experienced in daily life (14). However, in IDD, synthesis of ECM components, including aggrecan and collagen II, which constitute the majority of the ECM, is decreased, leading to reduced hydration.…”