Elsevier

Journal of Biomechanics

Volume 45, Issue 3, 2 February 2012, Pages 491-496
Journal of Biomechanics

Intervertebral disc viscoelastic parameters and residual mechanics spatially quantified using a hybrid confined/in situ indentation method

https://doi.org/10.1016/j.jbiomech.2011.11.050Get rights and content

Abstract

With advancing age, injury, musculoskeletal pathology or a combination of these, a degenerative cascade of biomechanical, biochemical, and nutritional alterations diminish the intervertebral discs’ ability to maintain its structure and function. While the biomechanics of isolated disc tissues has been investigated across this degenerative spectrum, none have attempted to retain the in situ disc-endplate morphology during compressive tissue characterization. The objective of this study was to spatially quantify the viscoelastic parameters of the intervertebral disc throughout degeneration, including the as yet unreported residual stress/strain. This required the development of a hybrid confined/in situ indentation methodology, which preserves the disc structural morphology. At four locations of the disc (anterior-AF, right and left lateral AF, and NP) stress-relaxation tests were performed using the hybrid confined/in situ indentation method, which utilizes the vertebral endplate as the porous indenter tip. This method allows the endplate to remain interwoven with the disc tissue, retaining its native orientation. Healthy disc tissue exhibited significantly higher residual stress values compared to both moderate and severe degeneration in all locations (p<0.0156). Furthermore, the equilibrium stress at 15% strain (stress relaxation) was significantly diminished with advancing disc degeneration (p<0.0241). The equilibrium viscoelastic parameters show healthy discs encounter higher forces at the same strain level, and are able to maintain this force, where degenerated discs are unable to maintain this force throughout time. This morphology-conserved method provides insight into the spatial compressive mechanical properties of the intervertebral disc across the degeneration spectrum and will aid in modeling these tissue changes.

Introduction

Back pain is most common cause of activity limitation for individuals younger than 45 years of age, affecting an estimated 70–85% of the American population at one time in their lives (Andersson, 1999). Chronic low back pain is the most prevalent musculoskeletal impairment in the United States, leading to the number one cause for lost wages and accounting for more than 700,000 surgical procedures per year with a total over $50 billion annually spent on treatment and care (Bao and Yuan, 2000). Although the causes of low back pain are poorly defined and indistinct, the most often implicated tissue as the origin for pain is the intervertebral disc (IVD). The intervertebral disc affords the spine its extensive multidirectional motion due to the complex interaction between two morphologically, biomechanically, and biochemically distinct tissues: the annulus fibrosus (AF) and the nucleus pulposus (NP). The AF consists of highly organized concentric rings (lamellae) of fibrocartilaginous material surrounding the gel-like collagen and proteoglycan composite of the NP. The lamellae are primarily composed of Type-I collagen fibers oriented at approximately ±30° from the horizontal and altering direction with each successive layer. The NP is composed of a hydrated, disorganized matrix of collagen, mainly Type-II, and proteoglycans, principally Aggrecan (Kim and Branch, 2006, Roughley and Melching, 2006). Due to the high concentration of proteoglycans, which are negatively charged hydrophilic molecules, water diffuses into the NP providing an internal osmotic pressure to the IVD.

With advancing age, injury, musculoskeletal pathology or a combination of these, a degenerative cascade of biomechanical, biochemical, and nutritional alterations diminish the discs’ ability to maintain its structure and function. Morphologically, disc degeneration presents with decreased proteoglycans, reduced water content, altered collagen synthesis and degradation, an amorphous transition zone between the annulus fibrosus and nucleus pulposus, and a decrease in total disc height (Roughley, 2004, Kim and Branch, 2006). Biomechanically, these changes lead to decreased spinal stability and have been shown to alter local tissue mechanical properties (Mimura et al., 1994). Understanding the degenerative effects on local tissue material properties is essential for developing new disc therapies, replacement strategies, and consequently assessing their viability. Due to the complexity in the structure of the IVD, there are many material properties that are necessary to adequately model the tissue. These include tensile, shear, and compressive properties, both of the different structures of the disc (AF and NP) as well as the disc as a whole (Nerurkar et al., 2010).

Previous studies have examined changes in the compressive moduli of the IVD with respect to degeneration severity through the use of confined compression or disc excision techniques (Best and Guilak, 1994, Umehara and Tadano, 1996, Iatridis and Setton, 1997, Johannessen and Elliott, 2005, Perie and Maclean, 2006). Johannessen et al.(2005) examined human disc samples in confined compression and reported a decrease in aggregate modulus of the NP as degeneration grade increases. Using similar techniques, Iatridis et al. (1997, 1998) concluded that both the compressive and shear moduli of the AF at one site increase with worsening degeneration. These studies underscore the need to include degenerative changes when modeling the disc; prior modeling efforts have also indicated the need for regional tissue properties. Williams et al. (2007) created a three-dimensional poroelastic finite element model that includes regional biomechanical property variations which resulted in better prediction of observed in vivo behavior and motion of the spine. Only one study to our knowledge has quantified spatially based mechanical properties at 10 mm increments across the entire surface of the disc (Umehara et al., 1996). This study involved excision for direct indentation of the IVD, which involves the removal of the endplate. Removal of this cartilaginous endplate, which is highly interwoven with the fibers of the disc (Fig. 1), causes disruption of the orientation of the annular fibers in the vertical direction (Adams and Roughley, 2006). Thus, removal of the endplate prevents precise quantification of in situ mechanical properties of the native IVD. Furthermore, all of these methods due to their destructive nature eliminate the possibility of measuring in situ residual disc properties.

Therefore, to gain insight into the in situ viscoelastic regional material properties, we have developed a new methodology of hybrid confined/in situ indentation which involves leaving the endplate attached to the IVD at the test site. This technique allows for the quantification of the in situ residual stresses of the solid matrix. It has been established that the IVD has an intrinsic resting hydrostatic pressure; however, the residual stresses have not been reported for healthy or degenerated IVD tissues (Urban and McMullin, 1988, Johnstone and Urban, 1992, Adams and McNally, 1996).

The objectives of the present study were to spatially quantify the following metrics to determine the regional properties of the IVD tissues from across the degenerative spectrum using the newly developed in situ indentation test: (1) IVD height, (2) residual stress and strain, (3) equilibrium stress, (4) compressive equilibrium and elastic moduli, and (5) three-series prony viscoelastic stress-relaxation function coefficients. Together, these measures will enable spatial and temporal modeling of the IVD throughout the degenerative spectrum.

Section snippets

Methods

A factorial study design was used to examine the spatial and degeneration dependent properties of intervertebral discs in a human cadaver model. Sixteen human cadaveric IVDs (L1–L2) were acquired from the University of Minnesota Anatomy Bequest Program free of injury or surgery. Prior to testing, an MRI (1.5 T) was acquired for each spinal unit to determine the degree of degeneration (Pfirrmann et al., 2001). Grades were issued by independent analysis performed by three orthopedic spine

Results

The left and right locations of the AF were grouped together after analyses confirmed no statistical difference in any of the outcome measures (p>0.433). Previous studies have also reported left and right lateral symmetry in the AF (Lewis et al., 2008).

Disc height decreased significantly between ‘healthy’ and ‘severe’ degenerated groups in the anterior annulus, 9.67±1.71 mm to 5.53±3.12 mm (p=0.016), and the lateral annulus, 9.42±1.71 mm to 6.53±2.59 mm (p=0.014), but no significant change was

Discussion

This study measured the relationship between the severity of degeneration and the regional compressive mechanics of the intervertebral disc using a newly developed hybrid confined/in situ indentation methodology. This technique leaves the cartilaginous endplate attached, not disrupting the orientation of the fibers beneath, allowing for quantification of the in situ mechanical properties of the native IVD. Similar studies have aimed to understand the compressive mechanics of IVD however they

Conclusion

A novel hybrid confined/in situ indentation method provides insight into both spatial and temporal compressive mechanical properties of the intervertebral disc across the degeneration spectrum and will aid in modeling these tissue changes. This methodology also enabled us to report, for the first time, the residual strains of the solid matrix in healthy and in degenerative discs.

Conflict of interest statement

The authors have no conflict of interest to report.

Acknowledgements

The author’s would like to thank David W. Polly Jr., M.D., Edward R. Santos, M.D., and Jonathan N. Sembrano, M.D. for grading degree of degeneration of intervertebral discs based on MR images. We also thank Conrad Lindquist for machining the custom jig used to release the endplate.

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