Effect of endplate calcification and mechanical deformation on the distribution of glucose in intervertebral disc: a 3D finite element study

The intervertebral disc (IVD) is avascular, receiving nutrition from surrounding vasculature. Theoretical modelling can supplement experimental results to understand nutrition to IVD more clearly. A new, 3D finite element model of the IVD was developed to investigate effects of endplate calcification and mechanical deformation on glucose distributions in IVD. The model included anatomical disc geometry, non-linear coupling of cellular metabolism with pH and oxygen concentration and strain-dependent properties of the extracellular matrix. Calcification was simulated by reducing endplate permeability (∼79%). Mechanical loading was applied based on in vivo disc deformation during the transition from supine to standing positions. Three static strain conditions were considered: supine, standing and weight-bearing standing. Minimum glucose concentrations decreased 45% with endplate calcification, whereas disc deformation led to a 4.8–63% decrease, depending on the endplate condition (i.e. normal vs. calcified). Furthermore, calcification more strongly affected glucose concentrations in the nucleus compared to the annulus fibrous region. This study provides important insight into nutrient distributions in IVD under mechanical deformation.

[1]  V. Haughton,et al.  Measuring diffusion of solutes into intervertebral disks with MR imaging and paramagnetic contrast medium. , 1998, AJNR. American journal of neuroradiology.

[2]  A Ratcliffe,et al.  Compressive properties of the cartilaginous end‐plate of the baboon lumbar spine , 1993, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[3]  H. Yao,et al.  Diffusivity of Ions in Agarose Gels and Intervertebral Disc: Effect of Porosity , 2004, Annals of Biomedical Engineering.

[4]  J. Urban,et al.  Swelling Pressure of the Lumbar Intervertebral Discs: Influence of Age, Spinal Level, Composition, and Degeneration , 1988, Spine.

[5]  V. Mow,et al.  A MIXED FINITE ELEMENT FORMULATION OF TRIPHASIC MECHANO-ELECTROCHEMICAL THEORY FOR CHARGED, HYDRATED BIOLOGICAL SOFT TISSUES , 1999 .

[6]  A. Nachemson,et al.  Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. , 1975, Journal of anatomy.

[7]  A Shirazi-Adl,et al.  Analysis of nonlinear coupled diffusion of oxygen and lactic acid in intervertebral discs. , 2005, Journal of biomechanical engineering.

[8]  S. Roberts,et al.  Biochemical and Structural Properties of the Cartilage End-Plate and its Relation to the Intervertebral Disc , 1989, Spine.

[9]  V C Mow,et al.  Alterations in the mechanical behavior of the human lumbar nucleus pulposus with degeneration and aging , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[10]  S. Roberts,et al.  The cartilage end‐plate and intervertebral disc in scoliosis: Calcification and other sequelae , 1993, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[11]  Hai Yao,et al.  Three-dimensional inhomogeneous triphasic finite-element analysis of physical signals and solute transport in human intervertebral disc under axial compression. , 2007, Journal of biomechanics.

[12]  J C Fairbank,et al.  Electrochemical Measurement of Transport Into Scoliotic Intervertebral Discs In Vivo Using Nitrous Oxide as a Tracer , 2001, Spine.

[13]  D. Elliott,et al.  Effects of Degeneration on the Biphasic Material Properties of Human Nucleus Pulposus in Confined Compression , 2005, Spine.

[14]  A. Jackson,et al.  Effects of Low Glucose Concentrations on Oxygen Consumption Rates of Intervertebral Disc Cells , 2007, Spine.

[15]  S. Bibby,et al.  Cell Viability in Scoliotic Discs in Relation to Disc Deformity and Nutrient Levels , 2002, Spine.

[16]  S Holm,et al.  Nutrition of the intervertebral disc: solute transport and metabolism. , 1981, Connective tissue research.

[17]  Pascal Swider,et al.  Influence of Location, Fluid Flow Direction, and Tissue Maturity on the Macroscopic Permeability of Vertebral End Plates , 2008, Spine.

[18]  A. Nachemson,et al.  Nutritional changes in the canine intervertebral disc after spinal fusion. , 1982, Clinical orthopaedics and related research.

[19]  H. Yao,et al.  Effects of Hydration and Fixed Charge Density on Fluid Transport in Charged Hydrated Soft Tissues , 2003, Annals of Biomedical Engineering.

[20]  D. S. Hickey,et al.  Relation Between the Structure of the Annulus Fibrosus and the Function and Failure of the Intervertebral Disc , 1980, Spine.

[21]  L. Manchikanti.  Epidemiology of low back pain. , 2000, Pain physician.

[22]  H. Cheung,et al.  New insight into deformation-dependent hydraulic permeability of gels and cartilage, and dynamic behavior of agarose gels in confined compression. , 2003, Journal of biomechanics.

[23]  A. Shirazi-Adl,et al.  Investigation of solute concentrations in a 3D model of intervertebral disc , 2009, European Spine Journal.

[24]  F. Marchand,et al.  Investigation of the Laminate Structure of Lumbar Disc Anulus Fibrosus , 1990, Spine.

[25]  A. Nachemson,et al.  In vitro diffusion of dye through the end-plates and the annulus fibrosus of human lumbar inter-vertebral discs. , 1970, Acta orthopaedica Scandinavica.

[26]  J. Oro,et al.  The Lumbar Spine and Back Pain. , 1994 .

[27]  A. Maroudas,et al.  Biophysical chemistry of cartilaginous tissues with special reference to solute and fluid transport. , 1975, Biorheology.

[28]  J A Buckwalter,et al.  Aging and degeneration of the human intervertebral disc. , 1995, Spine.

[29]  Qun Xia,et al.  Measurement of geometric deformation of lumbar intervertebral discs under in-vivo weightbearing condition. , 2009, Journal of biomechanics.

[30]  K. Ito,et al.  Direction-dependent constriction flow in a poroelastic solid: the intervertebral disc valve. , 2000, Journal of biomechanical engineering.

[31]  Patrick Chabrand,et al.  Nutrient distribution and metabolism in the intervertebral disc in the unloaded state: a parametric study. , 2009, Journal of biomechanics.

[32]  L. Claes,et al.  Influence of extracellular osmolarity and mechanical stimulation on gene expression of intervertebral disc cells , 2007, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[33]  W. Gu,et al.  Effects of mechanical compression on metabolism and distribution of oxygen and lactate in intervertebral disc. , 2008, Journal of biomechanics.

[34]  J. Zerwekh,et al.  Biochemical changes associated with the symptomatic human intervertebral disk. , 1993, Clinical orthopaedics and related research.

[35]  W M Lai,et al.  A mixture theory for charged-hydrated soft tissues containing multi-electrolytes: passive transport and swelling behaviors. , 1998, Journal of biomechanical engineering.

[36]  A Shirazi-Adl,et al.  Finite Element Study of Nutrient Diffusion in the Human Intervertebral Disc , 2003, Spine.

[37]  S. Eisenstein,et al.  Biochemical changes in intervertebral disc degeneration. , 1981, Biochimica et biophysica acta.

[38]  Hai Yao,et al.  Physical Signals and Solute Transport in Cartilage Under Dynamic Unconfined Compression: Finite Element Analysis , 2004, Annals of Biomedical Engineering.

[39]  K. Ogata,et al.  Nutritional Pathways of the Intervertebral Disc: An Experimental Study Using Hydrogen Washout Technique , 1981, Spine.

[40]  H. Brodin.  Paths of nutrition in articular cartilage and intervertebral discs. , 1955, Acta orthopaedica Scandinavica.

[41]  Daniel R. Benson,et al.  New Perspectives on Low Back Pain. , 1990 .

[42]  Mark D. Brown,et al.  Studies on the Permeability of the Intervertebral Disc During Skeletal Maturation , 1976 .

[43]  S. Bibby,et al.  Effect of nutrient deprivation on the viability of intervertebral disc cells , 2004, European Spine Journal.

[44]  V C Mow,et al.  Shear mechanical properties of human lumbar annulus fibrosus , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[45]  J. Urban,et al.  Effects of low oxygen concentrations and metabolic inhibitors on proteoglycan and protein synthesis rates in the intervertebral disc , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[46]  H. Horner,et al.  2001 Volvo Award Winner in Basic Science Studies: Effect of Nutrient Supply on the Viability of Cells From the Nucleus Pulposus of the Intervertebral Disc , 2001, Spine.

[47]  A Shirazi-Adl,et al.  Computation of coupled diffusion of oxygen, glucose and lactic acid in an intervertebral disc. , 2007, Journal of biomechanics.

[48]  Thijs Grünhagen,et al.  Notochordal intervertebral disc cells: sensitivity to nutrient deprivation. , 2009, Arthritis and rheumatism.

[49]  S Holm,et al.  Nutrition of the intervertebral disc: effect of fluid flow on solute transport. , 1982, Clinical orthopaedics and related research.

[50]  W M Lai,et al.  A triphasic theory for the swelling and deformation behaviors of articular cartilage. , 1991, Journal of biomechanical engineering.

[51]  Christopher M. Boxell,et al.  Pathophysiology of lumbar disc degeneration: a review of the literature. , 2002, Neurosurgical focus.

[52]  A Shirazi-Adl,et al.  Analysis of cell viability in intervertebral disc: Effect of endplate permeability on cell population. , 2010, Journal of biomechanics.

[53]  Hai Yao,et al.  Physical signals and solute transport in human intervertebral disc during compressive stress relaxation: 3D finite element analysis. , 2006, Biorheology.

[54]  Jill P. G. Urban,et al.  The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus , 2003, European Spine Journal.

[55]  R. Cailliet,et al.  Vertebral End-Plate Changes With Aging of Human Vertebrae , 1982, Spine.

[56]  Ruth M Ripley,et al.  Metabolism of the Intervertebral Disc: Effects of Low Levels of Oxygen, Glucose, and pH on Rates of Energy Metabolism of Bovine Nucleus Pulposus Cells , 2005, Spine.