Assessment of mechanical properties of isolated bovine intervertebral discs from multi-parametric magnetic resonance imaging

BMC Musculoskeletal Disorders

Gilles Beaudoin²  Guillaume Gilbert³  Delphine Périé¹  Maximilien Recuerda¹ 

[1] Research Center, CHU Sainte-Justine, Université de Montréal, Montréal, QC, Canada;CHUM Saint-Luc, Université de Montréal, Montréal, QC, Canada;Philips Healthcare, Montréal, QC, Canada

关键词: Multiple linear regressions;    Multi-parametric MRI;    Mechanical properties;    Compression tests;    Intervertebral disc;   

Others  :  1138267
DOI  :  10.1186/1471-2474-13-195

 received in 2012-02-01, accepted in 2012-10-08,  发布年份 2012

【 摘 要 】

Background

The treatment planning of spine pathologies requires information on the rigidity and permeability of the intervertebral discs (IVDs). Magnetic resonance imaging (MRI) offers great potential as a sensitive and non-invasive technique for describing the mechanical properties of IVDs. However, the literature reported small correlation coefficients between mechanical properties and MRI parameters. Our hypothesis is that the compressive modulus and the permeability of the IVD can be predicted by a linear combination of MRI parameters.

Methods

Sixty IVDs were harvested from bovine tails, and randomly separated in four groups (in-situ, digested-6h, digested-18h, digested-24h). Multi-parametric MRI acquisitions were used to quantify the relaxation times T1 and T2, the magnetization transfer ratio MTR, the apparent diffusion coefficient ADC and the fractional anisotropy FA. Unconfined compression, confined compression and direct permeability measurements were performed to quantify the compressive moduli and the hydraulic permeabilities. Differences between groups were evaluated from a one way ANOVA. Multi linear regressions were performed between dependent mechanical properties and independent MRI parameters to verify our hypothesis. A principal component analysis was used to convert the set of possibly correlated variables into a set of linearly uncorrelated variables. Agglomerative Hierarchical Clustering was performed on the 3 principal components.

Results

Multilinear regressions showed that 45 to 80% of the Young’s modulus E, the aggregate modulus in absence of deformation H_A0, the radial permeability k_r and the axial permeability in absence of deformation k₀ can be explained by the MRI parameters within both the nucleus pulposus and the annulus pulposus. The principal component analysis reduced our variables to two principal components with a cumulative variability of 52-65%, which increased to 70-82% when considering the third principal component. The dendograms showed a natural division into four clusters for the nucleus pulposus and into three or four clusters for the annulus fibrosus.

Conclusions

The compressive moduli and the permeabilities of isolated IVDs can be assessed mostly by MT and diffusion sequences. However, the relationships have to be improved with the inclusion of MRI parameters more sensitive to IVD degeneration. Before the use of this technique to quantify the mechanical properties of IVDs in vivo on patients suffering from various diseases, the relationships have to be defined for each degeneration state of the tissue that mimics the pathology. Our MRI protocol associated to principal component analysis and agglomerative hierarchical clustering are promising tools to classify the degenerated intervertebral discs and further find biomarkers and predictive factors of the evolution of the pathologies.

【 授权许可】

   
2012 Recuerda et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Klepps SJ, Lenke LG, Bridwell KH, Bassett GS, Whorton J: Prospective comparison of flexibility radiographs in adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2001, 26:E74-E79.
• [2]Cheh G, Lenke LG, Lehman RA Jr, Kim YJ, Nunley R, Bridwell KH: The reliability of preoperative supine radiographs to predict the amount of curve flexibility in adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2007, 32:2668-2672.
• [3]Cheung KM, Luk KD: Prediction of correction of scoliosis with use of the fulcrum bending radiograph. J Bone Joint Surg Am 1997, 79:1144-1150.
• [4]Lamarre ME, Parent S, Labelle H, Aubin CE, Joncas J, Cabral A, Petit Y: Assessment of spinal flexibility in adolescent idiopathic scoliosis: suspension versus side-bending radiography. Spine (Phila Pa 1976) 2009, 34:591-597.
• [5]Cassidy JJ, Hiltner A, Baer E: Hierarchical structure of the intervertebral disc. Connect Tissue Res 1989, 23:75-88.
• [6]Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IK, Bishop PB: Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine (Phila Pa 1976) 1990, 15:411-415.
• [7]Yao H, Justiz MA, Flagler D, Gu WY: Effects of swelling pressure and hydraulic permeability on dynamic compressive behavior of lumbar annulus fibrosus. Ann Biomed Eng 2002, 30:1234-1241.
• [8]Klisch SM, Lotz JC: A special theory of biphasic mixtures and experimental results for human annulus fibrosus tested in confined compression. J Biomech Eng 2000, 122:180-188.
• [9]Best BA, Guilak F, Setton LA, Zhu W, Saed-Nejad F, Ratcliffe A, Weidenbaum M, Mow VC: Compressive mechanical properties of the human anulus fibrosus and their relationship to biochemical composition. Spine (Phila Pa 1976) 1994, 19:212-221.
• [10]Iatridis JC, Setton LA, Foster RJ, Rawlins BA, Weidenbaum M, Mow VC: Degeneration affects the anisotropic and nonlinear behaviors of human anulus fibrosus in compression. J Biomech 1998, 31:535-544.
• [11]Perie D, Iatridis JC, Demers CN, Goswami T, Beaudoin G, Mwale F, Antoniou J: Assessment of compressive modulus, hydraulic permeability and matrix content of trypsin-treated nucleus pulposus using quantitative MRI. J Biomech 2006, 39:1392-1400.
• [12]Urban JP, Winlove CP: Pathophysiology of the intervertebral disc and the challenges for MRI. J Magn Reson Imaging 2007, 25:419-432.
• [13]Perie D, Korda D, Iatridis JC: Confined compression experiments on bovine nucleus pulposus and annulus fibrosus: sensitivity of the experiment in the determination of compressive modulus and hydraulic permeability. J Biomech 2005, 38:2164-2171.
• [14]Antoniou J, Mwale F, Demers CN, Beaudoin G, Goswami T, Aebi M, Alini M: Quantitative magnetic resonance imaging of enzymatically induced degradation of the nucleus pulposus of intervertebral discs. Spine (Phila Pa 1976) 2006, 31:1547-1554.
• [15]Toffanin R, Mlynarik V, Russo S, Szomolanyi P, Piras A, Vittur F: Proteoglycan depletion and magnetic resonance parameters of articular cartilage. Arch Biochem Biophys 2001, 390:235-242.
• [16]Antoniou J, Pike GB, Steffen T, Baramki H, Poole AR, Aebi M, Alini M: Quantitative magnetic resonance imaging in the assessment of degenerative disc disease. Magn Reson Med 1998, 40:900-907.
• [17]Antoniou J, Demers CN, Beaudoin G, Goswami T, Mwale F, Aebi M, Alini M: Apparent diffusion coefficient of intervertebral discs related to matrix composition and integrity. Magn Reson Imaging 2004, 22:963-972.
• [18]Paajanen H, Komu M, Lehto I, Laato M, Haapasalo H: Magnetization transfer imaging of lumbar disc degeneration. Correlation of relaxation parameters with biochemistry. Spine (Phila Pa 1976) 1994, 19:2833-2837.
• [19]Chiu EJ, Newitt DC, Segal MR, Hu SS, Lotz JC, Majumdar S: Magnetic resonance imaging measurement of relaxation and water diffusion in the human lumbar intervertebral disc under compression in vitro. Spine (Phila Pa 1976) 2001, 26:E437-E444.
• [20]Wang C, Witschey W, Goldberg A, Elliott M, Borthakur A, Reddy R: Magnetization transfer ratio mapping of intervertebral disc degeneration. Magn Reson Med 2010, 64(5):1520-1528.
• [21]Kurunlahti M, Kerttula L, Jauhiainen J, Karppinen J, Tervonen O: Correlation of diffusion in lumbar intervertebral disks with occlusion of lumbar arteries: a study in adult volunteers. Radiology 2001, 221:779-786.
• [22]Kerttula L, Kurunlahti M, Jauhiainen J, Koivula A, Oikarinen J, Tervonen O: Apparent diffusion coefficients and T2 relaxation time measurements to evaluate disc degeneration. A quantitative MR study of young patients with previous vertebral fracture. Acta Radiol 2001, 42:585-591.
• [23]Perie DS, MacLean JJ, Owen JP, Iatridis JC: Correlating material properties with tissue composition in enzymatically digested bovine annulus fibrosus and nucleus pulposus tissue. Ann Biomed Eng 2006, 34:769-777.
• [24]Nguyen M, Johannessen W, Yoder JH, Wheaton AJ, Vresilovic EJ, Borthakur A, Elliott DM: Noninvasive quantification of human nucleus pulposus pressure with use of T1{rho}-weighted magnetic resonance imaging. J Bone Joint Surg Br 2008, 90:796-802.
• [25]Mwale F, Demers CN, Michalek AJ, Beaudoin G, Goswami T, Beckman L, Iatridis JC, Antoniou J: Evaluation of quantitative magnetic resonance imaging, biochemical and mechanical properties of trypsin-treated intervertebral discs under physiological compression loading. J Magn Reson Imaging 2008, 27:563-573.
• [26]Périe D, Iatridis JC, Demers CN, Goswami T, Beaudoin G, Mwale F, Antoniou J: Assessment of compressive modulus, hydraulic permeability and matrix content of trypsin-treated nucleus pulposus using quantitative MRI. J Biomech 2006, 39(8):1392-1400.
• [27]Campana S, Charpail E, de Guise JA, Rillardon L, Skalli W, Mitton D: Relationships between viscoelastic properties of lumbar intervertebral disc and degeneration grade assessed by MRI. J Mech Behav Biomed Mater 2011, 4:593-599.
• [28]Heneghan P, Riches PE: Determination of the strain-dependent hydraulic permeability of the compressed bovine nucleus pulposus. J Biomech 2008, 41:903-906.
• [29]Gu WY, Mao XG, Foster RJ, Weidenbaum M, Mow VC, Rawlins BA: The anisotropic hydraulic permeability of human lumbar anulus fibrosus. Influence of age, degeneration, direction, and water content. Spine (Phila Pa 1976) 1999, 24:2449-2455.
• [30]Accadbled F, Laffosse JM, Ambard D, Gomez-Brouchet A, de Gauzy JS, Swider P: Influence of location, fluid flow direction, and tissue maturity on the macroscopic permeability of vertebral end plates. Spine (Phila Pa 1976) 2008, 33:612-619.
• [31]Wright P, Mougin O, Totman J, Peters A, Brookes M, Coxon R, Morris P, Clemence M, Francis S, Bowtell R, Gowland P: Water proton T₁ measurements in brain tissue at 7, 3, and 1.5T using IR-EPI, IR-TSE, and MPRAGE: results and optimization. Magn Resonan Mater Phys Biol Med 2008, 21:121-130.
• [32]Henkelman RM, Stanisz GJ, Graham SJ: Magnetization transfer in MRI: a review. NMR Biomed 2001, 14:57-64.
• [33]Kingsley PB: Introduction to diffusion tensor imaging mathematics: Part I. Tensors, rotations, and eigenvectors. Concepts Magn Reson Part A 2006, 28A:101-122.
• [34]Kingsley PB: Introduction to diffusion tensor imaging mathematics: Part II. Anisotropy, diffusion-weighting factors, and gradient encoding schemes. Concepts Magn Reson Part A 2006, 28A:123-154.
• [35]Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M: MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986, 161:401-407.
• [36]Recuerda M, Cote SP, Villemure I, Perie D: Influence of experimental protocols on the mechanical properties of the intervertebral disc in unconfined compression. J Biomech Eng 2011, 133:071006.
• [37]Allen KD, Athanasiou KA: Viscoelastic characterization of the porcine temporomandibular joint disc under unconfined compression. J Biomech 2006, 39:312-322.
• [38]DiSilvestro MR, Zhu Q, Suh JKF: Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: II–-effect of variable strain rates. J Biomech Eng 2001, 123:198-200.
• [39]DiSilvestro MR, Zhu Q, Wong M, Jurvelin JS, Suh JKF: Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: I–-simultaneous prediction of reaction force and lateral displacement. J Biomech Eng 2001, 123:191-197.
• [40]Mow VC, Kuei SC, Lai WM, Armstrong CG: Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J Biomech Eng 1980, 102:73-84.
• [41]Ateshian GA, Warden WH, Kim JJ, Grelsamer RP, Mow VC: Finite deformation biphasic material properties of bovine articular cartilage from confined compression experiments. J Biomech 1997, 30:1157-1164.
• [42]Holmes MH, Mow VC: The nonlinear characteristics of soft gels and hydrated connective tissues in ultrafiltration. J Biomech 1990, 23:1145-1156.
• [43]Swider P, Conroy M, Pedrono A, Ambard D, Mantell S, Soballe K, Bechtold JE: Use of high-resolution MRI for investigation of fluid flow and global permeability in a material with interconnected porosity. J Biomech 2007, 40:2112-2118.
• [44]Accadbled F, Ambard D, de Gauzy JS, Swider P: A measurement technique to evaluate the macroscopic permeability of the vertebral end-plate. Med Eng Phys 2008, 30:116-122.
• [45]Lyyra T, Arokoski JP, Oksala N, Vihko A, Hyttinen M, Jurvelin JS, Kiviranta I: Experimental validation of arthroscopic cartilage stiffness measurement using enzymatically degraded cartilage samples. Phys Med Biol 1999, 44:525-535.
• [46]Berg A, Singer T, Moser E: High-resolution diffusivity imaging at 3.0 T for the detection of degenerative changes: a trypsin-based arthritis model. Invest Radiol 2003, 38:460-466.