Abstract
The intervertebral disc is a complex fibro-cartilaginous material, consisting of a pressurized nucleus pulposus surrounded by the annulus fibrosus, which has an angle-ply structure. Disc injury and degeneration are noted by significant changes in tissue structure and function, which significantly alters stress distribution and disc joint stiffness. Differences in fibre orientation are thought to contribute to changes in disc torsion mechanics. Therefore, the objective of this study was to evaluate the effect of collagen fibre orientation on internal disc mechanics under compression combined with axial rotation. We developed and validated a finite element model (FEM) to delineate changes in disc mechanics due to fibre orientation from differences in material properties. FEM simulations were performed with fibres oriented at \(\pm 30^{\circ }\) throughout the disc (uniform by region and fibre layer). The initial model was validated by published experimental results for two load conditions, including \(0.48\,\hbox {MPa}\) axial compression and \(10\,\hbox {Nm}\) axial rotation. Once validated, fibre orientation was rotated by \(4^{\circ }\) or \(8^{\circ }\) towards the horizontal plane, resulting in a decrease in disc joint torsional stiffness. Furthermore, we observed that axial rotation caused a sinusoidal change in disc height and radial bulge, which may be beneficial for nutrient transport. In conclusion, including anatomically relevant fibre angles in disc joint FEMs is important for understanding stress distribution throughout the disc and will be important for understanding potential causes for disc injury. Future models will include regional differences in fibre orientation to better represent the fibre architecture of the native disc.
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References
Adams MA, McNally DS, Dolan P (1996) ’Stress’ distributions inside intervertebral discs. The effects of age and degeneration. J Bone Joint Surg Br 78(6):965–972
Adams MA, Peter JR (2006) What is intervertebral disc degeneration, and what causes it? Spine 31(18):2151–2161
Adams MA, Burton K, Bogduk N (2013) The biomechanics of back pain, 3rd edn. Elsevier, Edinburgh
Buckwalter JA (1995) Aging and degeneration of the human intervertebral disc. Spine 20(11):1307–1314
Beckstein JC, Sen S, Schaer TP, Vresilovic EJ, Elliott DM (2008) Comparison of animal discs used in disc research to human lumbar disc: axial compression mechanics and glycosaminoglycan content. Spine 33(6):E166–173
Berger-Roscher N, Casaroli GR, Villa T, Galbusera F, Wilke HJ (2016) Influence of complex loading conditions on intervertebral disc failure. Spine (Epub ahead of print)
Bezci SE, Nandy A, O’Connell GD (2015) Effect of hydration on healthy intervertebral disk mechanical stiffness. J Biomech Eng 137(10):101007
Blankenbaker DG, Haughton VM, Rogers BP, Meyerand ME, Fine JP (2006) Axial rotation of the lumbar spinal motion segments correlated with concordant pain on discography: a preliminary study. Am J Roentgenol 186(3):795–799
Cassidy JJ, Hiltner A, Baer E (1989) Hierarchical structure of the intervertebral disc. Connect Tissue Res 23(1):75–88
Chan SCW, Ferguson SJ, Wuertz K, Gantenbein-Ritter B (2011) Biological response of the intervertebral disc to repetitive short-term cyclic torsion. Spine 36(24):2021–2030
Costi JJ, Stokes IA, Gardner-Morse M, Laible JP, Scoffone HM, Iatridis JC (2007) Direct measurement of intervertebral disc maximum shear strain in six degrees of freedom: motions that place disc tissue at risk of injury. J Biomech 40(11):2457–2466
Coventry NB, Ghormley RK, Kernohan JW (1945) The intervertebral disc: its microscopic anatomy and pathology Part I: anatomy, development and physiology. J Bone Joint Surg 27A:105112
Dreischarf M, Zander T, Shirazi-Adl A, Puttlitz CM, Adam CJ, Chen CS, Goel VK, Kiapour A, Kim YH, Labus KM, Little JP, Park WM, Wang YH, Wilke HJ, Rohlmann A, Schmidt H (2014) Comparison of eight published static finite element models of the intact lumbar spine: predictive power of models improves when combined together. J Biomech 47(8):1757–1766
Duncan AE, Ricki JC, Patricia AK (2012) Sex differences in spinal osteoarthritis in humans and rhesus monkeys (Macaca mulatta). Spine 37(11):915
Elliott DM, Setton LA (2001) Anisotropic and inhomogeneous tensile behavior of the human anulus fibrosus: experimental measurement and material model predictions. J Biomech Eng 123(3):256–263
Elliott DM, Sarver JJ (2004) Young investigator award winner: validation of the mouse and rat disc as mechanical models of the human lumbar disc. Spine 29:713–22
Espinoza Orias AA, Mammoser NM, Triano JJ, An HS, Andersson GB, Inoue N (2016) Effects of axial torsion on disc height distribution: an in vivo study. J Manipulative Physiol Ther 39(4):294–303
Farfan HF (1984) The torsional injury of the lumbar spine. Spine 9(1):53
Goodwin RR, James KS, Daniels AU, Dunn HK (1994) Distraction and compression loads enhance spine torsional stiffness. J Biomech 27(8):1049–1057
Guerin HA, Elliott DM (2006) Degeneration affects the fiber reorientation of human annulus fibrosus under tensile load. J Biomech 39(8):1410–1418
Haberl H, Cripton PA, Orr TE, Beutler T, Frei H, Lanksch WR, Nolte LP (2004) Kinematic response of lumbar functional spinal units to axial torsion with and without superimposed compression and flexion/extension. Eur Spine J 13(6):560–566
Haughton VM, Lim TH, An H (1999) Intervertebral disk appearance correlated with stiffness of lumbar spinal motion segments. Am J Neuroradiol 20(6):1161–1165
Haughton VM, Rogers B, Meyerand ME, Resnick DK (2002) Measuring the axial rotation of lumbar vertebrae in vivo with MR imaging. Am J Neuroradiol 23(7):1110–1116
Heuer F, Schmidt H, Klezl Z, Claes L, Wilke HJ (2007) Stepwise reduction of functional spinal structures increase range of motion and change lordosis angle. J Biomech 40(2):271–280
Hickey DS, Hukins DWL (1980) X-ray diffraction studies of the arrangement of collagenous fibres in human fetal intervertebral disc. J Anat 131:8190
Holzapfel GA, Schulze-Bauer CA, Feigl G, Regitnig P (2005) Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech Model Mechanobiol 3(3):125–140
Homminga J, Lehr AM, Meijer GJ, Janssen MM, Schlosser TP, Verkerke GJ, Castelein RM (2013) Posteriorly directed shear loads and disc degeneration affect the torsional stiffness of spinal motion segments: a biomechanical modeling study. Spine 38(21):E1313–1319
Hoogendoorn WE, van Poppel MNM, Bongers PM, Koes BW, Bouter LM (1999) Physical load during work and leisure time as risk factors for back pain. Scand J Work Environ Health 25(5):387–403
Horton WG (1958) Further observations on the elastic mechanism of the intervertebral disc. J Bone Joint Surg [B] 40–B:551–557
Hsu EW, Lori AS (1999) Diffusion tensor microscopy of the intervertebral disc anulus fibrosus. Magn Reson Med 41(5):992–999
Jacobs NT, Cortes DH, Peloquin JM, Vresilovic EJ, Elliott DM (2014) Validation and application of an intervertebral disc finite element model utilizing independently constructed tissue-level constitutive formulations that are nonlinear, anisotropic, and time-dependent. J Biomech 47(11):2540–2546
Johnston SL, Campbell MR, Scheuring R, Feiveson AH (2010) Risk of herniated nucleus pulposus among US astronauts. Aviat Space Environ Med 81(6):566–574
Kelly TA, Roach BL, Weidner ZD, Mackenzie-Smith CR, OConnell GD, Lima EG, Stoker AM, Cook JL, Ateshian GA, Hung CT (2013) Tissue-engineered articular cartilage exhibits tension-compression nonlinearity reminiscent of the native cartilage. J Biomech 46(11):1784–1791
Klein JA, Hukins DWL (1982) Collagen fibre orientation in the annulus fibrosus of intervertebral disc during bending and torsion measured by X-ray diffraction. Biochim Biophys Acta 719(1):98–101
Korecki CL, MacLean JJ, Iatridis JC (2008) Dynamic compression effects on intervertebral disc mechanics and biology. Spine 33(13):1403–1409
Kuiper JI, Burdorf A, Frings-Dresen MHW, Kuijer PPFM, Spreeuwers D, Lotters FJB, Miedema HS (2005) Assessing the work-relatedness of nonspecific low-back pain. Scand J Work Environ Health 31(3):237–243
Li W, Wang S, Xia Q, Passias P, Kozanek M, Wood K, Li G (2011) Lumbar facet joint motion in patients with degenerative disc disease at affected and adjacent levels: an in vivo biomechanical study. Spine 36(10):E629
Lotters F, Burdorf A, Kuiper J, Miedema H (2003) Model for the work-relatedness of low-back pain. Scand J Work Environ Health 29(6):431–440
Lu YM, Hutton WC, Gharpuray VM (1996) Can variations in intervertebral disc height affect the mechanical function of the disc? Spine 21(19):2208–2216
Maas SA, Ellis BJ, Ateshian GA, Weiss JA (2012) FEBio: finite elements for biomechanics. J Biomech Eng 134(1):011005
Marchand F, Ahmed AM (1990) Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15(5):402–410
Meakin JR, Hukins DW (2000) Effect of removing the nucleus pulposus on the deformation of the annulus fibrosus during compression of the intervertebral disc. J Biomech 33(5):575–580
Moon SM, Yoder JH, Wright AC, Smith LJ, Vresilovic EJ, Elliott DM (2013) Evaluation of intervertebral disc cartilaginous endplate structure using magnetic resonance imaging. Eur Spine J 22(8):1820–1828
Natarajan RN, Andersson GB (1999) The influence of lumbar disc height and cross-sectional area on the mechanical response of the disc to physiologic loading. Spine 24(18):1873–1881
NIH-NINDS (2015) Low back pain fact sheet. In: Liaison OoCaP (ed), National Institutes of Health, Bethesda https://www.ninds.nih.gov/Disorders/Patient-Caregiver-Education/Fact-Sheets/Low-Back-Pain-Fact-Sheet
Ochia RS, Cavanagh PR (2007) Reliability of surface EMG measurements over 12 hours. J Electromyogr Kinesiol 17(3):365–371
O’Connell GD, Guerin HL, Elliott DM (2009) Theoretical and uniaxial experimental evaluation of human annulus fibrosus degeneration. J Biomech Eng 131(11):111007
O’Connell GD, Jacobs NT, Sen S, Vresilovic EJ, Elliott DM (2011a) Axial creep loading and unloaded recovery of the human intervertebral disc and the effect of degeneration. J Mech Behav Biomed Mater 4(7):933–942
O’Connell GD, Johannessen W, Vresilovic EJ, Elliott DM (2007a) Human internal disc strains in axial compression measured noninvasively using magnetic resonance imaging. Spine 32(25):2860–2868
O’Connell GD, Vresilovic EJ, Elliott DM (2007b) Comparison of animals used in disc research to human lumbar disc geometry. Spine 32(3):328–333
O’Connell GD, Vresilovic EJ, Elliott DM (2011b) Human intervertebral disc internal strain in compression: the effect of disc region, loading position, and degeneration. J Orthop Res 29(4):547–555
Pearcy MJ, Tibrewal SB (1984) Axial rotation and lateral bending in the normal lumbar spine measured by three-dimensional radiography. Spine 9(6):582–587
Peloquin JM, Yoder JH, Jacobs NT, Moon SM, Wright AC, Vresilovic EJ, Elliott DM (2014) Human L3L4 intervertebral disc mean 3D shape, modes of variation, and their relationship to degeneration. J Biomech 47(10):2452–9
Popovich JM, Welcher JB, Hedman TP, Tawackoli W, Anand N, Chen TC, Kulig K (2013) Lumbar facet joint and intervertebral disc loading during simulated pelvic obliquity. Spine J 13(11):1581–1589
Rodriguez AG, Rodriguez-Soto AE, Burghardt AJ, Berven S, Majumdar S, Lotz JC (2012) Morphology of the human vertebral endplate. J Orthop Res 30(2):280–287
Seidler A, Euler U, Bolm-Audorff U, Ellegast R, Grifka J, Haerting J, Jager M, Michaelis M, Kuss O (2011) Physical workload and accelerated occurrence of lumbar spine diseases: risk and rate advancement periods in a German multicenter case-control study. Scand J Work Environ Health 37(1):30–36
Shirazi-Adl A (1989) On the fibre composite material models of disc annulus—comparison of predicted stresses. J Biomech 22(4):357–365
Shirazi-Adl A (1991) Finite-element evaluation of contact loads on facets of an L2–L3 lumbar segment in complex loads. Spine 16(5):533–541
Shirazi-Adl A (1994) Nonlinear stress analysis of the whole lumbar spine in torsion—mechanics of facet articulation. J Biomech 27(3):289293–291299
Shirazi-Adl A, Abdul MA, Suresh CS (1986) Mechanical response of a lumbar motion segment in axial torque alone and combined with compression. Spine 11(9):914–927
Showalter BL, Beckstein JC, Martin JT, Beattie EE, Espinoza Orias AA, Schaer TP, Vresilovic EJ, Elliott DM (2012) Comparison of animal discs used in disc research to human lumbar disc: torsion mechanics and collagen content. Spine 37(15):E900–907
Skaggs DL, Weidenbaum M, Iatridis JC, Ratcliffe A, Mow VC (1994) Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19(12):1310–1319
Spilker RL (1980) Mechanical behavior of a simple model of an intervertebral disk under compressive loading. J Biomech 13(10):895–901
Tanaka N, An HS, Lim TH, Fujiwara A, Jeon CH, Haughton VM (2001) The relationship between disc degeneration and flexibility of the lumbar spine. Spine J 1(1):47–56
Tsai A, Yezzi A, Wells W, Tempany C, Tucker D, Fan A, Grimson WE, Willsky A (2003) A shape-based approach to the segmentation of medical imagery using level sets. IEEE Trans Med Imaging 22(2):137–154
van Deursen DL, Snijders CJ, Kingma I, van Dieen JH (2001) In vitro torsion-induced stress distribution changes in porcine intervertebral discs. Spine 26(23):2582–2586
Veres SP, Robertson PA, Broom ND (2010) The influence of torsion on disc herniation when combined with flexion. Eur Spine J 19(9):1468–1478
Wang C, Gonzales S, Levene H, Gu W, Huang CY (2013) Energy metabolism of intervertebral disc under mechanical loading. J Orthop Res 31(11):1733–1738
Wilke HJ, Kienle A, Maile S, Rasche V, Berger-Roscher N (2016) A new dynamic six degrees of freedom disc-loading simulator allows to provoke disc damage and herniation. Eur Spine J 25(5):1363–1372
Zirbel SA, Stolworthy DK, Howell LL, Bowden AE (2013) Intervertebral disc degeneration alters lumbar spine segmental stiffness in all modes of loading under a compressive follower load. Spine J 13(9):1134–1147
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This study was funded by the Hellman Foundation, San Francisco, CA, the Regents of the University of California, and J. K. Zee Fellowship (BY)
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Yang, B., O’Connell, G.D. Effect of collagen fibre orientation on intervertebral disc torsion mechanics. Biomech Model Mechanobiol 16, 2005–2015 (2017). https://doi.org/10.1007/s10237-017-0934-2
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DOI: https://doi.org/10.1007/s10237-017-0934-2