Annals of Biomedical Engineering

, Volume 46, Issue 9, pp 1280–1291 | Cite as

The Biomechanics of the Inter-Lamellar Matrix and the Lamellae During Progression to Lumbar Disc Herniation: Which is the Weakest Structure?

  • Javad Tavakoli
  • Dhara B. Amin
  • Brian J. C. Freeman
  • John J. CostiEmail author


While microstructural observations have improved our understanding of possible pathways of herniation progression, no studies have measured the mechanical failure properties of the inter-lamellar matrix (ILM), nor of the adjacent lamellae during progression to herniation. The aim of this study was to employ multiscale, biomechanical and microstructural techniques to evaluate the effects of progressive induced herniation on the ILM and lamellae in control, pre-herniated and herniated discs (N = 7), using 2 year-old ovine spines. Pre-herniated and herniated (experimental) groups were subjected to macroscopic compression while held in flexion (13°), before micro-mechanical testing. Micro-tensile testing of the ILM and the lamella from anterior and posterolateral regions was performed in radial and circumferential directions to measure failure stress, modulus, and toughness in all three groups. The failure stress of the ILM was significantly lower for both experimental groups compared to control in each of radial and circumferential loading directions in the posterolateral region (p < 0.032). Within each experimental group in both loading directions, the ILM failure stress was significantly lower by 36% (pre-herniation), and 59% (herniation), compared to the lamella (p < 0.029). In pre-herniated compared to control discs, microstructural imaging revealed significant tissue stretching and change in orientation (p < 0.003), resulting in a loss of distinction between respective lamellae and ILM boundaries.


Biomechanics Interlamellar matrix Lumbar disc herniation Microstructure Multiscale Lamellae Ovine model Failure stress 


Conflict of interest

The authors have nothing to declare. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.


  1. 1.
    Acaroglu, E. R., J. C. Iatridis, L. A. Setton, R. J. Foster, V. C. Mow, and M. Weidenbaum. Degeneration and aging affect the tensile behavior of human lumbar anulus fibrosus. Spine 20:2690–2701, 1995.CrossRefGoogle Scholar
  2. 2.
    Adams, M. A., B. J. Freeman, H. P. Morrison, I. W. Nelson, and P. Dolan. Mechanical initiation of intervertebral disc degeneration. Spine 25:1625–1636, 2000.CrossRefGoogle Scholar
  3. 3.
    Adams, M. A., and W. C. Hutton. Prolapsed intervertebral disc. A hyperflexion injury Volvo award in basic science. Spine 7(184–191):1982, 1981.Google Scholar
  4. 4.
    Amin, D. B., D. Sommerfeld, I. M. Lawless, R. M. Stanley, B. Ding, and J. J. Costi. Effect of degeneration on the six degree of freedom mechanical properties of human lumbar spine segments. J Orthop Res 34:1399–1409, 2016.CrossRefGoogle Scholar
  5. 5.
    Doube, M., M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine. BoneJ: free and extensible bone image analysis in ImageJ. Bone 47:1076–1079, 2010.CrossRefGoogle Scholar
  6. 6.
    Ebara, S., J. C. Iatridis, L. A. Setton, R. J. Foster, V. C. Mow, and M. Weidenbaum. Tensile properties of nondegenerate human lumbar anulus fibrosus. Spine 21:452–461, 1996.CrossRefGoogle Scholar
  7. 7.
    Fazzalari, N. L., J. J. Costi, T. C. Hearn, R. D. Fraser, B. Vernon-Roberts, J. Hutchinson, B. A. Manthey, I. H. Parkinson, and C. Sinclair. Mechanical and pathologic consequences of induced concentric anular tears in an ovine model. Spine 26:2575–2581, 2001.CrossRefGoogle Scholar
  8. 8.
    Fujita, Y., N. A. Duncan, and J. C. Lotz. Radial tensile properties of the lumbar annulus fibrosus are site and degeneration dependent. J Orthop Res 15:814–819, 1997.CrossRefGoogle Scholar
  9. 9.
    Gregory, D. E., W. C. Bae, R. L. Sah, and K. Masuda. Anular delamination strength of human lumbar intervertebral disc. Eur Spine J 21:1716–1723, 2012.CrossRefGoogle Scholar
  10. 10.
    Gregory, D. E., W. C. Bae, R. L. Sah, and K. Masuda. Disc degeneration reduces the delamination strength of the annulus fibrosus in the rabbit annular disc puncture model. Spine J 14:1265–1271, 2014.CrossRefGoogle Scholar
  11. 11.
    Gregory, D. E., and J. P. Callaghan. Does vibration influence the initiation of intervertebral disc herniation?: an examination of herniation occurrence using a porcine cervical disc model. Spine 36:E225–E231, 2011.CrossRefGoogle Scholar
  12. 12.
    Guthold, M., W. Liu, E. A. Sparks, L. M. Jawerth, L. Peng, M. Falvo, R. Superfine, R. R. Hantgan, and S. T. Lord. A comparison of the mechanical and structural properties of fibrin fibers with other protein fibers. Cell Biochem Biophys 49:165–181, 2007.CrossRefGoogle Scholar
  13. 13.
    Hart, L. G., R. A. Deyo, and D. C. Cherkin. Physician office visits for low back pain. Frequency, clinical evaluation, and treatment patterns from a U.S. national survey. Spine 20:11–19, 1995.CrossRefGoogle Scholar
  14. 14.
    Henry, J. L., K. Yashpal, H. Vernon, J. Kim, and H.-J. Im. Lumbar facet joint compressive injury induces lasting changes in local structure, nociceptive scores, and inflammatory mediators in a novel rat model. Pain Res Treat 2012:127636, 2012.Google Scholar
  15. 15.
    Holzapfel, G. A., C. A. J. Schulze-Bauer, G. Feigl, and P. Regitnig. Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech Model Mechanobiol 3:125–140, 2005.CrossRefGoogle Scholar
  16. 16.
    Iatridis, J., and I. ap Gwynn. Mechanisms for mechanical damage in the intervertebral disc annulus fibrosus. J Biomech 37:1165–1175, 2004.CrossRefGoogle Scholar
  17. 17.
    Koebbe, C. J., J. C. Maroon, A. Abla, H. El-Kadi, and J. Bost. Lumbar microdiscectomy: a historical perspective and current technical considerations. Neurosurg Focus 13:E3, 2002.Google Scholar
  18. 18.
    Lawless, I. M., B. Ding, B. S. Cazzolato, and J. J. Costi. Adaptive velocity-based six degree of freedom load control for real-time unconstrained biomechanical testing. J Biomech 47:3241–3247, 2014.CrossRefGoogle Scholar
  19. 19.
    Marchand, F., and A. M. Ahmed. Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15:402–410, 1990.CrossRefGoogle Scholar
  20. 20.
    Nachemson, A., and J. M. Morris. Invivo measurement of intradiscal pressure. A method for the determination of pressure in the lower lumbar discs. J Bone Joint Surg Am 46:1077–1092, 1964.CrossRefGoogle Scholar
  21. 21.
    Ninomiya, M., and T. Muro. Pathoanatomy of lumbar disc herniation as demonstrated by computed tomography/discography. Spine 17:1316–1322, 1992.CrossRefGoogle Scholar
  22. 22.
    Pezowicz, C. A., P. A. Robertson, and N. D. Broom. Intralamellar relationships within the collagenous architecture of the annulus fibrosus imaged in its fully hydrated state. J Anat 207:299–312, 2005.CrossRefGoogle Scholar
  23. 23.
    Schindelin, J., C. T. Rueden, M. C. Hiner, and K. W. Eliceiri. The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529, 2015.CrossRefGoogle Scholar
  24. 24.
    Schollum, M. L., P. A. Robertson, and N. D. Broom. A microstructural investigation of intervertebral disc lamellar connectivity: detailed analysis of the translamellar bridges. J Anat 214:805–816, 2009.CrossRefGoogle Scholar
  25. 25.
    Skaggs, D. L., M. Weidenbaum, J. C. Iatridis, A. Ratcliffe, and V. C. Mow. Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19:1310–1319, 1994.CrossRefGoogle Scholar
  26. 26.
    Tarulli, A. W., and E. M. Raynor. Lumbosacral radiculopathy. Neurol Clin 25:387–405, 2007.CrossRefGoogle Scholar
  27. 27.
    Tavakoli, J., and J. J. Costi. Development of a rapid matrix digestion technique for ultrastructural analysis of elastic fibers in the intervertebral disc. J Mech Behav Biomed Mater 71:175–183, 2017.CrossRefGoogle Scholar
  28. 28.
    Tavakoli, J., and J. Costi. New findings confirm the viscoelastic behaviour of the inter-lamellar matrix of the disc annulus fibrosus in radial and circumferential directions of loading. Acta Biomater 71:411–419, 2018.CrossRefGoogle Scholar
  29. 29.
    Tavakoli, J., D. M. Elliott, and J. J. Costi. Structure and mechanical function of the inter-lamellar matrix of the annulus fibrosus in the disc. J Orthop Res 34:1307–1315, 2016.CrossRefGoogle Scholar
  30. 30.
    Tavakoli, J., D. M. Elliott, and J. J. Costi. The ultra-structural organization of the elastic network in the intra- and inter-lamellar matrix of the intervertebral disc. Acta Biomater 58:269–277, 2017.CrossRefGoogle Scholar
  31. 31.
    van Heeswijk, V. M., A. Thambyah, P. A. Robertson, and N. D. Broom. Posterolateral disc prolapse in flexion initiated by lateral inner annular failure: an investigation of the herniation pathway. Spine 42:1604–1613, 2017.CrossRefGoogle Scholar
  32. 32.
    Veres, S. P., P. A. Robertson, and N. D. Broom. ISSLS prize winner: microstructure and mechanical disruption of the lumbar disc annulus part II: how the annulus fails under hydrostatic pressure. Spine 33:2711–2720, 2008.CrossRefGoogle Scholar
  33. 33.
    Veres, S. P., P. A. Robertson, and N. D. Broom. The morphology of acute disc herniation: a clinically relevant model defining the role of flexion. Spine 34:2288–2296, 2009.CrossRefGoogle Scholar
  34. 34.
    Veres, S. P., P. A. Robertson, and N. D. Broom. ISSLS prize winner: how loading rate influences disc failure mechanics: a microstructural assessment of internal disruption. Spine 35:1897–1908, 2010.CrossRefGoogle Scholar
  35. 35.
    Veres, S. P., P. A. Robertson, and N. D. Broom. The influence of torsion on disc herniation when combined with flexion. Eur Spine J 19:1468–1478, 2010.CrossRefGoogle Scholar
  36. 36.
    Vernon-Roberts, B., R. J. Moore, and R. D. Fraser. The natural history of age-related disc degeneration: the pathology and sequelae of tears. Spine 32:2797–2804, 2007.CrossRefGoogle Scholar
  37. 37.
    Wade, K. R., P. A. Robertson, A. Thambyah, and N. D. Broom. How healthy discs herniate: a biomechanical and microstructural study investigating the combined effects of compression rate and flexion. Spine 39:1018–1028, 2014.CrossRefGoogle Scholar
  38. 38.
    Wade, K. R., P. A. Robertson, A. Thambyah, and N. D. Broom. “Surprise” loading in flexion increases the risk of disc herniation due to annulus-endplate junction failure: a mechanical and microstructural investigation. Spine 40:891–901, 2015.CrossRefGoogle Scholar
  39. 39.
    Wade, K. R., M. L. Schollum, P. A. Robertson, A. Thambyah, and N. D. Broom. A more realistic disc herniation model incorporating compression, flexion and facet-constrained shear: a mechanical and microstructural analysis. Part I: low rate loading. Eur Spine J 26:2616–2628, 2017.CrossRefGoogle Scholar
  40. 40.
    Wilke, H.-J., A. Kettler, and L. E. Claes. Are sheep spines a valid biomechanical model for human spines? Spine 22:2365–2374, 1997.CrossRefGoogle Scholar
  41. 41.
    Wilke, H. J., P. Neef, M. Caimi, T. Hoogland, and L. E. Claes. New in vivo measurements of pressures in the ntervertebral disc in daily life. Spine 24:755–762, 1999.CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2018

Authors and Affiliations

  1. 1.Biomechanics and Implants Research Group, Medical Device Research Institute, College of Science and EngineeringFlinders UniversityAdelaideAustralia
  2. 2.Department of Spinal SurgeryRoyal Adelaide HospitalAdelaideAustralia
  3. 3.Centre for Orthopaedic and Trauma Research, Adelaide Health & Medical SciencesUniversity of AdelaideAdelaideAustralia
  4. 4.South Australian Health & Medical Research InstituteAdelaideAustralia

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