Advertisement

Biomechanics and Modeling in Mechanobiology

, Volume 3, Issue 3, pp 125–140 | Cite as

Single lamellar mechanics of the human lumbar anulus fibrosus

  • G. A. HolzapfelEmail author
  • C. A. J. Schulze-Bauer
  • G. Feigl
  • P. Regitnig
Original Paper

Abstract

The mechanical behavior of the entire anulus fibrosus is determined essentially by the tensile properties of its lamellae, their fiber orientations, and the regional variation of these quantities. Corresponding data are rare in the literature. The paper deals with an in vitro study of single lamellar anulus lamellae and aims to determine (i) their tensile response and regional variation, and (ii) the orientation of lamellar collagen fibers and their regional variation. Fresh human body-disc-body units (L1–L2, n=11) from cadavers were cut midsagittally producing two hemidisc units. One hemidisc was used for the preparation of single lamellar anulus specimens for tensile testing, while the other one was used for the investigation of the lamellar fiber orientation. Single lamellar anulus specimens with adjacent bone fragments were isolated from four anatomical regions: superficial and deep lamellae (3.9±0.21 mm, mean ± SD, apart from the outer boundary surface of the anulus fibrosus) at ventro-lateral and dorsal positions. The specimens underwent cyclic uniaxial tensile tests at three different strain rates in 0.15 mol/l NaCl solution at 37°C, whereby the lamellar fiber direction was aligned with the load axis. For the characterization of the tensile behavior three moduli were calculated: Elow (0–0.1 MPa), Emedium (0.1–0.5 MPa) and Ehigh (0.5–1 MPa). Additionally, specimens were tested with the load axis transverse to the fiber direction. From the second hemidisc fiber angles with respect to the horizontal plane were determined photogrammetrically from images taken at six circumferential positions from ventral to dorsal and at three depth levels. Tensile moduli along the fiber direction were in the range of 28–78 MPa (regional mean values). Superficial lamellae have larger Emedium (p=0.017) and Ehigh (p=0.012) than internal lamellae, and the mean value of superficial lamellae is about three times higher than that of deep lamellae. Tensile moduli of ventro-lateral lamellae do not differ significantly from the tensile moduli of dorsal lamellae, and Elow is generally indifferent with respect to the anatomical region. Tensile moduli transverse to the fiber direction were about two orders of magnitude smaller (0.22±0.2 MPa, mean ± SD, n=5). Tensile properties are not correlated significantly with donor age. Only small viscoelastic effects were observed. The regional variation of lamellar fiber angle ϕ is described appropriately by a regression line |ϕ|=23.2+0.130×α (r2=0.55, p<0.001), where α is the polar angle associated with the circumferential position. The single anulus lamella may be seen as the elementary structural unit of the anulus fibrosus, and exhibits marked anisotropy and distinct regional variation of tensile properties and fiber angles. These features must be considered for appropriate physical and numerical modeling of the anulus fibrosus.

Keywords

Intervertebral Disc Nucleus Pulposus Fiber Orientation Tensile Behavior Depth Level 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors are particularly indebted to Markus Fröhlich, Sulzer Medica (now Centerpulse Orthopedics Ltd.), Winterthur, Switzerland, for valuable contributions. We thank Professor Reinhold Reimann from the Institute of Anatomy, Medical University Graz, for helpful ideas and motivating comments, and Elisabeth Pernkopf and Christian Chiocirca for their help regarding the experimental and dissecting works. We also like to acknowledge Robert Eberlein, from Sulzer Markets and Technology Ltd., for valuable discussions. Financial support for this research was provided by Sulzer Medica (now Centerpulse Orthopedics Ltd.), which is gratefully acknowledged.

References

  1. Acaroglu ER, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M (1995) Degeneration and aging affect the tensile behavior of human lumbar anulus fibrosus. Spine 20:2690–2701PubMedGoogle Scholar
  2. Adams P, Eyre DR, Muir H (1977) Biochemical aspects of development and ageing of human lumbar intervertebral discs. Rheumatol Rehabil 16:22–29PubMedGoogle Scholar
  3. Alini M, Li W, Markovic P, Aebi M, Spiro RC, Roughley PJ (2003) The potential and limitations of a cell-seeded collagen/hyaluronan scaffold to engineer an intervertebral disc-like matrix. Spine 28:446–454CrossRefPubMedGoogle Scholar
  4. Bass EC, Duncan NA, Hariharan JS, Dusick J, Bueff HU, Lotz JC (1997) Frozen storage affects the compressive creep behavior of the porcine intervertebral disc. Spine 22:2867–2876CrossRefPubMedGoogle Scholar
  5. Bayliss MT, Johnstone B, O’Brien JP (1988) 1988 Volvo award in basic science. Proteoglycan synthesis in the human intervertebral disc. Variation with age, region and pathology. Spine 13:972–981PubMedGoogle Scholar
  6. Brickley-Parsons D, Glimcher MJ (1984) Is the chemistry of collagen in intervertebral discs an expression of Wolff’s Law? A study of the human lumbar spine. Spine 9:148–163PubMedGoogle Scholar
  7. Cassidy JJ, Hiltner A, Baer E (1989) Hierarchical structure of the intervertebral disc. Connect Tissue Res 23:75–88PubMedGoogle Scholar
  8. Ebara S, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M (1996) Tensile properties of nondegenerate human lumbar anulus fibrosus. Spine 21:452–461CrossRefPubMedGoogle Scholar
  9. Eberlein R, Holzapfel GA, Schulze-Bauer CAJ (2001) An anisotropic model for annulus tissue and enhanced finite element analyses of intact lumbar disc bodies. Comput Methods Biomech Biomed Eng 4:209–229Google Scholar
  10. Eberlein R, Holzapfel GA, Fröhlich M (2004) Multi-segment FEA of the human lumbar spine including the heterogeneity of the annulus fibrosus. Comput Mech 34:147–163Google Scholar
  11. Elliott DM, Setton LA (2000) A linear material model for fiber-induced anisotropy of the anulus fibrosus. J Biomech Eng 122:173–179CrossRefPubMedGoogle Scholar
  12. Elliott DM, Setton LA (2001) Anisotropic and inhomogeneous tensile behavior of the human anulus fibrosus: experimental measurement and material model predictions. J Biomech Eng 123:256–263CrossRefPubMedGoogle Scholar
  13. Eyre DR, Muir H (1976) Types I and II collagens in intervertebral disc. Interchanging radial distributions in annulus fibrosus. Biochem J 157:267–270PubMedGoogle Scholar
  14. Fujita Y, Duncan NA, Lotz JC (1997) Radial tensile properties of the lumbar annulus fibrosus are site and degeneration dependent. J Orthop Res 15:814–819PubMedGoogle Scholar
  15. Funk JR, Hall GW, Crandall JR, Pilkey WD (2000) Linear and quasi-linear viscoelastic characterization of ankle ligaments. J Biomech Eng 122:15–22CrossRefPubMedGoogle Scholar
  16. Galante JO (1967) Tensile properties of the human lumbar anulus fibrosus. Acta Orthop Scand Suppl 100:1–91Google Scholar
  17. Hickey DS, Hukins DW (1980) X-ray diffraction studies of the arrangement of collagenous fibres in human fetal intervertebral disc. J Anat 131:81–90PubMedGoogle Scholar
  18. Hickey DS, Aspden RM, Hukins DW, Jenkins JP, Isherwood I (1986) Analysis of magnetic resonance images from normal and degenerate lumbar intervertebral discs. Spine 11:702–708PubMedGoogle Scholar
  19. Hsu EW, Setton LA (1999) Diffusion tensor microscopy of the intervertebral disc anulus fibrosus. Magn Reson Med 41:992–999CrossRefPubMedGoogle Scholar
  20. Huyghe JM, Houben GB, Drost MR, van Donkelaar CC (2003) An ionised/non-ionised dual porosity model of intervertebral disc tissue: experimental quantification of parameters. Biomech Model Mechanobiol 2:3–19CrossRefPubMedGoogle Scholar
  21. Inoue H (1981) Three-dimensional architecture of lumbar intervertebral discs. Spine 6:139–146PubMedGoogle Scholar
  22. Inoue H, Takeda T (1975) Three-dimensional observation of collagen framework of lumbar intervertebral discs. Acta Orthop Scand 46:949–956PubMedGoogle Scholar
  23. Isherwood I, Prendergast DJ, Hickey DS, Jenkins JP (1986) Quantitative analysis of intervertebral disc structure. Acta Radiol Suppl 369:492–495Google Scholar
  24. Jenkins JP, Hickey DS, Zhu XP, Machin M, Isherwood I (1985) MR imaging of the intervertebral disc: a quantitative study. Br J Radiol 58:705–709Google Scholar
  25. Johnstone B, Urban JP, Roberts S, Menage J (1992) The fluid content of the human intervertebral disc. Comparison between fluid content and swelling pressure profiles of discs removed at surgery and those taken postmortem. Spine 17:412–416Google Scholar
  26. Klisch SM, Lotz JC (1999) Application of a fiber-reinforced continuum theory to multiple deformations of the annulus fibrosus. J Biomech 32:1027–1036CrossRefPubMedGoogle Scholar
  27. Laible JP, Pflaster DS, Krag MH, Simon BR, Haugh LD (1993) A poroelastic-swelling finite element model with application to the intervertebral disc. Spine 18:659–670PubMedGoogle Scholar
  28. Marchand F, Ahmed AM (1990) Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15:402–410PubMedGoogle Scholar
  29. Panagiotacopulos ND, Knauss WG, Bloch R (1979) On the mechanical properties of human intervertebral disc material. Biorheology 16:317–330PubMedGoogle Scholar
  30. Panagiotacopulos ND, Pope MH, Bloch R, Krag MH (1987a) Water content in human intervertebral discs. Part II. Viscoelastic behavior. Spine 12:918–924PubMedGoogle Scholar
  31. Panagiotacopulos ND, Pope MH, Krag MH, Bloch R (1987b) A mechanical model for the human intervertebral disc. J Biomech 20:839–850CrossRefPubMedGoogle Scholar
  32. Race A, Broom ND, Robertson P (2000) Effect of loading rate and hydration on the mechanical properties of the disc. Spine 25:662–669CrossRefPubMedGoogle Scholar
  33. Rannou F, Poiraudeau S, Foltz V, Boiteux M, Corvol M, Revel M (2000) Monolayer anulus fibrosus cell cultures in a mechanically active environment: local culture condition adaptations and cell phenotype study. J Lab Clin Med 136:412–421CrossRefPubMedGoogle Scholar
  34. Sato M, Asazuma T, Ishihara M, Ishihara M, Kikuchi T, Kikuchi M, Fujikawa K (2003) An experimental study of the regeneration of the intervertebral disc with an allograft of cultured annulus fibrosus cells using a tissue-engineering method. Spine 28:548–553CrossRefPubMedGoogle Scholar
  35. Shah JS, Hampson WG, Jayson MI (1978) The distribution of surface strain in the cadaveric lumbar spine. J Bone Joint Surg Br 60-B:246–251PubMedGoogle Scholar
  36. 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 19:1310–1319PubMedGoogle Scholar
  37. Stokes IA (1987) Surface strain on human intervertebral discs. J Orthop Res 5:348–355PubMedGoogle Scholar
  38. Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IK, Bishop PB (1990) Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 15:411–415PubMedGoogle Scholar
  39. Tsuji H, Hirano N, Ohshima H, Ishihara H, Terahata N, Motoe T (1993) Structural variation of the ventral and dorsal anulus fibrosus in the development of human lumbar intervertebral disc. A risk factor for intervertebral disc rupture. Spine 18:204–210Google Scholar
  40. Urban JP, McMullin JF (1988) Swelling pressure of the lumbar intervertebral discs: influence of age, spinal level, composition, and degeneration. Spine 13:179–187PubMedGoogle Scholar
  41. Woo SL, Gomez MA, Akeson WH (1981) The time and history-dependent viscoelastic properties of the canine medical collateral ligament. J Biomech Eng 103:293–298PubMedGoogle Scholar
  42. Wu HC, Yao RF (1976) Mechanical behavior of the human annulus fibrosus. J Biomech 9:1–7CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2004

Authors and Affiliations

  • G. A. Holzapfel
    • 1
    Email author
  • C. A. J. Schulze-Bauer
    • 1
  • G. Feigl
    • 2
  • P. Regitnig
    • 3
  1. 1.Institute for Structural Analysis—Computational BiomechanicsGraz University of TechnologyGrazAustria
  2. 2.Institute of AnatomyMedical University GrazGrazAustria
  3. 3.Institute of PathologyMedical University GrazGrazAustria

Personalised recommendations