Skip to main content

Advertisement

Biointerphases

Journal for Biophysical Chemistry

Biointerphases Cover Image

Spiral twisting of fiber orientation inside bone lamellae

Biointerphases volume 1, pages1–5(2006)Cite this article

Abstract

The secondary osteon — a fundamental building block in compact bone — is a multilayered cylindrical structure of mineralized collagen fibrils arranged around a blood vessel. Functionally, the osteon must be adapted to the in vivo mechanical stresses in bone at the level of its microstructure. However, questions remain about the precise mechanism by which this is achieved. By application of scanning x-ray diffraction with a micron-sized synchrotron beam, along with measurements of local mineral crystallographic axis direction, we reconstruct the three-dimensional orientation of the mineralized fibrils within a single osteon lamella (∼5 μm). We find that the mineralized collagen fibrils spiral around the central axis with varying degrees of tilt, which would — structurally — impart high extensibility to the osteon. As a consequence, strains inside the osteon would have to be taken up by means of shear between the fibrils.

References

  1. 1

    S. Weiner and H. Wagner, Annu. Rev. Mater. Sci. 28, 271 (1998).

  2. 2

    M. M. Giraud-Guille, L. Besseau, and R. Martin, J. Biomech. 36, 1571 (2003).

  3. 3

    J. Y. Rho, L. Kuhn-Spearing, and P. Zioupos, Med. Eng. Phys. 20, 92 (1998).

  4. 4

    A. C. Neville, Biology of fibrous composites: Development beyond the cell membrane (Cambridge University Press, New York, NY, 1993).

  5. 5

    V. Ziv and S. Weiner, Connect. Tissue Res. 30, 165 (1994).

  6. 6

    H. S. Gupta, W. Wagermaier, G. A. Zickler, D. Raz-Ben Aroush, S. S. Funari, P. Roschger, H. D. Wagner, and P. Fratzl, Nano Lett. 5, 2108 (2005).

  7. 7

    J. D. Currey, Bones: Structure and mechanics (Princeton University Press, Princeton, N.J., 2002).

  8. 8

    M. Portigliatti Barbos, P. Bianco, A. Ascenzi, and A. Boyde, Metab. Bone Dis. Relat. Res. 5, 309 (1984).

  9. 9

    T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, Anat. Rec. B New Anat. 274, 157 (2003).

  10. 10

    A. Ascenzi, A. Benvenuti, A. Bigi, E. Foresti, M. H. J. Koch, F. Mango, A. Ripamonyi, and N. Roveri, Calcif. Tissue Int. 62, 266 (1998).

  11. 11

    M. G. Ascenzi, A. Ascenzi, A. Benvenuti, M. Burghammer, S. Panzavolta, and A. Bigi, J. Struct. Biol. 141, 22 (2003).

  12. 12

    D. Jaschouz, O. Paris, P. Roschger, H. S. Hwang, and P. Fratzl, J. Appl. Crystallogr. 36, 494 (2003).

  13. 13

    H. R. Wenk and S. Grigull, J. Appl. Crystallogr. 36, 1040 (2003).

  14. 14

    O. Paris, I. Zizak, H. Lichtenegger, P. Roschger, K. Klaushofer, and P. Fratzl, Cell Mol. Biol. (Paris) 46, 993 (2000).

  15. 15

    P. Fratzl, M. Groschner, G. Vogl, H. Plenk, J. Eschberger, N. Fratzl-Zelman, K. Kolller, and K. Klaushofer, J. Bone Miner. Res. 7, 329 (1992).

  16. 16

    I. Zizak, O. Paris, P. Roschger, S. Bernstorff, H. Amenitsch, K. Klaushofer, and P. Fratzl, J. Appl. Crystallogr. 33, 820 (2000).

  17. 17

    C. Riekel and R. J. Davies, Curr. Opin. Colloid Interface Sci. 9, 396 (2005).

  18. 18

    L. Calderin, M. J. Stott, and A. Rubio, Phys. Rev. B 67, 134106 (2003).

  19. 19

    F. Heidelbach, C. Riekel, and H. R. Wenk, J. Appl. Crystallogr. 32, 841 (1999).

  20. 20

    H. Wenk and F. Heidelbach, Bone (N.Y.) 24, 361 (1999).

  21. 21

    W. J. Landis, K. J. Hodgens, J. Arena, M. J. Song, and B. F. McEwen, Microsc. Res. Tech. 33, 192 (1996).

  22. 22

    S. Weiner, W. Traub, and H. D. Wagner, J. Struct. Biol. 126, 241 (1999).

  23. 23

    A. P. Hammersley, S. O. Svensson, M. Hanfland, A. N. Fitch, and D. Hausermann, High Press. Res. 14, 235 (1996).

  24. 24

    H. Lichtenegger, A. Reiterer, S. E. Stanzl-Tschegg, and P. Fratzl, J. Struct. Biol. 128, 257 (1999).

  25. 25

    H. Lichtenegger, M. Müller, O. Paris, C. Riekel, and P. Fratzl, J. Appl. Crystallogr. 32, 1127 (1999).

  26. 26

    P. Fratzl, Curr. Opin. Colloid Interface Sci. 8, 32 (2003).

  27. 27

    A. Reiterer, H. Lichtenegger, S. Tschegg, and P. Fratzl, Philos. Mag. A 79, 2173 (1999).

  28. 28

    M. M. Giraud-Guille, Curr. Opin. Solid State Mater. Sci. 3, 221 (1998).

  29. 29

    S. C. Cowin, J. Non-Newtonian Fluid Mech. 119, 155 (2004).

  30. 30

    P. Fratzl, I. Burgert, and H. S. Gupta, Phys. Chem. Chem. Phys. 6, 5575 (2004).

Download references

Author information

Affiliations

  1. Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424, Potsdam, Germany
    • W. Wagermaier
    • , H. S. Gupta
    •  & A. Gourrier
  2. ESRF, European Synchrotron Radiation Facility, 30843, Grenoble, France
    • M. Burghammer
  3. Ludwig Boltzmann Institute of Osteology at the Hanusch Hospital of WGKK and AUVA Trauma Centre Meidling, 1120, Vienna, Austria
    • P. Roschger
  4. Department of Biomaterials, Max Planck Institute Colloids and Interfaces, 14424, Potsdam, Germany
    • P. Fratzl
Authors
  1. Search for W. Wagermaier in:
  2. Search for H. S. Gupta in:
  3. Search for A. Gourrier in:
  4. Search for M. Burghammer in:
  5. Search for P. Roschger in:
  6. Search for P. Fratzl in:

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wagermaier, W., S. Gupta, H., Gourrier, A. et al. Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1, 1–5 (2006). https://doi.org/10.1116/1.2178386

Download citation