Skip to main content
Biointerphases

Journal for Biophysical Chemistry

Biointerphases Cover Image
Download PDF

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).

    Article  CAS  Google Scholar 

  2. 2

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

    Article  Google Scholar 

  3. 3

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

    Article  CAS  Google Scholar 

  4. 4

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

    Google Scholar 

  5. 5

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  7. 7

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

    Google Scholar 

  8. 8

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  11. 11

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

    Article  Google Scholar 

  12. 12

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

    Article  CAS  Google Scholar 

  13. 13

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

    Article  CAS  Google Scholar 

  14. 14

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

    CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  16. 16

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

    Article  CAS  Google Scholar 

  17. 17

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

    Article  CAS  Google Scholar 

  18. 18

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

    Article  Google Scholar 

  19. 19

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

    Article  CAS  Google Scholar 

  20. 20

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

    Article  CAS  Google Scholar 

  21. 21

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

    Article  CAS  Google Scholar 

  22. 22

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

    Article  CAS  Google Scholar 

  23. 23

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

    Article  Google Scholar 

  24. 24

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

    Article  CAS  Google Scholar 

  25. 25

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

    Article  CAS  Google Scholar 

  26. 26

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

    Article  CAS  Google Scholar 

  27. 27

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

    Article  CAS  Google Scholar 

  28. 28

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

    Article  CAS  Google Scholar 

  29. 29

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

    Article  CAS  Google Scholar 

  30. 30

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

    Article  CAS  Google Scholar 

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. W. Wagermaier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. S. Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Gourrier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Burghammer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Roschger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Fratzl
    View author publications

    You can also search for this author in PubMed Google Scholar

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

\