TECHNICAL PAPERS
Jul 15, 2002

Micromechanical Model for Ultrastructural Stiffness of Mineralized Tissues

Publication: Journal of Engineering Mechanics
Volume 128, Issue 8

Abstract

We recently found that mineralized tissues (mineralized tendons and bones), at an observation scale of some microns, are open isotropic hydroxyapatite crystal foams which are reinforced unidirectionally by (organic) collagen molecules. The collagen reinforcement is mechanically activated by crosslinks between collagen assemblies and hydroxyapatite. With this morphology in mind, we develop in this paper a continuum micromechanics model for the ultrastructural stiffness of mineralized tissues. The homogenization is achieved in two steps: At a scale of some hundred nanometers, the isotropic crystal foam is represented as a two-phase polycrystal composed of a hydroxyapatite crystal phase and a nonminerally phase filling the intercrystalline space. At a scale above of some five to ten micrometers, the polycrystal plays the role of a connected matrix, in which a collagen inclusion phase is embedded. The effective stiffness of this phase is determined by the tight links between collagen and hydroxyapatite. The input for the model are the mineral volume fraction and the collagen volume fraction, which are species and tissue-type specific. Then, on the basis of four intrinsic micromechanical stiffness constants, the model is able to predict the full ultrastructural stiffness tensor of mineralized tissues, from low-mineralized turkey leg tendon to highly anisotropic human bones, and high-mineralized isotropic ear bones of whales. This is shown on the basis of a large data set compiled in the Appendix.

Get full access to this article

View all available purchase options and get full access to this article.

References

Ashman, R., Cowin, S., van Buskirk, W., and Rice, J.(1984). “A continuous wave technique for the measurement of the elastic properties of cortical bone.” J. Biomech., 17(5), 349–361.
Biltz, R., and Pellegrino, E.(1969). “The chemical anatomy of bone.” J. Bone Jt. Surg., Am. Vol., 51(3), 456–466.
Cusack, S., and Miller, A.(1979). “Determination of the elastic constants of collagen by Brillouin light scattering.” J. Mol. Biol., 135, 39–51.
Eshelby, J.(1957). “The determination of the elastic field of an ellipsoidal inclusion, and related problems.” Proc. R. Soc. London, Ser. A, 241, 376–396.
Fratzl, P., Schreiber, S., and Klaushofer, K.(1996). “Bone mineralization as studied by small-angle x-ray scattering.” Connect. Tissue Res., 34(4), 247–254.
Glimcher, M.(1984). “Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein bound phosphate bonds.” Philos. Trans. R. Soc. London, Ser. B, 304, 479–508.
Hasegawa, K., Turner, C., and Burr, D.(1994). “Contribution of collagen and mineral to the elastic anisotropy of bone.” Calcif. Tissue Int., 55, 381–386.
Hellmich, C., and Ulm, F. J. (2002). “Are mineralized tissues open crystal foams reinforced by crosslinked collagen?—some energy arguments.” J. Biomechan., in press.
Helnwein, P.(2001). “Some remarks on the compressed matrix representation of symmetric second-order and fourth-order tensors.” Comput. Methods Appl. Mech. Eng., 190, 2753–2770.
Hoffler, C., Moore, K., Kozloff, K., Zysset, P., Brown, M., and Goldstein, S.(2000). “Heterogeneity of bone lamellar-level elastic moduli.” Bone (N.Y.), 26, 603–609.
Hunter, G., Hauschka, P., Poole, A., Rosenberg, L., and Goldberg, H.(1996). “Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins.” Biochem. J., 317, 59–64.
Katz, J.(1980). “Anisotropy of Young’s modulus of bone.” Nature (London), 283, 106–107.
Katz, J., and Ukraincik, K.(1971). “On the anisotropic elastic properties of hydroxyapatite.” J. Biomech., 4, 221–227.
Kotha, S., and Guzelsu, N.(2000). “The effects of interphase and bonding on the elastic modulus of bone: Changes with age-related osteoporosis.” Med. Eng. Phys., 22, 575–585.
Lees, S.(1987). “Considerations regarding the structure of the mammalian mineralized osteoid from viewpoint of the generalized packing model.” Connect. Tissue Res., 16, 281–303.
Lees, S., Ahern, J., and Leonard, M.(1983). “Parameters influencing the sonic velocity in compact calcified tissues of various species.” J. Acoust. Soc. Am., 74(1), 28–33.
Lees, S., and Davidson, C.(1977). “The role of collagen in the elastic properties of calcified tissue.” J. Biomech., 10, 473–486.
Lees, S., Hanson, D., and Page, E.(1995). “Some acoustical properties of the otic bones of a fin whale.” J. Acoust. Soc. Am., 99(4), 2421–2427.
Lees, S., Hanson, D., Page, E., and Mook, H.(1994a). “Comparison of dosage-dependent effects of beta-aminopropionitrile, sodium fluoride, and hydrocortisone on selected physical properties of cortical bone.” J. Bone Miner. Res., 9(9), 1377–1389.
Lees, S., Heeley, J., and Cleary, P.(1979). “A study of some properties ofa sample of bovine cortical bone using ultrasound.” Calcif. Tissue Int., 29, 107–117.
Lees, S., and Page, E.(1992). “A study of some properties of mineralized turkey leg tendon.” Connect. Tissue Res., 28, 263–287.
Lees, S., Prostak, K., Ingle, V., and Kjoller, K.(1994b). “The loci of mineral in turkey leg tendon as seen by atomic force microscope and electron microscopy.” Calcif. Tissue Int., 55, 180–189.
Lees, S., Tao, N.-J., and Lindsay, M.(1990). “Studies of compact hard tissues and collagen by means of Brillouin light scattering.” Connect. Tissue Res., 24, 187–205.
Luo, G., Kaufman, J., Chiabrera, A., Bianco, B., Kinney, J., Haupt, D., Ryaby, J., and Siffert, R.(1999). “Computational methods for ultrasonic bone assessment.” Ultrasound Med. Biol., 25(5), 823–830;
reprinted with permission of Elsevier Science, Copyright 1999 by World Federation of Ultrasound in Medicine and Biology.
Prostak, K., and Lees, S.(1996). “Visualization of crystal-matrix structure. In situ demineralization of mineralized turkey leg tendon and bone.” Calcif. Tissue Int., 59, 474–479;
reprinted by permission of Springer, p. 478, Fig. 5(a).
Rietbergen, B. v., Müller, R., Ulrich, D., Rüegsegger, P., and Huiskes, R.(1999). “Tissue stresses and strain in trabeculae of a canine proximal femur can be quantified from computer reconstructions.” J. Biomech., 32, 165–173.
Schwefel, H. (1977). Numerische optimierung von computer-modellen mittels der evolution-sstrategie, Birkhäuser, Basel, Switzerland (in German).
Sevostianov, I., and Kachanov, M.(2000). “Impact of the porous microstructure on the overall elastic properties of the osteonal cortical bone.” J. Biomech., 33, 881–888.
Takano, Y., Turner, C., and Burr, D.(1996). “Mineral anisotropy in mineralized tissues is similar among species and mineral growth occurs independently of collagen orientation in rats: Results from acoustic velocity measurements.” J. Bone Miner. Res., 11(9), 1292–1301.
Urist, M., DeLange, R., and Finerman, G.(1983). “Bone cell differentiation and growth factors.” Science, 220, 680–686.
Weiner, S., and Wagner, H.(1998). “The material bone: Structure—mechanical function relations.” Annu. Rev. Mater. Sci., 28, 271–298;
with permission by Annual Reviews, www.AnnualReviews.org
Zaoui, A. (1997). “Structural morphology and constitutive behavior of microheterogeneous materials.” Continuum micromechanics, P. Suquet, ed., Springer, New York, 291–347 (in Suquet).

Information & Authors

Information

Published In

Go to Journal of Engineering Mechanics
Journal of Engineering Mechanics
Volume 128Issue 8August 2002
Pages: 898 - 908

History

Received: Mar 25, 2002
Accepted: Apr 1, 2002
Published online: Jul 15, 2002
Published in print: Aug 2002

Permissions

Request permissions for this article.

Authors

Affiliations

Christian Hellmich
University Assistant, Institute for Strength of Materials, Vienna Univ. of Technology (TU Wien), A-1040 Wien (Vienna), Austria.
Franz-Josef Ulm, M.ASCE
Esther and Harold E. Edgerton Associate Professor, Dept. of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139.

Metrics & Citations

Metrics

Citations

Download citation

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

View Options

Get Access

Access content

Please select your options to get access

Log in/Register Log in via your institution (Shibboleth)
ASCE Members: Please log in to see member pricing

Purchase

Save for later Information on ASCE Library Cards
ASCE Library Cards let you download journal articles, proceedings papers, and available book chapters across the entire ASCE Library platform. ASCE Library Cards remain active for 24 months or until all downloads are used. Note: This content will be debited as one download at time of checkout.

Terms of Use: ASCE Library Cards are for individual, personal use only. Reselling, republishing, or forwarding the materials to libraries or reading rooms is prohibited.
ASCE Library Card (5 downloads)
$105.00
Add to cart
ASCE Library Card (20 downloads)
$280.00
Add to cart
Buy Single Article
$35.00
Add to cart

Get Access

Access content

Please select your options to get access

Log in/Register Log in via your institution (Shibboleth)
ASCE Members: Please log in to see member pricing

Purchase

Save for later Information on ASCE Library Cards
ASCE Library Cards let you download journal articles, proceedings papers, and available book chapters across the entire ASCE Library platform. ASCE Library Cards remain active for 24 months or until all downloads are used. Note: This content will be debited as one download at time of checkout.

Terms of Use: ASCE Library Cards are for individual, personal use only. Reselling, republishing, or forwarding the materials to libraries or reading rooms is prohibited.
ASCE Library Card (5 downloads)
$105.00
Add to cart
ASCE Library Card (20 downloads)
$280.00
Add to cart
Buy Single Article
$35.00
Add to cart

Media

Figures

Other

Tables

Share

Share

Copy the content Link

Share with email

Email a colleague

Share