Skip to main content
Log in

The role of fluid flow on bone mechanobiology: mathematical modeling and simulation

  • Original Paper
  • Published:
Computational Geosciences Aims and scope Submit manuscript

Abstract

The effect of fluid flow on tissue adaptation was the focus of many research works during the last years. Moreover, the use of poroelasticity models to simulate and understand the interstitial flow movement has taken interest due to the possibility to include the fluid effect on mechanical simulations. In particular, shear stresses induced by bone canalicular fluid flow are suggested to be one of the mechanical stimulus controlling bone remodeling processes. Due to the high difficulty to measure canalicular fluid flow and shear stresses, computational poroelastic models can be used in order to estimate these parameters. In this work, a finite element dual porosity model based on Russian doll poroelasticity is developed. Two experiments with a turkey ulna and a human femur are simulated. Bone lacuno-canalicular fluid flow is computed and compared with the experimental results, focusing on the zones of bone remodeling and showing a relation between this flow and the bone formation process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Anderson, E.J., Kaliyamoorthy, S., Alexander, J.I.D., Knothe Tate, M.L.: Nano-microscale models of periosteocytic flow show differences in stresses imparted to cell body processes. Ann. Biomed. Eng. 33, 52–62 (2005)

    Article  Google Scholar 

  2. Anderson, E.J., Knothe Tate, M.L.: Idealization of pericellular fluid space geometry and dimension results in a profound underprediction of nano-microscale stresses imparted by fluid drag on osteocytes. J. Biomech. 41, 1736–1746 (2008)

    Article  Google Scholar 

  3. Bacabac, R.G., Smit, T.H., Mullender, M.G., Van Loon, J.J.W.A., Klein-Nulend, J.: Initial stress-kick is required for fluid shear stress-induced rate dependent activation bone cells. I. Ann. Biomed. Eng. 33, 104–110 (2005)

    Article  Google Scholar 

  4. Beno, T., Yoon, Y., Cowin, S.C., Fritton, S.P.: Estimation of bone permeability using accurate microstructural measurements. J. Biomech. 39, 2378–2387 (2006)

    Article  Google Scholar 

  5. Britz, H.M., Thomas, C.D.L., Clement, J.G., Cooper, D.M.: The relation of femoral osteon geometry to age, sex, height and weight. Bone 45(1), 77–83 (2009)

    Article  Google Scholar 

  6. Burger, E.H., Klein-Nulend, J., Smit, T.H.: Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon - a proposal. J. Biomech. 36, 1453–1459 (2003)

    Article  Google Scholar 

  7. Cardoso, L., Fritton, S.P., Gailani, G., Benalla, M., Cowin, S.C.: Advances in assessment of bone porosity, permeability and interstitial fluid flow. J. Biomech. 46(2), 253–265 (2013)

    Article  Google Scholar 

  8. Cowin, S.: Bone poroelasticity. J. Biomech. 32, 217–238 (1999)

    Article  Google Scholar 

  9. Cowin, S.: Mechanosensation and fluid transport in living bone. J. Muskuloske Neuron. Interact. 2, 256–260 (2002)

    Google Scholar 

  10. Cowin, S.C., Cardoso, L.: Blood and interstitial flow in the hierarchical pore space architecture of bone tissue. J. Biomech. 48(5), 842–854 (2015)

    Article  Google Scholar 

  11. Cowin, S.C., Gailani, G., Benalla, M.: Hierarchical poroelasticity: movement of interstitial fluid between porosity levels in bones. Philos. Trans. Royal Soc. A 367(1902), 3401–3444 (2009)

    Article  Google Scholar 

  12. Cowin, S.C., Hegedus, D.H.: Bone remodeling I: theory of adaptive elasticity. J. Elast. 6(3), 313–326 (1976)

    Article  Google Scholar 

  13. Fornells, P., García-Aznar, J.M., Doblaré, M.: A finite element dual porosity approach to model deformation-induced fluid flow in cortical bone. Ann. Biomed. Eng. 35, 1687–1698 (2007)

    Article  Google Scholar 

  14. Fritton, S.P., Weinbaum, S.: Fluid and solute transport in bone: flow-induced mechanotransduction. Annu. Rev. Fluid Mech. 41(1), 347–374 (2009)

    Article  Google Scholar 

  15. Gailani, G., Cowin, S.: Ramp loading in Russian doll poroelasticity. J. Mech. Phys. Solids 59(1), 103–120 (2011)

    Article  Google Scholar 

  16. Gururaja, S., Kim, H.J., Swan, C.C., Brand, R.A., Lakes, R.S.: Modeling deformation-induced fluid flow in cortical bone’s canalicular-lacunar system. Ann. Biomed. Eng. 33, 7–25 (2005)

    Article  Google Scholar 

  17. Harrigan, T.P., Hamilton, J.J.: Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications. J. Biomech. 26(2), 183–200 (1993)

    Article  Google Scholar 

  18. Kumar, N.C., Dantzig, J., Jasiuk, I.: Modeling of cortical bone adaptation in a rat ulna: effect of frequency. Bone 50(3), 792–797 (2012)

    Article  Google Scholar 

  19. Mak, A.F.T., Huang, D.T., Zhang, J.D., Tong, P.: Deformation induced hierarchical flows and drag forces in bone canaliculi and matrix microporosity. J. Biomech. 30, 11–18 (1997)

    Article  Google Scholar 

  20. Pereira, A.F., Javaheri, B., Pitsillides, A.A., Shefelbine, S.J.: Predicting cortical bone adaptation to axial loading in the mouse tibia. J. Royal Soc. Interface 12(110), 20150590 (2015)

    Article  Google Scholar 

  21. Pereira, A.F., Shefelbine, S.J.: The influence of load repetition in bone mechanotransduction using poroelastic finite-element models: the impact of permeability. Biomech. Model. Mechanobiol. 13(1), 215–225 (2014)

    Article  Google Scholar 

  22. Qin, Y., Rubin, C.T., McLeod, K.J.: Nonlinear dependence of loading intensity and cycle number in the maintenance of bone mass and morphology. J. Orthop. Res. 16, 482–489 (1998)

    Article  Google Scholar 

  23. Smit, T.H., Burger, E.H., Huyghe, J.M.: A case for strain-induced fluid flow as regulator of BMU-coupling and osteonal alignment. J. Bone Miner. Res. 17, 2021–2029 (2002)

    Article  Google Scholar 

  24. Steck, R., Niederer, P., Knothe Tate, M.L.: A finite element analysis for the prediction of load-induced fluid flow and mechanochemical transduction in bone. J. Theor. Biol. 220, 249–259 (2003)

    Article  Google Scholar 

  25. Wang, L., Fritton, S.P., Cowin, S.C., Weinbaum, S.: Fluid pressure relaxation depends upon osteon microstructure: modelling an oscillatory bending experiment. J. Biomech. 32, 663–672 (1999)

    Article  Google Scholar 

  26. Weinbaum, S., Cowin, S., Zeng, Y.: A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J. Biomech. 27(3), 339–360 (1994)

    Article  Google Scholar 

  27. Wolff, J.: Das Gesetz Der Transformation Der Knochen. Hirschwald, Berlin (1892)

    Google Scholar 

  28. Zhang, D., Weinbaum, S., Cowin, S.C.: Estimates of the peak pressures in bone pore water. J. Biomech. Eng. 120, 697–703 (1998)

    Article  Google Scholar 

Download references

Funding

This study is supported by the Spanish Ministry of Economy and Competitiveness throug research projects DPI2017-84780-C2-1-R, and RTI2018-094494-B393C21, and by Aragón Government (T50_17R).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Teresa Sánchez.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sánchez, M.T., Pérez, M.Á. & García-Aznar, J.M. The role of fluid flow on bone mechanobiology: mathematical modeling and simulation. Comput Geosci 25, 823–830 (2021). https://doi.org/10.1007/s10596-020-09945-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10596-020-09945-6

Keywords

Navigation