Abstract
This paper presents a theoretical investigation of the multiphysical phenomena that govern cortical bone behaviour. Taking into account the piezoelectricity of the collagen–apatite matrix and the electrokinetics governing the interstitial fluid movement, we adopt a multiscale approach to derive a coupled poroelastic model of cortical tissue. Following how the phenomena propagate from the microscale to the tissue scale, we are able to determine the nature of macroscopically observed electric phenomena in bone.
Similar content being viewed by others
References
Ahn, A., & Grodzinsky, A. (2009). Relevance of collagen piezoelectricity to Wolff’s law: A critical review. Med. Eng. Phys., 31, 733–741.
Anderson, J., & Eriksson, C. (1970). Piezoelectric properties of dry and wet bone. Nature, 227, 491–492.
Aschero, G., Gizdulich, P., & Mango, F. (1999). Statistical characterization of piezoelectric coefficient d23 in cow bone. J. Biomech., 32, 573–577.
Auriault, J. L. (1991). Heterogeneous medium is an equivalent macroscopic description possible? Int. J. Eng. Sci., 29, 785–795.
Auriault, J. L., & Adler, P. M. (1995). Taylor dispersion in porous media: Analysis by multiple scale expansions. Adv. Water Resour., 18, 217–226.
Auriault, J. L., & Sanchez-Palencia, E. (1977). Etude du comportment macroscopique d’un milieu poreux saturé déformable. J. Méc., 16, 575–603.
Bassett, C., Pawluk, R., & Becker, R. (1964). Effects of electric currents on bone in vivo. Nature, 204, 652–654.
Beretta, D., & Pollack, S. (1986). Ion concentration effects on the zeta potential of bone. J. Orthop. Res., 4, 337–341.
Biot, MA (1941). General theory of three-dimensional consolidation. J. Appl. Phys., 12, 155–164.
Buckwalter, J. A., Glimcher, M. J., Cooper, R. R., & Recker, R. (1995a). Bone biology. Part I: Structure, blood supply, cells, matrix, and mineralization. J. Bone Jt. Surg., Am. Vol., 77, 1256–1275.
Buckwalter, J. A., Glimcher, M. J., Cooper, R. R., & Recker, R. (1995b). Bone biology. Part II: Formation, form, modeling, remodeling, and regulation of cell function. J. Bone Jt. Surg., Am. Vol., 77, 1276–1289.
Bur, A. (1976). Measurements of the dynamic piezoelectric properties of bone as a function of temperature and humidity. J. Biomech., 9, 495–507.
Burger, E. H., & Klein-Nulend, J. (1999). Mechanotransduction in bone: Role of the lacuno-canalicular network. FASEB J., 13(Suppl), S101–112.
Burger, E. H., Klein-Nulend, J., & Smit, T. H. (2003). Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon—a proposal. J. Biomech., 36, 1453–1459.
Cochran, G. V. B., Dell, D. G., Palmieri, V. R., Johnson, M. W., Otter, M. W., & Kadaba, M. P. (1989). An improved design of electrodes for measurement of streaming potentials on wet bone in vitro and in vivo. J. Biomech., 22, 745–750.
Cowin, S. C. (1999). Bone poroelasticity. J. Biomech., 32, 217–238.
Cowin, S. C., Weinbaum, S., & Zeng, Y. (1995). A case for bone canaliculi as the anatomical site of strain generated potentials. J. Biomech., 28, 1281–1297.
Cowin, S., Gailani, G., & Benalla, M. (2009). Hierarchical poroelasticity: Movement of interstitial fluid between porosity levels in bones. Philos. Trans. R. Soc. A, 367, 3401–3444.
Crolet, J., & Racila, M. (2009). Elaboration of assumptions for the fluid problem at microscopic scale in sinupros, mathematical model of cortical bone. Math. Comput. Model., 49, 2182–2190.
Derjaguin, B., Churaev, N., & Muller, V. (1987). Surface forces. New York: Plenum.
Fukada, E., & Yasuda, I. (1957). On the piezoelectric effect of bone. J. Phys. Soc. Jpn., 12, 1158–1162.
Funk, R., Monsees, T., & Özkucur, N. (2009). Electromagnetic effects—From cell biology to medicine. Prog. Histochem. Cytochem., 43, 177–264.
Gailani, G., & Cowin, S. (2011). Ramp loading in Russian doll poroelasticity. J. Mech. Phys. Solids, 59, 103–120.
Grodzinsky, A. (1983). Electromechanical and physicochemical properties of connective tissue. Crit. Rev. Biomed. Eng., 9, 133–199.
Guzelsu, N., & Demiray, H. (1979). Electromechanical properties and related models of bone tissues: A review. Int. J. Eng. Sci., 17, 813–851.
Guzelsu, N., & Walsh, W. (1990). Streaming potential of intact wet bone. J. Biomech., 23, 673–685.
Han, Y., Cowin, S. C., Schaffler, M. B., & Weinbaum, S. (2004). Mechanotransduction and strain amplification in osteocyte cell processes. Proc. Natl. Acad. Sci. USA, 101, 16 689–16,694.
Hastings, G., & Mahmud, F. (1988). Electrical effects in bone. J. Biomed. Eng., 10, 515–521.
Hastings, G., ElMessiery, M., & Rakowski, S. (1981). Mechano-electrical properties of bone. Biomaterials, 2, 225–233.
Hunter, R. (1981). Zeta potential in colloid science: principles and applications. San Diego: Academic Press.
Johnson, M., Chakkalakal, D., Harper, R., & Katz, J. (1980). Comparison of the electromechanical effects in wet and dry bone. J. Biomech., 13, 437–442.
Justus, R., & Luft, J. (1970). A mechanochemical hypothesis for bone remodeling induced by mechanical stress. Calcif. Tissue Int., 5, 222–235.
Kaiser, J., Lemaire, T., Naili, S., & Sansalone, V. (2009). Multiscale modelling of fluid flow in charged porous media including cationic exchanges: application to bone tissues. C. R., Méc., 337, 768–775.
Lemaire, T., Moyne, C., Stemmelen, D., & Murad, M. (2002). Electro-chemo-mechanical couplings in swelling clays derived by homogenization: Electroviscous effects and Onsager’s relations. In Poromechanics II (pp. 489–500). Lisse: Balkema Publishers.
Lemaire, T., Naili, S., & Rémond, A. (2006). Multi-scale analysis of the coupled effects governing the movement of interstitial fluid in cortical bone. Biomech. Model. Mechanobiol., 5, 39–52.
Lemaire, T., Moyne, C., & Stemmelen, D. (2007). Modelling of electro-osmosis in clayey materials including ph effects. Phys. Chem. Earth Parts A/B/C, 32, 441–452.
Lemaire, T., Borocin, F., & Naili, S. (2008a). Mechanotransduction of bone remodelling: role of micro-cracks at the periphery of osteons. C. R., Méc., 336, 354–362.
Lemaire, T., Naili, S., & Rémond, A. (2008b). Study of the influence of fibrous pericellular matrix in the cortical interstitial fluid movement. J. Biomech. Eng., 130, 11,001,1–11.
Lemaire, T., Kaiser, J., Naili, S., & Sansalone, V. (2010a). Modelling of the transport in charged porous media including ionic exchanges. Mech. Res. Commun., 37, 495–499.
Lemaire, T., Sansalone, V., & Naili, S. (2010b). Multiphysical modelling of fluid transport through osteo-articular media. An. Acad. Bras. Cienc., 82, 127–144.
Lemaire, T., Capiez-Lernout, E., Kaiser, J., Naili, S., & Sansalone, V. (2011). What is the importance of multiphysical phenomena in bone remodelling signals expression? A multiscale perspective. J. Mech. Behav. Biomed. Mater. (in press).
Martin, R. B. (2002). Is all cortical bone remodeling initiated by microdamage? Bone, 30, 8–13.
Martin, R. B., Burr, D. B., & Sharkey, N. A. (1998). Skeletal tissue mechanics (1st ed.). New York: Springer.
Miara, B., Rohan, E., Zidi, M., & Labat, B. (2005). Piezomaterials for bone regeneration design–homogenization approach. J. Mech. Phys. Solids, 53, 2529–2556.
Moyne, C., & Murad, M. A. (2002). Electro-chemo-mechanical couplings in swelling clays derived from a micro/macro-homogenization procedure. Int. J. Solids Struct., 39, 6159–6190.
Nguyen, V. H., Lemaire, T., & Naili, S. (2009). Anisotropic poroelastic hollow cylinders with damaged periphery under harmonically axial loading: Relevance to bone remodelling. Multidiscip. Model. Mater. Struct., 5, 205–222.
Nguyen, V. H., Lemaire, T., & Naili, S. (2010). Poroelastic behaviour of cortical bone under harmonic axial loading: Theoretical study at the osteonal tissue scale. Med. Eng. Phys., 32, 384–390.
Nguyen, V. H., Lemaire, T., & Naili, S. (2011). Influence of interstitial bone microcracks on strain-induced fluid flow. Biomech. Model. Mechanobiol. doi:10.1007/s10237-011-0287-1.
Otter, M., Goheen, S., & Williams, W. (1988). Streaming potentials in chemically modified bone. J. Orthop. Res., 6, 346–359.
Piccolino, M. (1998). Animal electricity and the birth of electrophysiology: The legacy of Luigi Galvani. Brain Res. Bull., 46, 381–407.
Pollack, S., Petrov, N., Salzstein, R., Brankov, G., & Blagoeva, R. (1984). An anatomical model for streaming potentials in osteons. J. Biomech., 17, 627–636.
Reinish, G., & Nowick, A. (1975). Piezoelectric properties of bone as functions of moisture content. Nature, 253, 626–627.
Rémond, A., & Naili, S. (2005). Transverse isotropic poroelastic osteon model under cyclic loading. Mech. Res. Commun., 32, 645–651.
Rémond, A., Naili, S., & Lemaire, T. (2008). Interstitial fluid flow in the osteon with spatial gradients of mechanical properties: A finite element study. Biomech. Model. Mechanobiol., 7, 487–495.
Salzstein, R. A., & Pollack, S. R. (1987). Electromechanical potentials in cortical bone—ii. Experimental analysis. J. Biomech., 20, 271–280.
Shelley, M. (1818). Frankenstein, or, the modern Prometheus. Lackington, Hughes, Harding, Mavor, & Jones.
Taton, T. (2001). Boning up on biology. Nature, 412, 491–492.
Telega, J., & Wojnar, R. (2000). Flow of electrolyte through porous piezoelectric medium: Macroscopic equations. C. R. Acad. Sci., Sér. 2, Méc. Phys. Chim. Astron., 328, 225–230.
Wang, L., Wang, Y., Han, Y., Henderson, S. C., Majeska, R. J., Weinbaum, S., & Schaffler, M. B. (2005). In situ measurement of solute transport in the bone lacunar-canalicular system. Proc. Natl. Acad. Sci. USA, 102, 11,911–11,916.
Westbroek, I., Ajubi, N. E., Ablas, M. J., Semeins, C. M., Klein-Nulend, J., Burger, E. H., & Nijweide, P. J. (2000). Differential stimulation of prostaglandin g/h synthase-2 in osteocytes and other osteogenic cells by pulsating fluid flow. Biochem. Biophys. Res. Commun., 268, 414–419.
Wolff, J. (1892). Das Gesetz der Transformation der Knochen. Berlin: Hirschwald.
Yasuda, I. (1964). Piezoelectricity of living bone. Kyoto Furitsu Ika Daigaku Zasshi, 53, 2019–2024.
You, L., Cowin, S. C., Schaffler, M. B., & Weinbaum, S. (2001). A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J. Biomech., 34, 1375–1386.
You, L. D., Weinbaum, S., Cowin, S. C., & Schaffler, M. B. (2004). Ultrastructure of the osteocyte process and its pericellular matrix. Anat. Rec. A, 278A(2), 505–513.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lemaire, T., Capiez-Lernout, E., Kaiser, J. et al. A Multiscale Theoretical Investigation of Electric Measurements in Living Bone. Bull Math Biol 73, 2649–2677 (2011). https://doi.org/10.1007/s11538-011-9641-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11538-011-9641-9