Skip to main content

Advertisement

Log in

Dynamic permeability of the lacunar–canalicular system in human cortical bone

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

A new method for the experimental determination of the permeability of a small sample of a fluid-saturated hierarchically structured porous material is described and applied to the determination of the lacunar–canalicular permeability \((K_\mathrm{LC})\) in bone. The interest in the permeability of the lacunar–canalicular pore system (LCS) is due to the fact that the LCS is considered to be the site of bone mechanotransduction due to the loading-driven fluid flow over cellular structures. The permeability of this space has been estimated to be anywhere from \(10^{-17}\;\) to \(10^{-25}\; \hbox {m}^{2}\). However, the vascular pore system and LCS are intertwined, rendering the permeability of the much smaller-dimensioned LCS challenging to measure. In this study, we report a combined experimental and analytical approach that allowed the accurate determination of the \(K_\mathrm{LC}\) to be on the order of \(10^{-22}\; \hbox {m}^{2}\) for human osteonal bone. It was found that the \(K_\mathrm{LC}\) has a linear dependence on loading frequency, decreasing at a rate of \(2 \times 10^{-24}\; \hbox {m}^{2}\)/Hz from 1 to 100 Hz, and using the proposed model, the porosity alone was able to explain 86 % of the \(K_\mathrm{LC}\) variability.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson EJ, Kreuzer SM, Small O, Tate MLK (2008) Pairing computational and scaled physical models to determine permeability as a measure of cellular communication in micro- and nano-scale pericellular spaces. Microfluid Nanofluid 4(3):193–204. doi:10.1007/s10404-007-0156-5

    Article  Google Scholar 

  • Benalla M, Cardoso L, Cowin SC (2012) Analytical basis for the determination of the lacunar-canalicular permeability of bone using cyclic loading. Biomech Model Mechanobiol 11(6):767–780. doi:10.1007/s10237-011-0350-y

    Article  Google Scholar 

  • Beno T, Yoon YJ, Cowin SC, Fritton SP (2006) Estimation of bone permeability using accurate microstructural measurements. J Biomech 39(13):2378–2387. doi:10.1016/j.jbiomech.2005.08.005

    Article  Google Scholar 

  • Cardoso L, Fritton SP, Gailani G, Benalla M, Cowin SC (2013) Advances in assessment of bone porosity, permeability and interstitial fluid flow. J Biomech 46(2):253–265. doi:10.1016/j.jbiomech.2012.10.025

    Article  Google Scholar 

  • Carter Y, Thomas CD, Clement JG, Peele AG, Hannah K, Cooper DM (2013) Variation in osteocyte lacunar morphology and density in the human femur-a synchrotron radiation micro-CT study. Bone 52(1):126–132. doi:10.1016/j.bone.2012.09.010

    Article  Google Scholar 

  • Cowin SC, Gailani G, Benalla M (2009) Hierarchical poroelasticity: movement of interstitial fluid between porosity levels in bones. Philos Transact A Math Phys Eng Sci 367(1902):3401–3444. doi:10.1098/rsta2009.0099

    Article  MATH  MathSciNet  Google Scholar 

  • Dillaman RM (1984) Movement of ferritin in the 2-day-old chick femur. Anat Rec 209(4):445–453. doi:10.1002/ar.1092090404

    Article  Google Scholar 

  • Fritton SP, Weinbaum S (2009) Fluid and solute transport in bone: flow-induced mechanotransduction. Annu Rev Fluid Mech 41:347–374. doi:10.1146/annurev.fluid.010908.165136

    Article  Google Scholar 

  • Gailani G, Benalla M, Mahamud R, Cowin SC, Cardoso L (2009) Experimental determination of the permeability in the lacunar-canalicular porosity of bone. J Biomech Eng 131(10):101007. doi:10.1115/1.3200908

    Article  Google Scholar 

  • Gailani G, Cowin SC (2008) The unconfined compression of a porous annular cylindrical disk. J Mech Mater 40(6):507–523

    Article  Google Scholar 

  • Gailani G, Cowin SC (2011) Ramp loading in Russian doll poroelasticity. J Mech Phys Solids 53:103–120

    Article  MathSciNet  Google Scholar 

  • Galli M, Oyen ML (2009) Fast identification of poroelastic parameters from indentation test. Comput Model Eng Sci 48:241–270

    Google Scholar 

  • Gardinier JD, Townend CW, Jen KP, Wu Q, Duncan RL, Wang L (2010) In situ permeability measurement of the mammalian lacunar-canalicular system. Bone 46(4):1075–1081. doi:10.1016/j.bone.2010.01.371

    Article  Google Scholar 

  • Goulet GC, Coombe D, Martinuzzi RJ, Zernicke RF (2009) Poroelastic evaluation of fluid movement through the lacunocanalicular system. Ann Biomed Eng 37(7):1390–1402. doi:10.1007/s10439-009-9706-1

    Article  Google Scholar 

  • Gururaja S, Kim HJ, Swan CC, Brand RA, Lakes RS (2005) Modeling deformation-induced fluid flow in cortical bone’s canalicular-lacunar system. Ann Biomed Eng 33(1):7–25

    Article  Google Scholar 

  • Hannah KM, Thomas CDL, Clement JG, De Carlo F, Peele AG (2010) Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 47(5):866–871. doi:10.1016/j.bone.2010.07.025

    Article  Google Scholar 

  • Johnson MW (1984) Behavior of fluid in stressed bone and cellular stimulation. Calcif Tissue Int 36(Suppl 1):S72–76

    Article  Google Scholar 

  • Kameo Y, Adachi T, Sato N, Hojo M (2010) Estimation of bone permeability considering the morphology of lacuno-canalicular porosity. J Mech Behav Biomed Mater 3(3):240–248. doi:10.1016/j.jmbbm.2009.10.005

    Article  Google Scholar 

  • Lemaire T, Lemonnier S, Naili S (2012) On the paradoxical determinations of the lacuno-canalicular permeability of bone. Biomech Model Mechanobiol. doi:10.1007/s10237-011-0363-6

  • Lemaire T, Naili S, Remond A (2008) Study of the influence of fibrous pericellular matrix in the cortical interstitial fluid movement with hydroelectrochemical effects. J Biomech Eng 130(1):011001. doi:10.1115/1.2838025

    Article  Google Scholar 

  • Li GP, Bronk JT, An KN, Kelly PJ (1987) Permeability of cortical bone of canine tibiae. Microvasc Res 34(3):302–310

    Article  Google Scholar 

  • Lin Y, Xu S (2011) AFM analysis of the lacunar-canalicular network in demineralized compact bone. J Microsc 241(3):291–302. doi:10.1111/j.1365-2818.2010.03431.x

    Article  Google Scholar 

  • Malachanne E, Dureisseix D, Canadas P, Jourdan F (2008) Experimental and numerical identification of cortical bone permeability. J Biomech 41(3):721–725. doi:10.1016/j.jbiomech.2007.09.028

    Article  Google Scholar 

  • Marotti G (1990) The original contributions of the scanning electron microscope to the knowledge of bone structure. In: Bonucci E, Motta PM (eds) Ultrastructure of skeletal tissues. Boston, Kluwer Academic:19–39

  • Marotti G (1996) The structure of bone tissues and the cellular control of their deposition. Ital J Anat Embryol 101(4):25–79

    Google Scholar 

  • Marotti G, Ferretti M, Remaggi F, Palumbo C (1995) Quantitative evaluation on osteocyte canalicular density in human secondary osteons. Bone 16(1):125–128

    Article  Google Scholar 

  • Marotti G, Muglia MA, Zaffe D (1985) A SEM study of osteocyte orientation in alternately structured osteons. Bone 6(5):331–334

    Article  Google Scholar 

  • Martin-Badosa E, Amblard D, Nuzzo S, Elmoutaouakkil A, Vico L, Peyrin F (2003) Excised bone structures in mice: imaging at three-dimensional synchrotron radiation micro CT. Radiology 229(3):921–928. doi:10.1148/radiol.2293020558

    Article  Google Scholar 

  • Matsumoto T, Yoshino M, Asano T, Uesugi K, Todoh M, Tanaka M (2006) Monochromatic synchrotron radiation muCT reveals disuse-mediated canal network rarefaction in cortical bone of growing rat tibiae. J Appl Physiol 100(1):274–280. doi:10.1152/japplphysiol.00495.2005

    Article  Google Scholar 

  • McCreadie BR, Hollister SJ, Schaffler MB, Goldstein SA (2004) Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech 37(4):563–572. doi:10.1016/S0021-9290(03)00287-2

    Article  Google Scholar 

  • Neuman WF, Toribara TY, Mulryan BJ (1953) The surface chemistry of bone 7. The hydration shell. J Am Chem Soc 75(17):4239– 4242

    Article  Google Scholar 

  • Orias AAE, Deuerling JM, Landrigan MD, Renaud JE, Roeder RK (2009) Anatomic variation in the elastic anisotropy of cortical bone tissue in the human femur. J Mech Behav Biomed 2(3):255–263. doi:10.1016/j.jmbbm.2008.08.005

    Article  Google Scholar 

  • Oyen ML (2008) Poroelastic nanoindentation responses of hydrated bone. J Mater Res 23(5):1307–1314. doi:10.1557/Jmr2008.0156

    Article  Google Scholar 

  • Palacio-Mancheno PE, Larriera AI, Doty SB, Cardoso L, Fritton SP (2013) 3D assessment of cortical bone porosity and tissue mineral density using high-resolution micro-CT: effects of resolution and threshold method. J Bone Miner Res. doi:10.1002/jbmr.2012

  • Remaggi F, Cane V, Palumbo C, Ferreti M (1998) Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel fibered bones. Ital J Anat Embryol 103, 145–155

    Google Scholar 

  • Rouhana SW, Johnson MW, Chakkalakal DA, Harper RA (1981) Permeability of the osteocyte lacunocanalicular compact bone. Joint ASME ASCE Conf Biomech Symp AMD 43:169–172

    Google Scholar 

  • Schneider P, Meier M, Wepf R, Muller R (2011) Serial FIB/SEM imaging for quantitative 3D assessment of the osteocyte lacuno-canalicular network. Bone 49(2):304–311. doi:10.1016/j.bone.2011.04.005

    Article  Google Scholar 

  • Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, Muller R (2007) Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and Nano-CT. J Bone Miner Res 22(10):1557–1570. doi:10.1359/Jbmr.070703

    Google Scholar 

  • Sharma D, Ciani C, Marin PAR, Levy JD, Doty SB, Fritton SP (2012) Alterations in the osteocyte lacunar-canalicular microenvironment due to estrogen deficiency. Bone 51(3):488–497. doi:10.1016/j.bone.2012.05.014

    Google Scholar 

  • Smit TH, Huyghe JM, Cowin SC (2002) Estimation of the poroelastic parameters of cortical bone. J Biomech 35(6):829–835

    Article  Google Scholar 

  • Souzanchi MF, Palacio-Mancheno P, Borisov YA, Cardoso L, Cowin SC (2012) Microarchitecture and bone quality in the human calcaneus: local variations of fabric anisotropy. J Bone Miner Res 27(12):2562–2572. doi:10.1002/jbmr.1710

    Article  Google Scholar 

  • Sugawara Y, Ando R, Kamioka H, Ishihara Y, Honjo T, Kawanabe N, Kurosaka H, Takano-Yamamoto T, Yamashiro T (2011) The three-dimensional morphometry and cell-cell communication of the osteocyte network in chick and mouse embryonic calvaria. Calcif Tissue Int 88(5):416–424. doi:10.1007/s00223-011-9471-7

    Article  Google Scholar 

  • Sugawara Y, Kamioka H, Honjo T, Tezuka K, Takano-Yamamoto T (2005) Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone 36(5):877–883. doi:10.1016/j.bone.2004.10.008

    Article  Google Scholar 

  • Swan CC, Lakes RS, Brand RA, Stewart KJ (2003) Micromechanically based poroelastic modeling of fluid flow in Haversian bone. J Biomech Eng 125(1):25–37

    Article  Google Scholar 

  • Tommasini SM, Trinward A, Acerbo AS, De Carlo F, Miller LM, Judex S (2012) Changes in intracortical microporosities induced by pharmaceutical treatment of osteoporosis as detected by high resolution micro-CT. Bone 50(3):596–604. doi:10.1016/j.bone.2011.12.012

    Article  Google Scholar 

  • Wagner DW, Lindsey DP, Beaupre GS (2011) Deriving tissue density and elastic modulus from microCT bone scans. Bone 49(5):931–938

    Article  Google Scholar 

  • Wang L, Fritton SP, Cowin SC, Weinbaum S (1999) Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J Biomech 32(7):663–672

    Article  Google Scholar 

  • Wehrli FW, Fernandez-Seara MA (2005) Nuclear magnetic resonance studies of bone water. Ann Biomed Eng 33(1):79–86

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wen D, Androjna C, Vasanji A, Belovich J, Midura RJ (2010) Lipids and collagen matrix restrict the hydraulic permeability within the porous compartment of adult cortical bone. Ann Biomed Eng 38(3):558–569. doi:10.1007/s10439-009-9858-z

    Article  Google Scholar 

  • Windahl SH, Vidal O, Andersson G, Gustafsson JA, Ohlsson C (1999) Increased cortical bone mineral content but unchanged trabecular bone mineral density in female ERbeta(-/-) mice. J Clin Invest 104(7):895–901. doi:10.1172/JCI6730

    Article  Google Scholar 

  • You L, Cowin SC, Schaffler MB, Weinbaum S (2001) A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34(11):1375–1386

    Article  Google Scholar 

  • You LD, Weinbaum S, Cowin SC, Schaffler MB (2004) Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A Discov Mol Cell Evol Biol 278(2):505–513. doi:10.1002/ar.a.20050

    Article  Google Scholar 

  • Zhang D, Weinbaum S, Cowin SC (1998) Estimates of the peak pressures in bone pore water. J Biomech Eng 120(6):697–703

    Article  Google Scholar 

  • Zhou X, Novotny JE, Wang L (2008) Modeling fluorescence recovery after photobleaching in loaded bone: potential applications in measuring fluid and solute transport in the osteocytic lacunar-canalicular system. Ann Biomed Eng 36(12):1961–1977. doi:10.1007/s10439-008-9566-0

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by NSF (PHY-0848491, CMMI-1333560, MRI-0723027, and 1229449), NIH/NIA (AG34198), PSC-CUNY Research Award Program of the City University of New York and by a fellowship from the CUNY Graduate Center.

Conflict of interest

All authors state that they have no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. C. Cowin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benalla, M., Palacio-Mancheno, P.E., Fritton, S.P. et al. Dynamic permeability of the lacunar–canalicular system in human cortical bone. Biomech Model Mechanobiol 13, 801–812 (2014). https://doi.org/10.1007/s10237-013-0535-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-013-0535-7

Keywords

Navigation