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Poroelastic Evaluation of Fluid Movement Through the Lacunocanalicular System

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Abstract

A poroelastic lacunocanalicular model was developed for the quantification of physiologically relevant parameters related to bone fluid flow. The canalicular and lacunar microstructures were explicitly represented by a dual-continuum poroelastic model. Effective material properties were calculated using the theory of composite materials. Porosity and permeability values were determined using capillaric and spherical-shell models for the canalicular and lacunar microstructures, respectively. Pore fluid pressure and fluid shear stress were calculated in response to simulated mechanical loading applied over a range of frequencies. Species transport was simulated with convective and diffusive flow, and osteocyte consumption of nutrients was incorporated. With the calculated parameter values, realistic pore fluid pressure and fluid shear stress responses were predicted and shown to be consistent with previous experimental and theoretical studies. Stress-induced fluid flow was highlighted as a potent means of species transport, and the importance of high-magnitude low-frequency loading on osteocyte nutrition was demonstrated. This new model can serve as the foundation for future hierarchical modeling efforts that may provide insight into the underlying mechanisms of mechanotransduction and functional adaptation of bone.

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Abbreviations

B :

Skempton’s coefficient; Eq. (8); see Table 1

D :

Species diffusion coefficient; D g = 1.0 × 10−10 m2 s−1

E d :

Drained Young’s modulus; Eq. (6); see Table 1

E s :

Young’s modulus of solid phase; E s = 17.51 GPa

G d :

Drained shear modulus; Eq. (4)

G s :

Shear modulus of solid phase; G s = E s/2(1 + ν s) = 6.56 GPa

J con :

Convective species flux; Eq. (24)

J diff :

Diffusive species flux; Eq. (25)

K d :

Drained bulk modulus; Eq. (3)

K f :

Bulk modulus of the pore fluid; K f = 2.3 GPa

K s :

Bulk modulus of solid phase; K s = E s/3(1 − 2ν s) = 17.66 GPa

L :

Distance from the osteonal canal wall to the cement line; L = r o − r i = 100 μm

R i :

Radius of the osteocyte; R i = 4 μm

R o :

Radius of the lacuna; R o = 5 μm

a :

Radius of the osteocytic process; a = 0.1 μm

b :

Radius of the canaliculus; b = 0.23 μm

c :

Pressure diffusion coefficient (consolidation coefficient)

d :

Cross-sectional width and height of bone section; d = 21 μm

k c :

Bulk permeability of the canalicular material; Eq. (12); see Table 1

k l :

Bulk permeability of the lacunar material; Eq. (13); see Table 1

l :

Lacuna-to-lacuna distance; l = 30 μm

n c :

Canalicular density on the osteonal canal surface; n c = 5.5/100 μm2

p :

Pore fluid pressure

q :

Darcy fluid velocity; Eq. (19)

r i :

Inner radius of the osteon (radius of osteonal canal); r i = 25 μm

r o :

Outer radius of the osteon; r o = 125 μm

α :

Biot’s effective stress coefficient; Eq. (7); see Table 1

μ :

Dynamic viscosity of the pore fluid; μ = 0.001 Pa s

ν s :

Poisson’s ratio of solid phase; ν s = 0.335

ν d :

Drained Poisson’s ratio; Eq. (5); see Table 1

τ :

Shear stress; Eq. (20)

ϕc :

Porosity of the canalicular section with osteocyte process; Eq. (1); ϕc = 0.0074

ϕl :

Porosity of the lacunar section with osteocyte body; Eq. (2); ϕl = 0.119

References

  1. Anderson, E. J., S. Kaliyamoorthy, J. Iwan, D. Alexander, and M. L. Knothe Tate. Nano-microscale models of periosteocytic flow show differences in stresses imparted to cell body and processes. Ann Biomed Eng. 33: 52-62, 2005. doi:10.1007/s10439-005-8962-y

    Article  PubMed  Google Scholar 

  2. Bacabac, R. G., T. H. Smit, M. G. Mullender, J. J. Van Loon, and J. Klein-Nulend. Initial stress-kick is required for fluid shear stress-induced rate dependent activation of bone cells. Ann Biomed Eng. 33: 104-110, 2005. doi:10.1007/s10439-005-8968-5

    Article  PubMed  Google Scholar 

  3. Batra, N. N., Y. J. Li, C. E. Yellowley, L. You, A. M. Malone, C. H. Kim, and C. R. Jacobs. Effects of short-term recovery periods on fluid-induced signaling in osteoblastic cells. J Biomech. 38: 1909-1917, 2005. doi:10.1016/j.jbiomech.2004.08.009

    Article  PubMed  Google Scholar 

  4. Bird, R. B., W. E. Stewart, and E. N. Lightfoot. Transport Phenomena. New York: John Wiley & Sons, 1960.

    Google Scholar 

  5. Brookes, M. The Blood Supply of Bone. Butterworths, London, 1971.

    Google Scholar 

  6. Buechner, P. M., R. S. Lakes, C. Swan, and R. A. Brand. A broadband viscoelastic spectroscopic study of bovine bone: implications for fluid flow. Ann Biomed Eng. 29: 719-728, 2001. doi:10.1114/1.1385813

    Article  PubMed  CAS  Google Scholar 

  7. Chakkalakal, D. A. Mechanoelectric transduction in bone. Journal of Materials Research. 4: 1034-1046, 1989. doi:10.1557/JMR.1989.1034

    Article  Google Scholar 

  8. Christensen, R. M. Mechanics of Composite Materials. New York: Wiley, 1979.

    Google Scholar 

  9. Civan, F., and V. Nguyen. Particle migration and deposition in porous media. In: Handbook of Porous Media, edited by K. Vafai. CRC, 2005, p. 465.

  10. Cooper, R. R., J. W. Milgram, and R. A. Robinson. Morphology of the osteon. An electron microscopic study. J Bone Joint Surg. 48: 1239-1271, 1966.

    PubMed  CAS  Google Scholar 

  11. Cowin, S. C. (1999) Bone poroelasticity. J Biomech. 32: 217-238, 1999. doi:10.1016/S0021-9290(98)00161-4

    Article  PubMed  CAS  Google Scholar 

  12. Detournay, E., and A. H.-D. Cheng. Fundamentals of poroelasticity. In: Comprehensive Rock Engineering: Principles, Practice and Projects, Vol. II, Analysis and Design Method, edited by C. Fairhust. Pergamon Press, 1993, pp. 113–171.

  13. Dullien, F. A. L. Porous Media: Fluid Transport and Pore Structure. New York: Academic Press, 1979.

    Google Scholar 

  14. Fritton, S. P., K. J. McLeod, and C. T. Rubin. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech. 33: 317-325, 2000. doi:10.1016/S0021-9290(99)00210-9

    Article  PubMed  CAS  Google Scholar 

  15. Goulet, G. C., D. M. Cooper, D. Coombe, and R. F. Zernicke. Influence of cortical canal architecture on lacunocanalicular pore pressure and fluid flow. Comput Methods Biomech Biomed Engin. 11: 379-387, 2008. doi:10.1080/10255840701814105

    Article  CAS  Google Scholar 

  16. Goulet, G. C., N. Hamilton, D. Cooper, D. Coombe, D. Tran, R. Martinuzzi, and R. F. Zernicke. Influence of vascular porosity on fluid flow and nutrient transport in loaded cortical bone. J Biomech. 41: 2169-2175, 2008. doi:10.1016/j.jbiomech.2008.04.022

    Article  PubMed  Google Scholar 

  17. Gururaja, S., H. J. Kim, C. C. Swan, R. A. Brand, and R. S. Lakes. Modeling deformation-induced fluid flow in cortical bone’s canalicular-lacunar system. Ann Biomed Eng. 33: 7-25, 2005. doi:10.1007/s10439-005-8959-6

    Article  PubMed  CAS  Google Scholar 

  18. Harding, R. M. Survival in Space: Medical Problems of Manned Spaceflight. London: Routledge, 1989.

    Google Scholar 

  19. Iannacone, W., E. Korostoff, and S. R. Pollack. Microelectrode study of stress-generated potentials obtained from uniform and nonuniform compression of human bone. J Biomed Mater Res. 13: 753-763, 1979. doi:10.1002/jbm.820130507

    Article  PubMed  CAS  Google Scholar 

  20. Klein-Nulend, J., C. M. Semeins, N. E. Ajubi, P. J. Nijweide, and E. H. Burger. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts–correlation with prostaglandin upregulation. Biochem Biophys Res Commun. 217: 640-648, 1995. doi:10.1006/bbrc.1995.2822

    Article  PubMed  CAS  Google Scholar 

  21. Knothe Tate, M. L. 2001 Mixing mechanisms and net solute transport in bone. Ann Biomed Eng. 29: 810-811; author reply 812-816, 2001.

    Article  PubMed  CAS  Google Scholar 

  22. Knothe Tate, M. L., and U. Knothe. An ex vivo model to study transport processes and fluid flow in loaded bone. J Biomech. 33: 247-254, 2000. doi:10.1016/S0021-9290(99)00143-8

    Article  PubMed  CAS  Google Scholar 

  23. Knothe Tate, M. L., U. Knothe, and P. Niederer. Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and functional adaptation. Am J Med Sci. 316: 189-195, 1998. doi:10.1097/00000441-199809000-00007

    Article  PubMed  CAS  Google Scholar 

  24. Knothe Tate, M. L., R. Steck, M. R. Forwood, and P. Niederer. In vivo demonstration of load-induced fluid flow in the rat tibia and its potential implications for processes associated with functional adaptation. J Exp Biol. 203: 2737-2745, 2000.

    PubMed  CAS  Google Scholar 

  25. Kufahl, R. H., and S. Saha. A theoretical model for stress-generated fluid flow in the canaliculi-lacunae network in bone tissue. J Biomech. 23: 171-180, 1990. doi:10.1016/0021-9290(90)90350-C

    Article  PubMed  CAS  Google Scholar 

  26. Li, G. P., J. T. Bronk, K. N. An, and P. J. Kelly. Permeability of cortical bone of canine tibiae. Microvasc Res. 34: 302-310, 1987. doi:10.1016/0026-2862(87)90063-X

    Article  PubMed  CAS  Google Scholar 

  27. Marotti, G., M. Ferretti, F. Remaggi, and C. Palumbo. Quantitative evaluation on osteocyte canalicular density in human secondary osteons. Bone. 16: 125-128, 1995. doi:10.1016/S8756-3282(94)00019-0

    Article  PubMed  CAS  Google Scholar 

  28. Marotti, G., M. A. Muglia, and D. Zaffe. A SEM study of osteocyte orientation in alternately structured osteons. Bone. 6: 331-334, 1985. doi:10.1016/8756-3282(85)90324-2

    Article  PubMed  CAS  Google Scholar 

  29. Maroudas, A., R. A. Stockwell, A. Nachemson, and J. Urban. Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. J Anat. 120: 113-130, 1975.

    PubMed  CAS  Google Scholar 

  30. Neuman, W. F., and M. W. Neuman. The chemical dynamics of bone mineral. Chicago: University of Chicago Press, 1958.

    Google Scholar 

  31. Oballa, V., D. A. Coombe, and W. L. Buchanan. Factors affecting the thermal response of naturally fractured reservoirs. J Can Petrol Tech. 32: 31-42, 1993.

    CAS  Google Scholar 

  32. Petrov, N., and S. R. Pollack. Comparative analysis of diffusive and stress induced nutrient transport efficiency in the lacunar-canalicular system of osteons. Biorheology. 40: 347-353, 2003.

    PubMed  CAS  Google Scholar 

  33. Piekarski, K., and M. Munro. Transport mechanism operating between blood supply and osteocytes in long bones. Nature. 269: 80-82, 1977. doi:10.1038/269080a0

    Article  PubMed  CAS  Google Scholar 

  34. Rubin, C. T., and L. E. Lanyon. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am. 66: 397-402, 1984.

    PubMed  CAS  Google Scholar 

  35. Rubin, C. T., and K. J. McLeod. Promotion of bony ingrowth by frequency-specific, low-amplitude mechanical strain. Clin. Orthop. Relat. Res. 298:165–174, 1994.

    PubMed  Google Scholar 

  36. Salzstein, R. A., and S. R. Pollack. Electromechanical potentials in cortical bone–II. Experimental analysis. J Biomech. 20: 271-280, 1987. doi:10.1016/0021-9290(87)90294-6

    Article  PubMed  CAS  Google Scholar 

  37. Scheidegger, A. E. The Physics of Flow Through Porous Media. Toronto: University of Toronto Press, 1974.

    Google Scholar 

  38. Smit, T. H., J. M. Huyghe, and S. C. Cowin. Estimation of the poroelastic parameters of cortical bone. J Biomech. 35: 829-835, 2002. doi:10.1016/S0021-9290(02)00021-0

    Article  PubMed  Google Scholar 

  39. Tran, D., L. Nghiem, and W. L. Buchanan. Improved iterative coupling of geomechanics with reservoir simulation. Society of Petroleum Engineers. 9: 362-369, 2004.

    Google Scholar 

  40. Wang, L., S. C. Cowin, S. Weinbaum, and S. P. Fritton. Modeling tracer transport in an osteon under cyclic loading. Ann Biomed Eng. 28: 1200-1209, 2000. doi:10.1114/1.1317531

    Article  PubMed  CAS  Google Scholar 

  41. Wang, L., S. P. Fritton, S. C. Cowin, and S. Weinbaum. Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J Biomech. 32: 663-672, 1999. doi:10.1016/S0021-9290(99)00059-7

    Article  PubMed  CAS  Google Scholar 

  42. Weinbaum, S., S. C. Cowin, and Y. Zeng. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. 27: 339-360, 1994. doi:10.1016/0021-9290(94)90010-8

    Article  PubMed  CAS  Google Scholar 

  43. Wilkes, C. H., and M. B. Visscher. Some physiological aspects of bone marrow pressure. J Bone Joint Surg Am. 57: 49-57, 1975.

    PubMed  CAS  Google Scholar 

  44. Zhang, D. Oscillatory pressurization of an animal cell as a poroelastic spherical body. Ann Biomed Eng. 33: 1249-1269, 2005. doi:10.1007/s10439-005-5688-9

    Article  PubMed  Google Scholar 

  45. Zhang, D., S. Weinbaum, and S. C. Cowin. Estimates of the peak pressures in bone pore water. J Biomech Eng. 120: 697-703, 1998. doi:10.1115/1.2834881

    Article  PubMed  CAS  Google Scholar 

  46. Zhang, D., S. Weinbaum, and S. C. Cowin. On the calculation of bone pore water pressure due to mechanical loading. Int J Solids Structures. 35: 4981-4997, 1998. doi:10.1016/S0020-7683(98)00105-X

    Article  Google Scholar 

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Acknowledgments

The authors extend thanks to the Natural Sciences and Engineering Research Council of Canada, Alberta Heritage Foundation for Medical Research, and Wood Professorship in Joint Injury Research for partial funding support.

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Correspondence to Ronald F. Zernicke.

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Goulet, G.C., Coombe, D., Martinuzzi, R.J. et al. Poroelastic Evaluation of Fluid Movement Through the Lacunocanalicular System. Ann Biomed Eng 37, 1390–1402 (2009). https://doi.org/10.1007/s10439-009-9706-1

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