Skip to main content
Top
Published in: Acta Mechanica Sinica 4/2020

25-07-2020 | Research Paper

Multi-scale mechanotransduction of the poroelastic signals from osteon to osteocyte in bone tissue

Authors: Xiaogang Wu, Chaoxin Li, Kuijun Chen, Yuqin Sun, Weilun Yu, Meizhen Zhang, Yanqin Wang, Yixian Qin, Weiyi Chen

Published in: Acta Mechanica Sinica | Issue 4/2020

Log in

Activate our intelligent search to find suitable subject content or patents.

search-config
loading …

Abstract

In order to quantify the poroelastic mechanical signals conduction and evaluate the biomechanical effectiveness of functional units (osteocyte processes, canaliculi and lacuna) in lacunar-canalicular system (LCS), a multiscale poroelastic finite element model was established by using the Comsol Multiphysics software. The poroelastic mechanical signals (pore pressure, fluid velocity, von-Mises stress, strain) were analyzed inside the osteon-osteocyte system. The effects of osteocyte (OCY)’s shape (ellipse and circle), long axis directions (horizontal and vertical) and mechanical properties (Elastic modulus and permeability) on its poroelastic responses were examined. It is found that the OCY processes is the best mechanosensor compared with the OCY body, lacunae and canaliculi. The mechanotransduction ability of the elliptic shaped OCY is stronger than that of circular shaped. The pore pressure and flow velocity around OCYs increase as the elastic modulus and permeability of OCY increase. The established model can be used for studying the mechanism of bone mechanotransduction at the multiscale level.

Graphic abstract

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

  • über 102.000 Bücher
  • über 537 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Maschinenbau + Werkstoffe
  • Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 390 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Maschinenbau + Werkstoffe




 

Jetzt Wissensvorsprung sichern!

Literature
1.
go back to reference Granke, M., Does, M.D., Nyman, J.S.: The role of water compartments in the material properties of cortical bone. Calcif. Tissue Int. 97, 292–307 (2015) Granke, M., Does, M.D., Nyman, J.S.: The role of water compartments in the material properties of cortical bone. Calcif. Tissue Int. 97, 292–307 (2015)
2.
go back to reference Schaffler, M.B., Cheung, W.Y., Majeska, R., et al.: Osteocytes: master orchestrators of bone. Calcif. Tissue Int. 94, 5–24 (2014) Schaffler, M.B., Cheung, W.Y., Majeska, R., et al.: Osteocytes: master orchestrators of bone. Calcif. Tissue Int. 94, 5–24 (2014)
3.
go back to reference Bonewald, L.F.: The amazing osteocyte. J. Bone Miner. Res. 26, 229–238 (2011) Bonewald, L.F.: The amazing osteocyte. J. Bone Miner. Res. 26, 229–238 (2011)
4.
go back to reference Chen, H., Senda, T., Kubo, K.Y.: The osteocyte plays multiple roles in bone remodeling and mineral homeostasis. Med. Mol. Morphol. 48, 61–68 (2015) Chen, H., Senda, T., Kubo, K.Y.: The osteocyte plays multiple roles in bone remodeling and mineral homeostasis. Med. Mol. Morphol. 48, 61–68 (2015)
5.
go back to reference Yu, B., Pacureanu, A., Oliver, C., et al.: Assessment of the human bone lacuno-canalicular network at the nanoscale and impact of spatial resolution. Sci Rep. 10, 4567 (2020) Yu, B., Pacureanu, A., Oliver, C., et al.: Assessment of the human bone lacuno-canalicular network at the nanoscale and impact of spatial resolution. Sci Rep. 10, 4567 (2020)
6.
go back to reference Tanska, P., Venalainen, M.S., Erdemir, A., et al.: A multiscale framework for evaluating three-dimensional cell mechanics in fibril-reinforced poroelastic tissues with anatomical cell distribution—analysis of chondrocyte deformation behavior in mechanically loaded articular cartilage. J. Biomech. 101, 109648 (2020) Tanska, P., Venalainen, M.S., Erdemir, A., et al.: A multiscale framework for evaluating three-dimensional cell mechanics in fibril-reinforced poroelastic tissues with anatomical cell distribution—analysis of chondrocyte deformation behavior in mechanically loaded articular cartilage. J. Biomech. 101, 109648 (2020)
7.
go back to reference Wu, X.G., Chen, W.Y.: A hollow osteon model for examining its poroelastic behaviors: mathematically modeling an osteon with different boundary cases. Eur. J. Mech. A-Solid 40, 34–49 (2013)MathSciNetMATH Wu, X.G., Chen, W.Y.: A hollow osteon model for examining its poroelastic behaviors: mathematically modeling an osteon with different boundary cases. Eur. J. Mech. A-Solid 40, 34–49 (2013)MathSciNetMATH
8.
go back to reference Wu, X.G., Chen, W.Y., Gao, Z.P., et al.: The effects of Haversian fluid pressure and harmonic axial loading on the poroelastic behaviors of a single osteon. Sci. China-Phys. Mech. Astron. 55, 1646–1656 (2012) Wu, X.G., Chen, W.Y., Gao, Z.P., et al.: The effects of Haversian fluid pressure and harmonic axial loading on the poroelastic behaviors of a single osteon. Sci. China-Phys. Mech. Astron. 55, 1646–1656 (2012)
9.
go back to reference Rémond, A., Naili, S.: Transverse isotropic poroelastic osteon model under cyclic loading. Mech. Res. Commun. 32, 645–651 (2005)MATH Rémond, A., Naili, S.: Transverse isotropic poroelastic osteon model under cyclic loading. Mech. Res. Commun. 32, 645–651 (2005)MATH
10.
go back to reference Nguyen, V.H., Lemaire, T., Naili, S.: Poroelastic behaviour of cortical bone under harmonic axial loading: a finite element study at the osteonal scale. Med. Eng. Phys. 32, 384–390 (2010) Nguyen, V.H., Lemaire, T., Naili, S.: Poroelastic behaviour of cortical bone under harmonic axial loading: a finite element study at the osteonal scale. Med. Eng. Phys. 32, 384–390 (2010)
11.
go back to reference Weinkamer, R., Kollmannsberger, P., Fratzl, P.: Towards a connectomic description of the osteocyte lacunocanalicular network in bone. Curr. Osteoporos Rep. 17, 186–194 (2019) Weinkamer, R., Kollmannsberger, P., Fratzl, P.: Towards a connectomic description of the osteocyte lacunocanalicular network in bone. Curr. Osteoporos Rep. 17, 186–194 (2019)
12.
go back to reference Wang, L.: Solute transport in the bone lacunar-canalicular system (lcs). Curr. Osteoporos Rep. 16, 32–41 (2018) Wang, L.: Solute transport in the bone lacunar-canalicular system (lcs). Curr. Osteoporos Rep. 16, 32–41 (2018)
13.
go back to reference Liu, Y., Chen, B., Yin, D.: Effects of direction and shape of osteocyte lacunae on resisting impact and micro-damage of osteon. J. Mater. Sci. Mater. Med. 28, 38 (2017) Liu, Y., Chen, B., Yin, D.: Effects of direction and shape of osteocyte lacunae on resisting impact and micro-damage of osteon. J. Mater. Sci. Mater. Med. 28, 38 (2017)
14.
go back to reference Wang, L., Dong, J., Xian, C.J.: Strain amplification analysis of an osteocyte under static and cyclic loading: a finite element study. Biomed. Res. Int. 2015, 376474 (2015) Wang, L., Dong, J., Xian, C.J.: Strain amplification analysis of an osteocyte under static and cyclic loading: a finite element study. Biomed. Res. Int. 2015, 376474 (2015)
15.
go back to reference Verbruggen, S.W., Vaughan, T.J., Mcnamara, L.M.: Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J. R. Soc. Interface 9, 2735–2744 (2012) Verbruggen, S.W., Vaughan, T.J., Mcnamara, L.M.: Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J. R. Soc. Interface 9, 2735–2744 (2012)
16.
go back to reference Cowin, S.C.: Bone poroelasticity. J. Biomech. 32, 217–238 (1999) Cowin, S.C.: Bone poroelasticity. J. Biomech. 32, 217–238 (1999)
17.
go back to reference Hove, R.P.V., Nolte, P.A., Vatsa, A., et al.: Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density—is there a role for mechanosensing? Bone 45, 321–329 (2009) Hove, R.P.V., Nolte, P.A., Vatsa, A., et al.: Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density—is there a role for mechanosensing? Bone 45, 321–329 (2009)
18.
go back to reference Joukar, A., Niroomand-Socuii, H., Ghalichi, F.: Numerical simulation of osteocyte cell in response to directional mechanical loadings and mechanotransduction analysis: considering lacunar-canalicular interstitial fluid flow. Comput. Meth. Prog. Biomed. 133, 133–141 (2016) Joukar, A., Niroomand-Socuii, H., Ghalichi, F.: Numerical simulation of osteocyte cell in response to directional mechanical loadings and mechanotransduction analysis: considering lacunar-canalicular interstitial fluid flow. Comput. Meth. Prog. Biomed. 133, 133–141 (2016)
19.
go back to reference Wang, L., Fritton, S.P., Cowin, S.C., et al.: Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J. Biomech. 32, 663–672 (1999) Wang, L., Fritton, S.P., Cowin, S.C., et al.: Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J. Biomech. 32, 663–672 (1999)
20.
go back to reference Gururaja, S., Kim, H.J., Swan, C.C., et al.: Modeling deformation-induced fluid flow in cortical bone’s canalicular-lacunar system. Ann. Biomed. Eng. 33, 7–25 (2005) Gururaja, S., Kim, H.J., Swan, C.C., et al.: Modeling deformation-induced fluid flow in cortical bone’s canalicular-lacunar system. Ann. Biomed. Eng. 33, 7–25 (2005)
21.
go back to reference Yu, W., Wu, X., Cen, H., et al.: Study on the biomechanical responses of the loaded bone in macroscale and mesoscale by multiscale poroelastic fe analysis. Biomed. Eng. Online 18, 122 (2019) Yu, W., Wu, X., Cen, H., et al.: Study on the biomechanical responses of the loaded bone in macroscale and mesoscale by multiscale poroelastic fe analysis. Biomed. Eng. Online 18, 122 (2019)
22.
go back to reference Le Pense, S., Chen, Y.: Contribution of fluid in bone extravascular matrix to strain-rate dependent stiffening of bone tissue—a poroelastic study. J. Mech. Behav. Biomed. Mater. 65, 90–101 (2017) Le Pense, S., Chen, Y.: Contribution of fluid in bone extravascular matrix to strain-rate dependent stiffening of bone tissue—a poroelastic study. J. Mech. Behav. Biomed. Mater. 65, 90–101 (2017)
23.
go back to reference 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) 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)
25.
go back to reference Zhao, S., Liu, H., Li, Y., et al.: Numerical analysis of the flow field in the lacunar-canalicular system under different magnitudes of gravity. Med. Biol. Eng. Comput. 58, 509–518 (2020) Zhao, S., Liu, H., Li, Y., et al.: Numerical analysis of the flow field in the lacunar-canalicular system under different magnitudes of gravity. Med. Biol. Eng. Comput. 58, 509–518 (2020)
26.
go back to reference Burr, D.B., Milgrom, C., Fyhrie, D., et al.: In vivo measurement of human tibial strains during vigorous activity. Bone 18, 405–410 (1996) Burr, D.B., Milgrom, C., Fyhrie, D., et al.: In vivo measurement of human tibial strains during vigorous activity. Bone 18, 405–410 (1996)
27.
go back to reference Rubin, C.T.: Skeletal strain and the functional significance of bone architecture. Calcif. Tissue Int. 36(Suppl), S11–S18 (1984) Rubin, C.T.: Skeletal strain and the functional significance of bone architecture. Calcif. Tissue Int. 36(Suppl), S11–S18 (1984)
28.
go back to reference Burger, E.: Influence of mechanical factors on bone formation, resorption and growth in vitro. Bone 7, 37–56 (1993) Burger, E.: Influence of mechanical factors on bone formation, resorption and growth in vitro. Bone 7, 37–56 (1993)
29.
go back to reference Biot, M.A.: Theory of elasticity and consolidation for a porous anisotropic solid. J. Appl. Phys. 26, 182–185 (1955)MathSciNetMATH Biot, M.A.: Theory of elasticity and consolidation for a porous anisotropic solid. J. Appl. Phys. 26, 182–185 (1955)MathSciNetMATH
30.
go back to reference Cheng, A.-D.: Material coefficients of anisotropic poroelasticity. Int. J. Rock. Mech. Min. 34, 199–205 (1997) Cheng, A.-D.: Material coefficients of anisotropic poroelasticity. Int. J. Rock. Mech. Min. 34, 199–205 (1997)
31.
go back to reference Stern, A.R., Nicolella, D.P.: Measurement and estimation of osteocyte mechanical strain. Bone 54, 191–195 (2013) Stern, A.R., Nicolella, D.P.: Measurement and estimation of osteocyte mechanical strain. Bone 54, 191–195 (2013)
32.
go back to reference Verbruggen, S.W., Vaughan, T.J., Mcnamara, L.M.: Fluid flow in the osteocyte mechanical environment: a fluid-structure interaction approach. Biomech. Model. Mechanobiol. 13, 85–97 (2014) Verbruggen, S.W., Vaughan, T.J., Mcnamara, L.M.: Fluid flow in the osteocyte mechanical environment: a fluid-structure interaction approach. Biomech. Model. Mechanobiol. 13, 85–97 (2014)
33.
go back to reference Nguyen, V.H., Lemaire, T., Naili, S.: Numerical study of deformation-induced fluid flows in periodic osteonal matrix under harmonic axial loading. Comptes Rendus Mecanique 337, 268–276 (2009)MATH Nguyen, V.H., Lemaire, T., Naili, S.: Numerical study of deformation-induced fluid flows in periodic osteonal matrix under harmonic axial loading. Comptes Rendus Mecanique 337, 268–276 (2009)MATH
34.
go back to reference Cavahug-Zuckerman, P., Stout, R.F., Majeska, R.J., et al.: Potential role for a specialized β3 Integrin-based structure on osteocyte processes in bone mechanosensation: novel mechanotransduction structure on osteocyte process. J. Orthopaed. Res. 36, 642–652 (2017) Cavahug-Zuckerman, P., Stout, R.F., Majeska, R.J., et al.: Potential role for a specialized β3 Integrin-based structure on osteocyte processes in bone mechanosensation: novel mechanotransduction structure on osteocyte process. J. Orthopaed. Res. 36, 642–652 (2017)
35.
go back to reference Wu, X.G., Chen, K.J., Wang, Z.W., et al.: An analytical poroelastic model for laboratorial mechanical testing of the articular cartilage (ac). Appl. Math. Mech-Engl. 39, 813–828 (2018)MathSciNetMATH Wu, X.G., Chen, K.J., Wang, Z.W., et al.: An analytical poroelastic model for laboratorial mechanical testing of the articular cartilage (ac). Appl. Math. Mech-Engl. 39, 813–828 (2018)MathSciNetMATH
36.
go back to reference Bonivtch, A.R., Bonewald, L.F., Nicolella, D.P.: Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J. Biomech. 40, 2199–2206 (2007) Bonivtch, A.R., Bonewald, L.F., Nicolella, D.P.: Tissue strain amplification at the osteocyte lacuna: a microstructural finite element analysis. J. Biomech. 40, 2199–2206 (2007)
37.
go back to reference Schneider, P., Ruffoni, D., Larsson, D., et al.: Image-based finite element models for the investigation of osteocyte mechanotransduction. J. Biomech. S436 (2012) Schneider, P., Ruffoni, D., Larsson, D., et al.: Image-based finite element models for the investigation of osteocyte mechanotransduction. J. Biomech. S436 (2012)
38.
go back to reference Wang, L., Dong, J., Xian, C.J.: Computational Investigation on the biomechanical responses of the osteocytes to the compressive stimulus: a poroelastic model. Biomed. Res. Int. 2018, 4071356 (2018) Wang, L., Dong, J., Xian, C.J.: Computational Investigation on the biomechanical responses of the osteocytes to the compressive stimulus: a poroelastic model. Biomed. Res. Int. 2018, 4071356 (2018)
39.
go back to reference Verbruggen, S.W., Vaughan, T.J., Mcnamara, L.M.: Mechanisms of osteocyte stimulation in osteoporosis. J. Mech. Behav. Biomed. Mater. 62, 158–168 (2016) Verbruggen, S.W., Vaughan, T.J., Mcnamara, L.M.: Mechanisms of osteocyte stimulation in osteoporosis. J. Mech. Behav. Biomed. Mater. 62, 158–168 (2016)
40.
go back to reference Mccreadie, B.R., Hollister, S.J.: Strain concentrations surrounding an ellipsoid model of lacunae and osteocytes. Comput. Methods Biomech. Biomed. Eng. 1, 61–68 (1997) Mccreadie, B.R., Hollister, S.J.: Strain concentrations surrounding an ellipsoid model of lacunae and osteocytes. Comput. Methods Biomech. Biomed. Eng. 1, 61–68 (1997)
41.
go back to reference Mccreadie, B.R., Goulet, R.W., Feldkamp, L.A., et al.: Hierarchical structure of bone and micro-computed tomography. Adv. Exp. Med. Biol. 496, 67–83 (2001) Mccreadie, B.R., Goulet, R.W., Feldkamp, L.A., et al.: Hierarchical structure of bone and micro-computed tomography. Adv. Exp. Med. Biol. 496, 67–83 (2001)
42.
go back to reference You, L., Cowin, S.C., Schaffler, M.B., et al.: A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J. Biomech. 34, 1375–1386 (2001) You, L., Cowin, S.C., Schaffler, M.B., et al.: A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J. Biomech. 34, 1375–1386 (2001)
43.
go back to reference Varga, P., Hesse, B., Langer, M., et al.: Synchrotron x-ray phase nano-tomography-based analysis of the lacunar-canalicular network morphology and its relation to the strains experienced by osteocytes in situ as predicted by case-specific finite element analysis. Biomech. Model. Mechanobiol. 14, 267–282 (2015) Varga, P., Hesse, B., Langer, M., et al.: Synchrotron x-ray phase nano-tomography-based analysis of the lacunar-canalicular network morphology and its relation to the strains experienced by osteocytes in situ as predicted by case-specific finite element analysis. Biomech. Model. Mechanobiol. 14, 267–282 (2015)
44.
go back to reference Pidaparti, R.M.V., Naick, P.A., Turner, C.H., et al.: Effect of cement line properties on interface stresses. J. Biomech. 26, 288 (1993) Pidaparti, R.M.V., Naick, P.A., Turner, C.H., et al.: Effect of cement line properties on interface stresses. J. Biomech. 26, 288 (1993)
45.
go back to reference Wittig, N.K., Laugesen, M., Birkbak, M.E., et al.: Canalicular Junctions in the osteocyte lacuno-canalicular network of cortical bone. ACS Nano 13, 6421–6430 (2019) Wittig, N.K., Laugesen, M., Birkbak, M.E., et al.: Canalicular Junctions in the osteocyte lacuno-canalicular network of cortical bone. ACS Nano 13, 6421–6430 (2019)
46.
go back to reference Gatti, V., Azoulay, E.M., Fritton, S.P.: Microstructural changes associated with osteoporosis negatively affect loading-induced fluid flow around osteocytes in cortical bone. J. Biomech. 66, 127–136 (2018) Gatti, V., Azoulay, E.M., Fritton, S.P.: Microstructural changes associated with osteoporosis negatively affect loading-induced fluid flow around osteocytes in cortical bone. J. Biomech. 66, 127–136 (2018)
47.
go back to reference Wilson, Z.D., Kohles, S.S.: Two-dimensional modeling of nanomechanical strains in healthy and diseased single-cells during microfluidic stress applications. J. Nanotechnol. Eng. Med. 1, 21005 (2010) Wilson, Z.D., Kohles, S.S.: Two-dimensional modeling of nanomechanical strains in healthy and diseased single-cells during microfluidic stress applications. J. Nanotechnol. Eng. Med. 1, 21005 (2010)
48.
go back to reference Lee, J.H., Park, H.K., Kim, K.S.: Intrinsic and extrinsic mechanical properties related to the differentiation of mesenchymal stem cells. Biochem. Biophys. Res. Commun. 473, 752–757 (2016) Lee, J.H., Park, H.K., Kim, K.S.: Intrinsic and extrinsic mechanical properties related to the differentiation of mesenchymal stem cells. Biochem. Biophys. Res. Commun. 473, 752–757 (2016)
49.
go back to reference Guo, H., Maher, S.A., Torzilli, P.A.: A biphasic multiscale study of the mechanical microenvironment of chondrocytes within articular cartilage under unconfined compression. J. Biomech. 47, 2721–2729 (2014) Guo, H., Maher, S.A., Torzilli, P.A.: A biphasic multiscale study of the mechanical microenvironment of chondrocytes within articular cartilage under unconfined compression. J. Biomech. 47, 2721–2729 (2014)
50.
go back to reference Alexopoulos, L.G., Setton, L.A., Guilak, F.: The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomater. 1, 317–325 (2005) Alexopoulos, L.G., Setton, L.A., Guilak, F.: The biomechanical role of the chondrocyte pericellular matrix in articular cartilage. Acta Biomater. 1, 317–325 (2005)
Metadata
Title
Multi-scale mechanotransduction of the poroelastic signals from osteon to osteocyte in bone tissue
Authors
Xiaogang Wu
Chaoxin Li
Kuijun Chen
Yuqin Sun
Weilun Yu
Meizhen Zhang
Yanqin Wang
Yixian Qin
Weiyi Chen
Publication date
25-07-2020
Publisher
The Chinese Society of Theoretical and Applied Mechanics; Institute of Mechanics, Chinese Academy of Sciences
Published in
Acta Mechanica Sinica / Issue 4/2020
Print ISSN: 0567-7718
Electronic ISSN: 1614-3116
DOI
https://doi.org/10.1007/s10409-020-00975-y

Other articles of this Issue 4/2020

Acta Mechanica Sinica 4/2020 Go to the issue

Premium Partners