Research advances of fluid bio-mechanics in bone_Journal of Biomedical Engineering

Authors：

CHEN Zebin ,  HUO Bo

School of Aerospace Engineering, Beijing Institute of Technology, Beijing 100081, P.R.China;

Corresponding author：

HUO Bo, Email: huobo@bit.edu.cn

Keywords：

cavity structure; trabecula; lacunar-canalicular system; fluid flow; bone cells

DOI：

10.7507/1001-5515.201611024

Video：

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It has been found for more than one century that when experiencing mechanical loading, the structure of bone will adapt to the changing mechanical environment, which is called bone remodeling. Bone remodeling is charaterized as two processes of bone formation and bone resorption. A large number of studies have confirmed that the shear stress is resulted from interstitial fluid flow within bone cavities under mechanical loading and it is the key factor of stimulating the biological responses of bone cells. This review summarizes the major research progress during the past years, including the biological response of bone cells under fluid flow, the pressure within bone cavities, the theoretical modeling, numerical simulation and experiments about fluid flow within bone, and finally analyzes and predicts the possible tendency in this field in the future.

Citation： CHEN Zebin, HUO Bo. Research advances of fluid bio-mechanics in bone. Journal of Biomedical Engineering, 2017, 34(2): 308-313. doi: 10.7507/1001-5515.201611024 Copy

1.	Wolff J. Das gesetz der transformation der knochen. DMW-Deutsche Medizinische Wochenschrift, 1893, 19(47): 1222-1224.
2.	Ren Li, Yang Pengfei, Wang Zhe, et al. Biomechanical and biophysical environment of bone from the macroscopic to the pericellular and molecular level. J Mech Behav Biomed Mater, 2015, 50: 104-122.
3.	Fehrendt H, Linn T, Hartmann S, et al. Negative influence of a long-term high-fat diet on murine bone architecture. Int J Endocrinol, 2014, 2014: 318924.
4.	Li F F, Chen F L, Wang H, et al. Proteomics based detection of differentially expressed proteins in human osteoblasts subjected to mechanical stress. Biochem Cell Biol, 2013, 91(2): 109-115.
5.	Gong Xiaoyuan, Yang Weidong, Wang Liyun, et al. Prostaglandin E2 modulates F-actin stress fiber in FSS-stimulated MC3T3-E1 cells in a PKA-dependent manner. Acta Biochim Biophys Sin (Shanghai), 2014, 46(1): 40-47.
6.	Cowin S C. Bone poroelasticity. J Biomech, 1999, 32(3): 217-238.
7.	van der Meijden K, Bakker A D, van Essen H W, et al. Mechanical loading and the synthesis of 1, 25(OH)₂D in primary human osteoblasts. J Steroid Biochem Mol Biol, 2016, 156: 32-39.
8.	Pathak J L, Bravenboer N, Luyten F P, et al. Mechanical loading reduces inflammation-induced human osteocyte-to-osteoclast communication. Calcif Tissue Int, 2015, 97(2): 169-178.
9.	Lee K L, Guevarra M D, Nguyen A M, et al. The primary cilium functions as a mechanical and calcium signaling nexus. Cilia, 2015, 4: 7.
10.	Roy B, Das T, Mishra D, et al. Oscillatory shear stress induced calcium flickers in osteoblast cells. Integr Biol (Camb), 2014, 6(3): 289-299.
11.	Jing D, Baik A D, Lu X L, et al. In situ intracellular calcium oscillations in osteocytes in intact mouse long bones under dynamic mechanical loading. FASEB Journal, 2014, 28(4): 1582-1592.
12.	Xu Huiyun, Guan Ying, Wu Jiawei, et al. Polycystin 2 is involved in the nitric oxide production in responding to oscillating fluid shear in MLO-Y4 cells. J Biomech, 2014, 47(2): 387-391.
13.	Obara C, Tomiyama K I, Takizawa K, et al. Characteristics of three-dimensional prospectively isolated mouse bone marrow mesenchymal stem/stromal cell aggregates on nanoculture plates. Cell Tissue Res, 2016, 366(1): 113-127.
14.	Filipowska J, Reilly G C, Osyczka A M. A single short session of media perfusion induces osteogenesis in hBMSCs cultured in porous scaffolds, dependent on cell differentiation stage. Biotechnol Bioeng, 2016, 113(8): 1814-1824.
15.	Du D, Ushida T, Furukawa K S. Influence of cassette design on three-dimensional perfusion culture of artificial bone. J Biomed Mater Res B Appl Biomater, 2015, 103(1): 84-91.
16.	Clarke S A, Choi S Y, Mckechnie M, et al. Osteogenic cell response to 3-D hydroxyapatite scaffolds developed via replication of natural marine sponges. J Mater Sci Mater Med, 2016, 27(2): 22.
17.	Kim J, Bae W G, Choung H W, et al. Multiscale patterned transplantable stem cell patches for bone tissue regeneration. Biomaterials, 2014, 35(33): 9058-9067.
18.	Pan C J, Qin H, Nie Y D, et al. Control of osteoblast cells adhesion and spreading by microcontact printing of extracellular matrix protein patterns. Colloids Surf B Biointerfaces, 2013, 104: 18-26.
19.	Qin Y X, Hu M. Mechanotransduction in musculoskeletal tissue regeneration: effects of fluid flow, loading, and cellular-molecular pathways. Biomed Res Int, 2014, 2014: 863421.
20.	Hu M, Qin Y X. Dynamic fluid flow stimulation on cortical bone and alterations of the gene expressions of osteogenic growth factors and transcription factors in a rat functional disuse model. Arch Biochem Biophys, 2014, 545: 154-161.
21.	Gardinier J, Gangadharan V, Wang L, et al. Hydraulic pressure during fluid flow regulates purinergic signaling and cytoskeleton organization of osteoblasts. Cell Mol Bioeng, 2014, 7(2): 266-277.
22.	Lai X, Price C, Lu X L, et al. Imaging and quantifying solute transport across periosteum: implications for muscle-bone crosstalk. Bone, 2014, 66: 82-89.
23.	Ciani C, Sharma D, Doty S B, et al. Ovariectomy enhances mechanical load-induced solute transport around osteocytes in rat cancellous bone. Bone, 2014, 59: 229-234.
24.	Granke M, Does M D, Nyman J S. The role of water compartments in the material properties of cortical bone. Calcif Tissue Int, 2015, 97(3, SI): 292-307.
25.	Wang L, Wang Y, Han Y, et al. In situ measurement of solute transport in the bone lacunar-canalicular system. Proc Natl Acad Sci U S A, 2005, 102(33): 11911-11916.
26.	Lai X, Price C, Modla S, et al. The dependences of osteocyte network on bone compartment, age, and disease. Bone Res, 2015, 3: 15009.
27.	Cowin S C, Cardoso L. Blood and interstitial flow in the hierarchical pore space architecture of bone tissue. J Biomech, 2015, 48(5, SI): 842-854.
28.	Metzger T A, Kreipke T C, Vaughan T J, et al. The in situ mechanics of trabecular bone marrow: the potential for mechanobiological response. J Biomech Eng, 2015, 137(1). doi: 10.1115/1.4028985.
29.	Wang L Y, Fritton S P, Cowin S C, et al. Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J Biomech, 1999, 32(7): 663-672.
30.	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, 2014, 13(4): 801-812.
31.	Zhao F, Vaughan T J, Mcnamara L M. Multiscale fluid-structure interaction modelling to determine the mechanical stimulation of bone cells in a tissue engineered scaffold. Biomech Model Mechanobiol, 2015, 14(2): 231-243.
32.	Birmingham E, Grogan J A, Niebur G L, et al. Computational modelling of the mechanics of trabecular bone and marrow using fluid structure interaction techniques. Ann Biomed Eng, 2013, 41(4): 814-826.
33.	Fan L, Pei S, Lucas Lu X, et al. A multiscale 3D finite element analysis of fluid/solute transport in mechanically loaded bone. Bone Res, 2016, 4: 16032.
34.	Verbruggen S W, Vaughan T J, Mcnamara L M. Fluid flow in the osteocyte mechanical environment: a fluid-structure interaction approach. Biomech Model Mechanobiol, 2014, 13(1): 85-97.
35.	Vaughan T J, Mullen C A, Verbruggen S W, et al. Bone cell mechanosensation of fluid flow stimulation: a fluid-structure interaction model characterising the role integrin attachments and primary cilia. Biomech Model Mechanobiol, 2015, 14(4): 703-718.

1. Wolff J. Das gesetz der transformation der knochen. DMW-Deutsche Medizinische Wochenschrift, 1893, 19(47): 1222-1224.
2. Ren Li, Yang Pengfei, Wang Zhe, et al. Biomechanical and biophysical environment of bone from the macroscopic to the pericellular and molecular level. J Mech Behav Biomed Mater, 2015, 50: 104-122.
3. Fehrendt H, Linn T, Hartmann S, et al. Negative influence of a long-term high-fat diet on murine bone architecture. Int J Endocrinol, 2014, 2014: 318924.
4. Li F F, Chen F L, Wang H, et al. Proteomics based detection of differentially expressed proteins in human osteoblasts subjected to mechanical stress. Biochem Cell Biol, 2013, 91(2): 109-115.
5. Gong Xiaoyuan, Yang Weidong, Wang Liyun, et al. Prostaglandin E2 modulates F-actin stress fiber in FSS-stimulated MC3T3-E1 cells in a PKA-dependent manner. Acta Biochim Biophys Sin (Shanghai), 2014, 46(1): 40-47.
6. Cowin S C. Bone poroelasticity. J Biomech, 1999, 32(3): 217-238.
7. van der Meijden K, Bakker A D, van Essen H W, et al. Mechanical loading and the synthesis of 1, 25(OH)₂D in primary human osteoblasts. J Steroid Biochem Mol Biol, 2016, 156: 32-39.
8. Pathak J L, Bravenboer N, Luyten F P, et al. Mechanical loading reduces inflammation-induced human osteocyte-to-osteoclast communication. Calcif Tissue Int, 2015, 97(2): 169-178.
9. Lee K L, Guevarra M D, Nguyen A M, et al. The primary cilium functions as a mechanical and calcium signaling nexus. Cilia, 2015, 4: 7.
10. Roy B, Das T, Mishra D, et al. Oscillatory shear stress induced calcium flickers in osteoblast cells. Integr Biol (Camb), 2014, 6(3): 289-299.
11. Jing D, Baik A D, Lu X L, et al. In situ intracellular calcium oscillations in osteocytes in intact mouse long bones under dynamic mechanical loading. FASEB Journal, 2014, 28(4): 1582-1592.
12. Xu Huiyun, Guan Ying, Wu Jiawei, et al. Polycystin 2 is involved in the nitric oxide production in responding to oscillating fluid shear in MLO-Y4 cells. J Biomech, 2014, 47(2): 387-391.
13. Obara C, Tomiyama K I, Takizawa K, et al. Characteristics of three-dimensional prospectively isolated mouse bone marrow mesenchymal stem/stromal cell aggregates on nanoculture plates. Cell Tissue Res, 2016, 366(1): 113-127.
14. Filipowska J, Reilly G C, Osyczka A M. A single short session of media perfusion induces osteogenesis in hBMSCs cultured in porous scaffolds, dependent on cell differentiation stage. Biotechnol Bioeng, 2016, 113(8): 1814-1824.
15. Du D, Ushida T, Furukawa K S. Influence of cassette design on three-dimensional perfusion culture of artificial bone. J Biomed Mater Res B Appl Biomater, 2015, 103(1): 84-91.
16. Clarke S A, Choi S Y, Mckechnie M, et al. Osteogenic cell response to 3-D hydroxyapatite scaffolds developed via replication of natural marine sponges. J Mater Sci Mater Med, 2016, 27(2): 22.
17. Kim J, Bae W G, Choung H W, et al. Multiscale patterned transplantable stem cell patches for bone tissue regeneration. Biomaterials, 2014, 35(33): 9058-9067.
18. Pan C J, Qin H, Nie Y D, et al. Control of osteoblast cells adhesion and spreading by microcontact printing of extracellular matrix protein patterns. Colloids Surf B Biointerfaces, 2013, 104: 18-26.
19. Qin Y X, Hu M. Mechanotransduction in musculoskeletal tissue regeneration: effects of fluid flow, loading, and cellular-molecular pathways. Biomed Res Int, 2014, 2014: 863421.
20. Hu M, Qin Y X. Dynamic fluid flow stimulation on cortical bone and alterations of the gene expressions of osteogenic growth factors and transcription factors in a rat functional disuse model. Arch Biochem Biophys, 2014, 545: 154-161.
21. Gardinier J, Gangadharan V, Wang L, et al. Hydraulic pressure during fluid flow regulates purinergic signaling and cytoskeleton organization of osteoblasts. Cell Mol Bioeng, 2014, 7(2): 266-277.
22. Lai X, Price C, Lu X L, et al. Imaging and quantifying solute transport across periosteum: implications for muscle-bone crosstalk. Bone, 2014, 66: 82-89.
23. Ciani C, Sharma D, Doty S B, et al. Ovariectomy enhances mechanical load-induced solute transport around osteocytes in rat cancellous bone. Bone, 2014, 59: 229-234.
24. Granke M, Does M D, Nyman J S. The role of water compartments in the material properties of cortical bone. Calcif Tissue Int, 2015, 97(3, SI): 292-307.
25. Wang L, Wang Y, Han Y, et al. In situ measurement of solute transport in the bone lacunar-canalicular system. Proc Natl Acad Sci U S A, 2005, 102(33): 11911-11916.
26. Lai X, Price C, Modla S, et al. The dependences of osteocyte network on bone compartment, age, and disease. Bone Res, 2015, 3: 15009.
27. Cowin S C, Cardoso L. Blood and interstitial flow in the hierarchical pore space architecture of bone tissue. J Biomech, 2015, 48(5, SI): 842-854.
28. Metzger T A, Kreipke T C, Vaughan T J, et al. The in situ mechanics of trabecular bone marrow: the potential for mechanobiological response. J Biomech Eng, 2015, 137(1). doi: 10.1115/1.4028985.
29. Wang L Y, Fritton S P, Cowin S C, et al. Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J Biomech, 1999, 32(7): 663-672.
30. 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, 2014, 13(4): 801-812.
31. Zhao F, Vaughan T J, Mcnamara L M. Multiscale fluid-structure interaction modelling to determine the mechanical stimulation of bone cells in a tissue engineered scaffold. Biomech Model Mechanobiol, 2015, 14(2): 231-243.
32. Birmingham E, Grogan J A, Niebur G L, et al. Computational modelling of the mechanics of trabecular bone and marrow using fluid structure interaction techniques. Ann Biomed Eng, 2013, 41(4): 814-826.
33. Fan L, Pei S, Lucas Lu X, et al. A multiscale 3D finite element analysis of fluid/solute transport in mechanically loaded bone. Bone Res, 2016, 4: 16032.
34. Verbruggen S W, Vaughan T J, Mcnamara L M. Fluid flow in the osteocyte mechanical environment: a fluid-structure interaction approach. Biomech Model Mechanobiol, 2014, 13(1): 85-97.
35. Vaughan T J, Mullen C A, Verbruggen S W, et al. Bone cell mechanosensation of fluid flow stimulation: a fluid-structure interaction model characterising the role integrin attachments and primary cilia. Biomech Model Mechanobiol, 2015, 14(4): 703-718.

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