Trabecular bone remodelling simulation considering osteocytic response to fluid-induced shear stress

In bone functional adaptation by remodelling, osteocytes in the lacuno-canalicular system are believed to play important roles in the mechanosensory system. Under dynamic loading, bone matrix deformation generates an interstitial fluid flow in the lacuno-canalicular system; this flow induces shear stress on the osteocytic process membrane that is known to stimulate the osteocytes. In this sense, the osteocytes behave as mechanosensors and deliver mechanical information to neighbouring cells through the intercellular communication network. In this study, bone remodelling is assumed to be regulated by the mechanical signals collected by the osteocytes. From the viewpoint of multi-scale biomechanics, we propose a mathematical model of trabecular bone remodelling that takes into account the osteocytic mechanosensory network system. Based on this model, a computational simulation of trabecular bone remodelling was conducted for a single trabecula under cyclic uniaxial loading, demonstrating functional adaptation to the applied mechanical loading as a load-bearing construct.

[1]  J. Wolff Das Gesetz der Transformation der Knochen , 1893 .

[2]  J. Sethian,et al.  Fronts propagating with curvature-dependent speed: algorithms based on Hamilton-Jacobi formulations , 1988 .

[3]  H. Grootenboer,et al.  Adaptive bone-remodeling theory applied to prosthetic-design analysis. , 1987, Journal of biomechanics.

[4]  L. S. Matthews,et al.  Trabecular bone remodeling: an experimental model. , 1991, Journal of biomechanics.

[5]  S. Cowin,et al.  Candidates for the mechanosensory system in bone. , 1991, Journal of biomechanical engineering.

[6]  Sheldon Weinbaum,et al.  Viscous flow in a channel with periodic cross-bridging fibres: exact solutions and Brinkman approximation , 1991, Journal of Fluid Mechanics.

[7]  S C Cowin,et al.  Bone stress adaptation models. , 1993, Journal of biomechanical engineering.

[8]  A. Cheng,et al.  Fundamentals of Poroelasticity , 1993 .

[9]  S. Cowin,et al.  A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. , 1994, Journal of biomechanics.

[10]  H Weinans,et al.  A physiological approach to the simulation of bone remodeling as a self-organizational control process. , 1994, Journal of biomechanics.

[11]  A. Parfitt Osteonal and hemi‐osteonal remodeling: The spatial and temporal framework for signal traffic in adult human bone , 1994, Journal of cellular biochemistry.

[12]  H J Donahue,et al.  Cell‐to‐cell communication in osteoblastic networks: Cell line–dependent hormonal regulation of gap junction function , 1995, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[13]  R. Huiskes,et al.  Proposal for the regulatory mechanism of Wolff's law , 1995, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[14]  P. Nijweide,et al.  Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts--correlation with prostaglandin upregulation. , 1995, Biochemical and biophysical research communications.

[15]  A. van der Plas,et al.  Sensitivity of osteocytes to biomechanical stress in vitro , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[16]  R Huiskes,et al.  Osteocytes and bone lining cells: which are the best candidates for mechano-sensors in cancellous bone? , 1997, Bone.

[17]  J. Gupta A Theoretical Framework , 1997 .

[18]  R E Guldberg,et al.  Trabecular bone adaptation to variations in porous-coated implant topology. , 1997, Journal of biomechanics.

[19]  Masao Tanaka,et al.  Simulation of Trabecular Surface Remodeling based on Local Stress Nonuniformity. , 1997 .

[20]  P A Hill,et al.  Bone Remodelling , 1998, British journal of orthodontics.

[21]  T. Adachi,et al.  Uniform stress state in bone structure with residual stress. , 1998, Journal of biomechanical engineering.

[22]  M. Longair The Theoretical Framework , 1998 .

[23]  P. Niederer,et al.  Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and functional adaptation. , 1998, The American journal of the medical sciences.

[24]  S. Cowin Bone poroelasticity. , 1999, Journal of biomechanics.

[25]  J. Klein-Nulend,et al.  MECHANOTRANSDUCTION IN BONE : ROLE OF THE LACUNOCANALICULAR NETWORK , 1999 .

[26]  Herbert F. Wang Theory of Linear Poroelasticity with Applications to Geomechanics and Hydrogeology , 2000 .

[27]  Rik Huiskes,et al.  Effects of mechanical forces on maintenance and adaptation of form in trabecular bone , 2000, Nature.

[28]  S J Hollister,et al.  Trabecular surface remodeling simulation for cancellous bone using microstructural voxel finite element models. , 2001, Journal of biomechanical engineering.

[29]  S. Cowin,et al.  A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. , 2001, Journal of biomechanics.

[30]  T. Takano-Yamamoto,et al.  A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. , 2001, Bone.

[31]  Theo H Smit,et al.  Estimation of the poroelastic parameters of cortical bone. , 2002, Journal of biomechanics.

[32]  Taiji Adachi,et al.  Functional adaptation of cancellous bone in human proximal femur predicted by trabecular surface remodeling simulation toward uniform stress state. , 2002, Journal of biomechanics.

[33]  Taiji Adachi,et al.  Changes in the Fabric and Compliance Tensors of Cancellous Bone due to Trabecular Surface Remodeling, Predicted by a Digital Image-based Model , 2004, Computer methods in biomechanics and biomedical engineering.

[34]  S. Cowin,et al.  Ultrastructure of the osteocyte process and its pericellular matrix. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[35]  Taiji Adachi,et al.  Spatial and temporal regulation of cancellous bone structure: characterization of a rate equation of trabecular surface remodeling. , 2005, Medical engineering & physics.

[36]  M G Mullender,et al.  Mechanobiology of bone tissue. , 2005, Pathologie-biologie.

[37]  Z. Jaworski,et al.  The rate of osteoclastic bone erosion in Haversian remodeling sites of adult dog's rib , 2005, Calcified Tissue Research.

[38]  R Huiskes,et al.  A theoretical framework for strain-related trabecular bone maintenance and adaptation. , 2005, Journal of biomechanics.

[39]  Teruko Takano-Yamamoto,et al.  Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. , 2005, Bone.

[40]  Stephen C Cowin,et al.  Estimation of bone permeability using accurate microstructural measurements. , 2006, Journal of biomechanics.

[41]  Taiji Adachi,et al.  Simulation Study on Local and Integral Mechanical Quantities at Single Trabecular Level as Candidates of Remodeling Stimuli , 2006 .

[42]  Patrick J Prendergast,et al.  Bone remodelling algorithms incorporating both strain and microdamage stimuli. , 2007, Journal of biomechanics.

[43]  S. Cowin The significance of bone microstructure in mechanotransduction. , 2007, Journal of biomechanics.

[44]  S. Weinbaum,et al.  A model for the role of integrins in flow induced mechanotransduction in osteocytes , 2007, Proceedings of the National Academy of Sciences.

[45]  Qiaobing Xu,et al.  Fluid Flow Induced Calcium Response in Bone Cell Network , 2008, Cellular and molecular bioengineering.

[46]  Yoshitaka Kameo,et al.  Transient response of fluid pressure in a poroelastic material under uniaxial cyclic loading , 2008 .

[47]  P. Prendergast,et al.  An algorithm for bone mechanoresponsiveness: implementation to study the effect of patient-specific cell mechanosensitivity on trabecular bone loss , 2008, Computer methods in biomechanics and biomedical engineering.

[48]  Mark L. Johnson,et al.  Osteocytes, mechanosensing and Wnt signaling. , 2008, Bone.

[49]  In Gwun Jang,et al.  Computational study of Wolff's law with trabecular architecture in the human proximal femur using topology optimization. , 2008, Journal of biomechanics.

[50]  Masaki Hojo,et al.  Calcium response in single osteocytes to locally applied mechanical stimulus: differences in cell process and cell body. , 2009, Journal of biomechanics.

[51]  H. Rodrigues,et al.  Numerical modeling of bone tissue adaptation--a hierarchical approach for bone apparent density and trabecular structure. , 2009, Journal of Biomechanics.

[52]  Sheldon Weinbaum,et al.  Fluid and Solute Transport in Bone: Flow-Induced Mechanotransduction. , 2009, Annual review of fluid mechanics.

[53]  T. Adachi,et al.  Asymmetric intercellular communication between bone cells: propagation of the calcium signaling. , 2009, Biochemical and biophysical research communications.

[54]  J. M. García-Aznar,et al.  A bone remodelling model including the directional activity of BMUs , 2009, Biomechanics and modeling in mechanobiology.

[55]  Ralph Müller,et al.  In silico biology of bone modelling and remodelling: adaptation , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[56]  Tomonori Yamada,et al.  Computer simulation of trabecular remodeling in human proximal femur using large-scale voxel FE models: Approach to understanding Wolff's law. , 2009, Journal of biomechanics.

[57]  T. Adachi,et al.  Osteocyte calcium signaling response to bone matrix deformation. , 2009, Journal of biomechanics.

[58]  J. W. C. Dunlop,et al.  New Suggestions for the Mechanical Control of Bone Remodeling , 2009, Calcified Tissue International.

[59]  Yoshitaka Kameo,et al.  Fluid pressure response in poroelastic materials subjected to cyclic loading , 2009 .

[60]  T. Yamashiro,et al.  A Method for Observing Silver-Stained Osteocytes In Situ in 3-μm Sections Using Ultra-High Voltage Electron Microscopy Tomography , 2009, Microscopy and Microanalysis.

[61]  Yoshitaka Kameo,et al.  Estimation of bone permeability considering the morphology of lacuno-canalicular porosity. , 2010, Journal of the mechanical behavior of biomedical materials.