A fatigue microcrack alters fluid velocities in a computational model of interstitial fluid flow in cortical bone.

Targeted remodeling is activated by fatigue microcracks and plays an important role in maintaining bone integrity. It is widely believed that fluid flow-induced shear stress plays a major role in modulating the mechanotransduction process. Therefore, it is likely that fluid flow-induced shear stress plays a major role in the initiation of the repair of fatigue damage. Since no in vivo measurements of fluid flow within bone exist, computational and mathematical models must be employed to investigate the fluid flow field and the shear stress occurring within cortical bone. We developed a computational fluid dynamic model of cortical bone to examine the effect of a fatigue microcrack on the fluid flow field. Our results indicate that there are alterations in the fluid flow field as far as 150 microm away from the crack, and that at distances farther than this, the fluid flow field is similar to the fluid flow field of intact bone. Through the crack and immediately above and below it, the fluid velocity is higher, while at the lateral edges it is lower than that calculated for the intact model, with a maximum change of 29%. Our results suggest that the presence of a fatigue microcrack can alter the shear stress in regions near the crack. These alterations in shear stress have the potential to significantly alter mechanotransduction and may play a role in the initiation of the repair of fatigue microcracks.

[1]  R. Martin,et al.  Studies of skeletal remodeling in aging men. , 1980, Clinical orthopaedics and related research.

[2]  D. Zaffe,et al.  Quantitative investigation on osteocyte canaliculi in human compact and spongy bone. , 1985, Bone.

[3]  C Milgrom,et al.  Aging and matrix microdamage accumulation in human compact bone. , 1995, Bone.

[4]  T. Gross,et al.  Canalicular fluid flow induced by bending of a long bone. , 2000, Medical engineering & physics.

[5]  B. Martin,et al.  A theory of fatigue damage accumulation and repair in cortical bone , 1992, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

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

[7]  D. Burr,et al.  Bone Microdamage and Skeletal Fragility in Osteoporotic and Stress Fractures , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[8]  D B Burr,et al.  Increased intracortical remodeling following fatigue damage. , 1993, Bone.

[9]  P. Niederer,et al.  A finite element analysis for the prediction of load-induced fluid flow and mechanochemical transduction in bone. , 2003, Journal of theoretical biology.

[10]  D. Taylor.,et al.  Visualisation of three‐dimensional microcracks in compact bone , 2000, Journal of anatomy.

[11]  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.

[12]  M. Ferretti,et al.  Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. , 1998, Italian journal of anatomy and embryology = Archivio italiano di anatomia ed embriologia.

[13]  Subrata Saha,et al.  A theoretical model for stress-generated fluid flow in the canaliculi-lacunae network in bone tissue. , 1990, Journal of biomechanics.

[14]  S. Cowin,et al.  Estimates of the peak pressures in bone pore water. , 1998, Journal of biomechanical engineering.

[15]  Eric A Nauman,et al.  Permeability of musculoskeletal tissues and scaffolding materials: experimental results and theoretical predictions. , 2003, Critical reviews in biomedical engineering.

[16]  M. Biot General Theory of Three‐Dimensional Consolidation , 1941 .

[17]  Marvin W. Johnson Behavior of fluid in stressed bone and cellular stimulation , 2006, Calcified Tissue International.

[18]  R. Dillaman,et al.  Fluid movement in bone: theoretical and empirical. , 1991, Journal of biomechanics.

[19]  R. Keanini,et al.  A theoretical model of circulatory interstitial fluid flow and species transport within porous cortical bone. , 1995, Journal of biomechanics.

[20]  P J Kelly,et al.  Permeability of cortical bone of canine tibiae. , 1987, Microvascular research.

[21]  Theo H Smit,et al.  Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon--a proposal. , 2003, Journal of biomechanics.

[22]  P. Muir,et al.  Microcrack density and length in the proximal and distal metaphyses of the humerus and radius in dogs. , 2000, American journal of veterinary research.

[23]  David B. Burr,et al.  Remodeling and the repair of fatigue damage , 2005, Calcified Tissue International.

[24]  S. Hughes,et al.  Fluid space in bone. , 1978, Clinical orthopaedics and related research.

[25]  M. K. Knothe Tate,et al.  An ex vivo model to study transport processes and fluid flow in loaded bone. , 2000, Journal of biomechanics.

[26]  S. Cowin,et al.  Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. , 1999, Journal of biomechanics.

[27]  Stephen C. Cowin,et al.  Modeling Tracer Transport in an Osteon under Cyclic Loading , 2004, Annals of Biomedical Engineering.

[28]  L. Lanyon,et al.  Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. , 2003, American journal of physiology. Cell physiology.

[29]  M W Otter,et al.  Mechanotransduction in bone: do bone cells act as sensors of fluid flow? , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[30]  N. Sharkey,et al.  Bone strain and microcracks at stress fracture sites in human metatarsals. , 2000, Bone.

[31]  D. Burr,et al.  Suppressed Bone Turnover by Bisphosphonates Increases Microdamage Accumulation and Reduces Some Biomechanical Properties in Dog Rib , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[32]  H J Donahue,et al.  Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. , 2001, American journal of physiology. Cell physiology.

[33]  Marvin W. Johnson,et al.  Fluid flow in bone in vitro. , 1982, Journal of biomechanics.

[34]  K. Piekarski,et al.  Transport mechanism operating between blood supply and osteocytes in long bones , 1977, Nature.

[35]  R. Martin,et al.  Is all cortical bone remodeling initiated by microdamage? , 2002, Bone.

[36]  S. Cowin,et al.  A case for bone canaliculi as the anatomical site of strain generated potentials. , 1995, Journal of biomechanics.

[37]  E. Radin,et al.  Bone remodeling in response to in vivo fatigue microdamage. , 1985, Journal of biomechanics.

[38]  E H Burger,et al.  The production of nitric oxide and prostaglandin E(2) by primary bone cells is shear stress dependent. , 2001, Journal of biomechanics.

[39]  A. Mak,et al.  Deformation-induced hierarchical flows and drag forces in bone canaliculi and matrix microporosity. , 1997, Journal of biomechanics.

[40]  D P Fyhrie,et al.  Intracortical remodeling in adult rat long bones after fatigue loading. , 1998, Bone.

[41]  L. Raisz Physiology and pathophysiology of bone remodeling. , 1999, Clinical chemistry.

[42]  P. Nasser,et al.  The Role of Interstitial Fluid Flow in the Remodeling Response to Fatigue Loading , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[43]  D. Davy,et al.  Machine vision photogrammetry: a technique for measurement of microstructural strain in cortical bone. , 2001, Journal of biomechanics.

[44]  P. Niederer,et al.  A finite difference model of load-induced fluid displacements within bone under mechanical loading. , 2000, Medical engineering & physics.

[45]  D B Burr,et al.  Targeted and nontargeted remodeling. , 2002, Bone.

[46]  Olivier Verborgt,et al.  Spatial Distribution of Bax and Bcl‐2 in Osteocytes After Bone Fatigue: Complementary Roles in Bone Remodeling Regulation? , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.