Fluid/solid Interactions in Cancellous Bone

Bone is a self-repairing structural material, which adapts its material properties, and shape in response to altered mechanical loading. The specific mechanism responsible for skeletal adaptation is not well understood. When cancellous bone is subjected to mechanical loading, bone marrow displacements occur within the bone matrix. This load induced bone marrow / matrix interaction in cancellous bone might play a role in skeletal adaptation. To study this bone marrow / matrix interaction, the basic parameters that characterize this phenomenon have to be well understood. Three parameters that characterize the fluid-flow properties of cancellous bone in the human calcaneus were studied. They are (1) the rheological properties of bone marrow obtained from the human calcaneus, (2) the permeability of cancellous bone harvested from different locations in the human calcaneus, and (3) the nature of pressures that occurred in the human calcaneus during physiological loading. The influence of shear rate on viscosity depended on the state of health of subjects, with some pathological marrow behaving like a non-Newtonian fluid and the normal yellow marrow as a Newtonian fluid. The average viscosity of yellow marrow in normal individuals at approximately 36°C was found to be 37.5 centipoise. Permeability in the calcaneus was dependent on the location of bone cores. In the calcaneus, the mediolateral bone cores offered the highest resistance to fluid flow. Comparing the micro-architectural measurements with permeability values revealed that permeability values were dependent on the presence of rods and plates. The calcaneus of cadaver feet displayed both positive and negative pressures during stimulated standing and toe off phase. The results from this study will help us understand the bone marrow/matrix interaction in the calcaneus during normal activities of daily living.

Year	Entry
1993	Harrigan TP, Hamilton JJ. Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications. J Biomech. February 1993;26(2):183-200.
2000	Vico L, Collet P, Guignandon A, Lafage-Proust M-H, Thomas T, Rehailia M, Alexandre C. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet. May 6, 2000;355(9215):1607-1611.
2000	Brown TD. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech. January 2000;33(1):3-14.
1998	Riggs BL, Khosla S, Melton LJ III. A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res. May 1998;13(5):763-773.
1992	Parfitt AM. Implications of architecture for the pathogenesis and prevention of vertebral fracture. Bone. 1992;13(suppl 2):S41-S47.
1997	Smalt R, Mitchell FT, Howard RL, Chambers TJ. Induction of NO and prostaglandin E₂ in osteoblasts by wall-shear stress but not mechanical strain. Am J Physiol Endocrinol Metab. October 1997;273(4):E751-E758.
2004	Mullender M, El Haj AJ, Yang Y, van Duin MA, Burger EH, Klein-Nulend J. Mechanotransduction of bone cells in vitro: mechanobiology of bone tissue. Med Biol Eng Comput. January 2004;42(1):14-21.
2002	Seeman E. Pathogenesis of bone fragility in women and men. Lancet. May 25, 2002;359(9320):1841-1850.
1990	Sharp DJ, Tanner KE, Bonfield W. Measurement of the density of trabecular bone. J Biomech. 1990;23(8):853-857.
1993	Mori S, Burr DB. Increased intracortical remodeling following fatigue damage. Bone. March–April 1993;14(2):103-109.
2000	Knothe Tate M, Knothe U. An ex vivo model to study transport processes and fluid flow in loaded bone. J Biomech. February 2000;33(2):247-254.
2000	Sabry FF, Ebraheim NA, Mehalik JN, Rezcallah AT. Internal architecture of the calcaneus: implications for calcaneus fractures. Foot Ankle Int. 2000;21(2):114-118.
1988	Montgomery RJ, Sutker BD, Bronk JT, Smith SR, Kelly PJ. Interstitial fluid flow in cortical bone. Microvasc Res. May 1988;35(3):295-307.
1999	Cowin SC. Bone poroelasticity. J Biomech. March 1999;32(3):217-238.
1990	Eriksen EF, Hodgson SF, Eastell R, Cedel SL, O'Fallon WM, Riggs BL. Cancellous bone remodeling in type I (postmenopausal) osteoporosis: quantitative assessment of rates of formation, resorption, and bone loss at tissue and cellular levels. J Bone Miner Res. April 1990;5(4):311-319.
1996	Biewener AA, Fazzalari NL, Konieczynski DD, Baudinette RV. Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone. July 1996;19(1):1-8.
1991	Turner CH. Homeostatic control of bone structure: an application of feedback theory. Bone. 1991;12(3):203-217.
2000	Martin RB. Toward a unifying theory of bone remodeling. Bone. January 2000;26(1):1-6.
1977	Piekarski K, Munro M. Transport mechanism operating between blood supply and osteocytes in long bones. Nature. September 1, 1977;270(5623):80-82.
1997	Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Prog Biomed. 1997;1(1):15-23.
2001	Rubin C, Xu G, Judex S. The anabolic activity of bone tissue, suppressed by disuse, is normalized by brief exposure to extremely low‐magnitude mechanical stimuli. FASEB J. October 2001;15(12):2225-2229.
2002	Qin Y-X, Lin W, Rubin C. The pathway of bone fluid flow as defined by in vivo intramedullary pressure and streaming potential measurements. Ann Biomed Eng. May 2002;30(5):693-702.
2001	Rubin C, Turner AS, Bain S, Mallinckrodt C, McLeod K. Low mechanical signals strengthen long bones. Nature. August 9, 2001;412(6847):603-604.
2000	Giddings VL, Beaupré GS, Whalen RT, Carter DR. Calcaneal loading during walking and running. Med Sci Sports Exer. March 2000;32(3):627-634.
1994	Müller R, Hildebrand T, Rüegsegger P. Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. Phys Med Biol. January 1994;39(1):145-164.
1993	Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone. 1993;14(4):595-608.
1998	Turner CH, Pavalko FM. Mechanotransduction and functional response of the skeleton to physical stress: the mechanisms and mechanics of bone adaptation. J Orthop Sci. November 1998;3(6):346-355.
2000	Gefen A, Megido-Ravid M, Itzchak Y, Arcan M. Biomechanical analysis of the three-dimensional foot structure during gait: a basic tool for clinical applications. J Biomech Eng. December 2000;122(6):630-639.
2001	Gefen A, Megido-Ravid M, Itzchak Y. In vivo biomechanical behavior of the human heel pad during the stance phase of gait. J Biomech. 2001;34(12):1661-1665.
1991	Dillaman RM, Roer RD, Gay DM. Fluid movement in bone: theoretical and empirical. J Biomech. 1991;24(suppl 1):163-177.
1962	Bassett CAL, Becker RO. Generation of electric potentials by bone in response to mechanical stress. Science. September 28, 1962;137(3535):1063.
2001	van Rietbergen B, Huiskes R. Elastic constants of cancellous bone. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:15-1–15-24.
1983	Bryant JD. The effect of impact on the marrow pressure of long bones in vitro. J Biomech. 1983;16(8):659-665.
1984	Feldkamp LA, Davis LC, Kress JW. Practical cone-beam algorithm. J Opt Soc Am. 1984;A1(6):612-619.
2002	Parfitt AM. Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone. January 2002;30(1):5-7.
1996	Oxlund H, Mosekilde L, Ørtoft G. Reduced concentration of collagen reducible cross links in human trabecular bone with respect to age and osteoporosis. Bone. November 1996;19(5):479-484.
1995	Klein-Nulend J, van der Plas A, Semeins CM, Ajubi NE, Frangos JA, Nijweide PJ, Burger EH. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. March 1995;9(5):441-445.
1994	Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. March 1994;27(3):339-360.
1993	Odgaard A, Gundersen HJG. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone. March–April 1993;14(2):173-182.
1995	Pitsillides AA, Rawlinson SCF, Suswillo RFL, Bourrin S, Zaman G, Lanyon LE. Mechanical strain‐induced NO production by bone cells: a possible role in adaptive bone (re)modeling? FASEB J. December 1995;9(15):1614-1622.
2001	Jee WSS. Integrated bone tissue physiology: anatomy and physiology. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:1-1–1-68.
2003	Heaney RP. Is the paradigm shifting? Bone. October 2003;33(4):457-465.
1998	Majumdar S, Kothari M, Augat P, Newitt DC, Link TM, Lin JC, Lang T, Lu Y, Genant HK. High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone. May 1998;22(5):445-454.
2001	Arramon YP, Nauman EA. The intrinsic permeability of cancellous bone. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:25-1–25-17.
1999	Burger EH, Klein-Nulend J. Mechanotransduction in bone: role of the lacunocanalicular network. FASEB J. May 1999;12(9001):S101-S112.
2003	Qin Y-X, Kaplan T, Saldanha A, Rubin C. Fluid pressure gradients, arising from oscillations in intramedullary pressure, is correlated with the formation of bone and inhibition of intracortical porosity. J Biomech. October 2003;36(10):1427-1437.
2002	Burr DB. The contribution of the organic matrix to bone's material properties. Bone. July 2002;31(1):8-11.
2000	Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. April 2000;21(2):115-137.
1997	Mullender MG, Huiskes R. Osteocytes and bone lining cells: which are the best candidates for mechano-sensors in cancellous bone? Bone. June 1997;20(6):527-532.

Year

Entry

1993

Harrigan TP, Hamilton JJ. Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications. J Biomech. February 1993;26(2):183-200.

2000

Vico L, Collet P, Guignandon A, Lafage-Proust M-H, Thomas T, Rehailia M, Alexandre C. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet. May 6, 2000;355(9215):1607-1611.

2000

Brown TD. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech. January 2000;33(1):3-14.

1998

Riggs BL, Khosla S, Melton LJ III. A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res. May 1998;13(5):763-773.

1992

Parfitt AM. Implications of architecture for the pathogenesis and prevention of vertebral fracture. Bone. 1992;13(suppl 2):S41-S47.