Fluid movement in bone: theoretical and empirical

wbldb

Dillaman, Richard M.¹; Roer, Robert D.¹; Gay, Daniel M.¹

Fluid movement in bone: theoretical and empirical

J Biomech. 1991;24(suppl 1):163-177

Affiliations

¹Center for Marine Science Research, University of North Carolina at Wilmington, 7205 Wrightsvilk Ave., Wilmington, North Carolina 28403, U.S.A.
Abstract

Evidence from the literature and from our laboratory demonstrates a pronounced and rapid flow of fluids and associated solutes through the extravascular spaces in bone. Minutes after injection, large molecules such as ferritin and horseradish peroxidase (HRP) have been localized throughout the osteocytic lacunae and canaliculi of cortical bone in the chick, rat and dog. Patterns of marker movement preclude diffusion as the mechanism for solute movement and suggest a centrifugal bulk flow of fluids. We have developed a computer model of bone fluid flow that has led to the conclusion that the pattern and rate of fluid movement is governed by the pressure differential across the bone, the vascular architecture, and the porosity of the mineralized matrix. The validity of simulations in which a substance is injected and monitored over time has been tested by comparisons with actual injections of markers in the rat. Evidence is presented for a relationship between blood flow and bone dynamics in growth, repair and pathology of bone. We employed the tail suspension model of weightlessness in the rat to test the effect of posture on the perfusion of cortical bone using injections of HRP. Data indicated that perfusion of the femur was reduced by this treatment. We propose a “rheostat” mechanism, which suggests that bone perfusion may set limits for bone growth and remodeling. Therefore, bone mass reflects the ability of the vasculature to supply oxygen and nutrients to the cells on and within the mineralized matrix.
Links

DOI: 10.1016/0021-9290(91)90386-2

PubMed: 1791176

WoS: A1991HB54500015
History

Revised: 1991-01-1

Online: 2004-04-2

Cited Works (10)

Year	Entry
1990	Reich KM, Gay CV, Frangos JA. Fluid shear stress as a mediator of osteoblast cyclic adenosine monophosphate production. J Cell Physiol. April 1990;143(1):100-103.
1978	Morey ER, Baylink DJ. Inhibition of bone formation during space flight. Science. September 22, 1978;201(4361):1138-1141.
1982	Johnson MW, Chakkalakal DA, Harper RA, Katz JL, Rouhana SW. Fluid flow in bone in vitro. J Biomech. 1982;15(11):881-885.
1970	Donaldson CL, Hulley SB, Vogel JM, Hattner RS, Bayers JH, McMillan DE. Effect of prolonged bed rest on bone mineral. Metabolism. December 1970;19(12):1071-1084.
1990	Leblanc AD, Schneider VS, Evans HJ, Engelbretson DA, Krebs JM. Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res. August 1990;5(8):843-850.
1989	Petrov N, Pollack S, Blagoeva R. A discrete model for streaming potentials in a single osteon. J Biomech. 1989;22(6-7):517-521.
1982	Morris MA, Lopez-Curto JA, Hughes SP, An K-N, Bassingthwaighte JB, Kelly PJ. Fluid spaces in canine bone and marrow. Microvasc Res. May 1982;23(2):188-200.
1986	Globus RK, Bikle DD, Morey-Holton E. The temporal response of bone to unloading. Endocrinology. February 1986;118(2):733-742.
1987	Li G, Bronk JT, An K-N, Kelly PJ. Permeability of cortical bone of canine tibiae. Microvasc Res. November 1987;34(3):302-310.
1984	Pollack SR, Petrov N, Salzstein R, Brankov G, Blagoeva R. An anatomical model for streaming potentials in osteons. J Biomech. 1984;17(8):627-636.

Cited By (38)

Year	Entry
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.
2010	Jacobs CR, Temiyasathit S, Castillo AB. Osteocyte mechanobiology and pericellular mechanics. Annu Rev Biomed Eng. 2010;12:369-400.
1994	Hillsley MV, Frangos JA. Review: bone tissue engineering: the role of interstitial fluid flow. Biotechnol Bioeng. March 25, 1994;43(7):573-581.
1995	Turner CH, Forwood MR. What role does the osteocyte network play in bone adaptation? Bone. March 1995;16(3):283-285.
1998	Knothe Tate ML, Niederer P, Knothe U. In vivo tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone. February 1998;22(2):107-117.
2004	Wang L, Ciani C, Doty SB, Fritton SP. Delineating bone's interstitial fluid pathway in vivo. Bone. March 2004;34(3):499-509.
2010	Gardinier JD, Townend CW, Jen K-P, Wu Q, Duncan RL, Wang L. In situ permeability measurement of the mammalian lacunar–canalicular system. Bone. April 2010;46(4):1075-1081.
1995	Duncan RL, Turner CH. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tiss Int. December 1995;57(5):344-358.
1994	Turner CH, Forwood MR, Otter MW. Mechanotransduction in bone: do bone cells act as sensors of fluid flow? FASEB J. August 1994;8(11):875-878.
2006	Rubin J, Rubin C, Jacobs CR. Molecular pathways mediating mechanical signaling in bone. Gene. February 15, 2006;367:1-16.
2012	Thompson WR, Rubin CT, Rubin J. Mechanical regulation of signaling pathways in bone. Gene. July 25, 2012;503(2):179-193.
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.
1997	Mak AFT, Huang DT, Zhang JD, Tong P. Deformation-induced hierarchical flows and drag forces in bone canaliculi and matrix microporosity. J Biomech. January 1997;30(1):11-18.
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.
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.
2004	Ferguson SJ, Ito K, Nolte L-P. Fluid flow and convective transport of solutes within the intervertebral disc. J Biomech. February 2004;37(2):213-221.
2006	Beno T, Yoon Y-J, Cowin SC, Fritton SP. Estimation of bone permeability using accurate microstructural measurements. J Biomech. 2006;39(13):2378-2387.
2011	Brynk T, Hellmich C, Fritsch A, Zysset P, Eberhardsteiner J. Experimental poromechanics of trabecular bone strength: role of Terzaghi's effective stress and of tissue level stress fluctuations. J Biomech. 2011;44(3):501-508.
1999	McAllister TN, Frangos JA. Steady and transient fluid shear stress stimulate NO release in osteoblasts through distinct biochemical pathways. J Bone Miner Res. June 1999;14(6):930-936.
1994	Aarden EM, Burger EH, Nijweide PJ. Function of osteocytes in bone. J Cell Biochem. July 1994;55(3):287-299.
2003	Steck R, Niederer P, Knothe Tate ML. A finite element analysis for the prediction of load-induced fluid flow and mechanochemical transduction in bone. J Theo Biol. January 21, 2003;220(2):249-259.
1996	Hillam RA. Response of Bone to Mechanical Load and Alterations in Circulating Hormones [PhD thesis]. Bristol, UK: University of Bristol; October 1996.
2011	Miller RM. Mechanobiological Investigation of Periosteum Through Finite Element Modeling and Histology [Master's thesis]. Cleveland, OH: Case Western Reserve University; August 2011.
2004	Samuel SP. Fluid/solid Interactions in Cancellous Bone [PhD thesis]. Cleveland State University; August 2004.
2002	Wang L. Investigating the Role of Interstitial Fluid Flow in Bone Adaptation and Metabolism [PhD thesis]. New York, NY: The City University of New York; 2002.
2005	Beno T. Investigating the Role of Microstructure in Bone Permeability [PhD thesis]. New York, NY: The City University of New York; 2005.
2008	Ciani C. Characterization of Microporosities and Load-Induced Interstitial Fluid Movement in Normal and Osteopenic Bone [PhD thesis]. New York, NY: The City University of New York; 2008.
2009	Gailani G. Russian Doll Poroelasticity [PhD thesis]. New York, NY: The City University of New York; 2009.
2012	Benalla M. Experimental Detrmination of the Lacunar-Canalicular Permeability Using Cyclic Loading [PhD thesis]. New York, NY: The City University of New York; 2012.
2009	Massey CJ. Finite Element Analysis and Materials Characterization of Changes Due to Aging and Degeneration of the Human Intervertebral Disc [PhD thesis]. Drexel University; September 2009.
2014	Ferro Pereira A. Cortical Bone Adaptation: A Finite-Element Study of the Mouse Tibia [PhD thesis]. Imperial College London; January 2014.
1998	Giddings VL. Computer Simulations of Calcaneal Loading and Bone Adaptation [PhD thesis]. Stanford University; June 1998.
1997	Qin Y-X. Fluid Flow, Matrix Strain and Loading Frequency as Interdependent Control Parameters in Skeletal Adaptation [PhD thesis]. Stony Brook, NY: State University of New York at Stony Brook; May 1997.
2006	Xie L. Low Level Mechanical Vibrations Enhance Musculoskeletal Accretion in Growing Mice [PhD thesis]. Stony Brook, NY: Stony Brook University; December 2006.
2000	Shymkiw RC-C. Measurement of Blood Flow in Bone by Laser Doppler Imaging [Master's thesis]. Calgary, AB: University of Calgary; May 2000.
1996	Adams DJ. Mechanical Factors Initiating Appositional Bone Formation [PhD thesis]. University of Iowa; May 1996.
1996	Beck BR. The Relationship of Streaming Potential Magnitude to Strain and Periosteal Modeling [PhD thesis]. Eugene, OR: University of Oregon; December 1996.
1995	Grimm MJ. Ultrasound Propagation Through the Calcaneus: Dependence on "Bone Quality" and Prediction by Biot's Theory [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 1995.