Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications

wbldb

Harrigan, Timothy P.¹; Hamilton, James J.¹

Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications

J Biomech. February 1993;26(2):183-200

©1993 Pergamon Press Ltd

Affiliations

¹Department of Orthopedic Surgery, University of Missouri at Kansas City Medical School, 2301 Holmes St, Kansas City, MO 64108, U.S.A.
Abstract

A model is developed in which osteoblasts can sense the strains applied to a small region of bone through electrical coupling between adjacent cells. The stress-generated potentials within bone are assumed to occur through streaming potentials, and the coupled network of osteocytes is assumed to act in a manner similar to the classical cable model for nerve cells. In a one-dimensional model, the linear poroelastic equations for motion of the fluid are solved analytically for sinusoidally varying imposed strains, and the streaming potentials are predicted from the fluid flow. The changes in the osteocyte and osteoblast transmembrane potential are given by an analytical solution to the governing equations, and the dependence of the transmembrane potential changes (TPC) on position, loading rate, manner of loading (compression versus bending), and on the degree of cellular coupling is discussed. The model correctly predicts the rate dependence of remodelling established by other investigators. The influence of the electrical parameters within the model indicate that further study of the cellular coupling in bone can yield important new information on bone remodelling.
Links

DOI: 10.1016/0021-9290(93)90048-J

PubMed: 8429060

WoS: A1993KJ75500009
History

Revised: 1992-06-11

Cited Works (14)

Year	Entry
1987	Frank EH, Grodzinsky AJ. Cartilage electromechanics, I: electrokinetic transduction and the effects of electrolyte pH and ionic strength. J Biomech. 1987;20(6):615-627.
1987	Cowin SC. Bone remodeling of diaphyseal surfaces by torsional loads: theoretical predictions. J Biomech. 1987;20(11-12):1111-1120.
1990	Beaupré GS, Orr TE, Carter DR. An approach for time‐dependent bone modeling and remodeling: theoretical development. J Orthop Res. September 1990;8(5):651-661.
1987	Salzstein RA, Pollack SR. Electromechanical potentials in cortical bone, II: experimental analysis. J Biomech. 1987;20(3):271-280.
1979	Starkebaum W, Pollack SR, Korostoff E. Midroelectrode studies of stress-generated potentials in four-point bending of bone. J Mater Res. September 1979;13(5):729-751.
1987	Salzstein RA, Pollack SR, Mak AFT, Petrov N. Electromechanical potentials in cortical bone, I: a continuum approach. J Biomech. 1987;20(3):261-270.
1987	Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala B, Slooff TJ. Adaptive bone-remodeling theory applied to prosthetic-design analysis. J Biomech. 1987;20(11-12):1135-1150.
1990	Beaupré GS, Orr TE, Carter DR. An approach for time‐dependent bone modeling and remodeling—application: a preliminary remodeling simulation. J Orthop Res. September 1990;8(5):662-670.
1987	Frank EH, Grodzinsky AJ. Cartilage electromechanics, II: a continuum model of cartilage electrokinetics and correlation with experiments. J Biomech. 1987;20(6):629-639.
1989	Carter DR, Orr TE, Fyhrie DP. Relationships between loading history and femoral cancellous bone architecture. J Biomech. 1989;22(3):231-244.
1984	Cowin SC. Mechanical modeling of the stress adaptation process in bone. Calcif Tiss Int. March 1984;36(suppl 1):S98-S103.
1987	Rubin CT, Lanyon LE. Osteoregulatory nature of mechanical stimuli: function as a determinant for adaptive remodeling in bone. J Orthop Res. 1987;5(2):300-310.
1984	Johnson MW. Behavior of fluid in stressed bone and cellular stimulation. Calcif Tiss Int. March 1984;36(suppl 1):S72-S76.
1987	Carter DR, Fyhrie DP, Whalen RT. Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy. J Biomech. 1987;20(8):785-794.

Cited By (23)

Year	Entry
1997	Zhang D, Cowin SC, Weinbaum S. Electrical signal transmission and gap junction regulation in a bone cell network: a cable model for an osteon. Ann Biomed Eng. March 1997;25(2):357-374.
2009	Fritton SP, Weinbaum S. Fluid and solute transport in bone: flow-induced mechanotransduction. Annu Rev Fluid Mech. 2009;41:347-374.
1995	Turner CH, Forwood MR. What role does the osteocyte network play in bone adaptation? Bone. March 1995;16(3):283-285.
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.
2000	Martin RB. Toward a unifying theory of bone remodeling. Bone. January 2000;26(1):1-6.
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.
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.
1995	Cowin SC, Weinbaum S, Zeng Y. A case for bone canaliculi as the anatomical site of strain generated potentials. J Biomech. November 1995;28(11):1281-1297.
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.
1995	Luo G, Cowin SC, Sadegh AM, Arramon YP. Implementation of strain rate as a bone remodeling stimulus. J Biomech Eng. August 1995;117(3):329-338.
1995	Mullender MG, Huiskes R. Proposal for the regulatory mechanism of Wolff's law. J Orthop Res. July 1995;13(4):503-512.
2004	Samuel SP. Fluid/solid Interactions in Cancellous Bone [PhD thesis]. Cleveland State University; August 2004.
1994	Luo G. A Computational Study of the Long Term Stability of Total Hip Implants [PhD thesis]. New York, NY: The City University of New York; 1994.
1997	Zhang D. Electromechanical Mechanisms of Bone Remodeling [PhD thesis]. New York, NY: The City University of New York; 1997.
2002	You L. A New View of Mechanotransduction in Bone Cells [PhD thesis]. New York, NY: The City University of New York; 2002.
2004	Mi LY. Analysis of Avian Bone Response to Mechanical Loading Using a Computational Connected Network [PhD thesis]. New York, NY: The City College of New York; 2004.
2004	Thi MM. Cellular Communication and Mechanotransduction in Response to Fluid Shear Stress [PhD thesis]. New York, NY: The City University of New York; 2004.
2002	Hudson JA. The Ontogeny of Transverse Femoral Geometry and Bone Modeling in the Ward Skeletal Population [PhD thesis]. Kent State University; August 2002.
2006	Hannay G. Mechanical and Electrical Environments to Stimulate Bone Cell Development [PhD thesis]. Queensland University of Technology; August 2006.
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.
2000	Borodkin JL. The Influence of Interface Micromechanics on the Biological Fixation of Porous-Coated Implants [PhD thesis]. University of Michigan; 2000.
1996	Beck BR. The Relationship of Streaming Potential Magnitude to Strain and Periosteal Modeling [PhD thesis]. Eugene, OR: University of Oregon; December 1996.