On the Electric Potentials Inside a Charged Soft Hydrated Biological Tissue: Streaming Potential Versus Diffusion Potential

2000 ◽  
Vol 122 (4) ◽  
pp. 336-346 ◽  
Author(s):  
W. Michael Lai ◽  
Van C. Mow ◽  
Daniel D. Sun ◽  
Gerard A. Ateshian

The main objective of this study is to determine the nature of electric fields inside articular cartilage while accounting for the effects of both streaming potential and diffusion potential. Specifically, we solve two tissue mechano-electrochemical problems using the triphasic theories developed by Lai et al. (1991, ASME J. Biomech Eng., 113, pp. 245–258) and Gu et al. (1998, ASME J. Biomech. Eng., 120, pp. 169–180) (1) the steady one-dimensional permeation problem; and (2) the transient one-dimensional ramped-displacement, confined-compression, stress-relaxation problem (both in an open circuit condition) so as to be able to calculate the compressive strain, the electric potential, and the fixed charged density (FCD) inside cartilage. Our calculations show that in these two technically important problems, the diffusion potential effects compete against the flow-induced kinetic effects (streaming potential) for dominance of the electric potential inside the tissue. For softer tissues of similar FCD (i.e., lower aggregate modulus), the diffusion potential effects are enhanced when the tissue is being compressed (i.e., increasing its FCD in a nonuniform manner) either by direct compression or by drag-induced compaction; indeed, the diffusion potential effect may dominate over the streaming potential effect. The polarity of the electric potential field is in the same direction of interstitial fluid flow when streaming potential dominates, and in the opposite direction of fluid flow when diffusion potential dominates. For physiologically realistic articular cartilage material parameters, the polarity of electric potential across the tissue on the outside (surface to surface) may be opposite to the polarity across the tissue on the inside (surface to surface). Since the electromechanical signals that chodrocytes perceive in situ are the stresses, strains, pressures and the electric field generated inside the extracellular matrix when the tissue is deformed, the results from this study offer new challenges for the understanding of possible mechanisms that control chondrocyte biosyntheses. [S0148-0731(00)00604-X]

1981 ◽  
Vol 103 (4) ◽  
pp. 280-292 ◽  
Author(s):  
R. C. Lee ◽  
E. H. Frank ◽  
A. J. Grodzinsky ◽  
D. K. Roylance

The compressive stiffness of articular cartilage was examined in oscillatory confined compression over a wide frequency range including high frequencies relevant to impact loading. Nonlinear behavior was found when the imposed sinusoidal compression amplitude exceeded a threshold value that depended on frequency. Linear behavior was attained only by suitable control of the compression amplitude. This was enabled by real time Fourier analysis of data which provided an accurate assessment of the extent of nonlinearity. For linear viscoelastic behavior, a stiffness could be defined in the usual sense. The dependence of the stiffness on ionic strength and proteoglycan content showed that electrostatic forces between matrix charge groups contribute significantly to cartilage’s compressive stiffness over the 0.001 to 20 Hz frequency range. Sinusoidal streaming potentials were also generated by oscillatory compression. A theory relating the streaming potential field to the fluid velocity field is derived and used to interpret the data. The observed magnitude of the streaming potential suggests that interstitial fluid flow is significant to cartilage behavior over the entire frequency range. The use of simultaneous streaming potential and stiffness data with an appropriate theory appears to be an important tool for assessing the relative contribution of fluid flow, intrinsic matrix viscoelasticity, or other molecular mechanisms to energy dissipation in cartilage. This method is applicable in general to hydrated, charged polymers.


Author(s):  
Heath B. Henninger ◽  
Clayton J. Underwood ◽  
Gerard A. Ateshian ◽  
Jeffrey A. Weiss

Permeability is defined as the ability of a fluid to pass through a porous medium. The ease of water movement is a determinant of the interstitial fluid flow-dependent viscoelastic properties of hydrated soft tissues and also modulates transport of solutes. For articular cartilage, permeability has been quantified directly via permeation experiments and indirectly by analyzing the data from stress relaxation testing under confined compression. It is unclear whether these different methods result in consistent measurements. This further complicates quantification of the effect of an experimental treatment on permeability such as the removal of sulfated glycosaminoglycans (GAGs) [1, 2]. The objective of this study was to elucidate the impact of sulfated GAGs on the permeability of articular cartilage using direct permeation versus stress relaxation testing, and to assess any differences in permeability calculated from the two test methods.


Author(s):  
W. Scott Van Dyke ◽  
Eric Nauman ◽  
Ozan Akkus

The causes, mechanisms, and biology of bone adaptation have been under intense investigation ever since Julius Wolff proposed that bone architecture is determined by mathematical laws as a result of mechanical loading. How bone responds to mechanical loads by converting the mechanical signals into chemical signals is known as mechanotransduction. The in vivo environment of bone is complex, and most studies of cell-level phenomena have relied on the use of in vitro experiments using mechanical bioreactors. The main types of bioreactors are fluid flow shear stress, tensile and/or compressive strain, and hydrostatic pressure [1–2]. Of these bioreactors, the most intuitive mechanical stimulus for bone would be the tensile and compressive strain bioreactors. However, many researchers now claim that shear stress via interstitial fluid flow in the lacunar-canalicular porosity is the primary mechanosensory stimulus [3]. A handful of studies have attempted to compare the effects of both of these mechanical stimuli on osteoblasts, but these studies are lacking in two respects [4–6]. First, if both fluid flow and strain are performed in the same bioreactor, the magnitude of one loading mode is explicitly determined through constitutive equations, while the other is only estimated. Second, if the magnitudes of the loading modes are able to be explicitly determined they are performed in different bioreactors, providing the cells different extracellular environments. Therefore, a highly controllable dual-loading mode mechanical bioreactor, as described and characterized in this study, is a necessary tool to further understand the mechanotransduction of bone.


1999 ◽  
Author(s):  
Michael A. Soltz ◽  
Anna Stankiewicz ◽  
Gerard Ateshian ◽  
Robert L. Mauck ◽  
Clark T. Hung

Abstract The objective of this study was to determine the intrinsic hydraulic permeability of 2% agarose hydrogels. Two-percent agarose was chosen because it is a concentration typically used for encapsulation of chondrocytes in suspension cultures [3–5], Hydraulic permeability is a measure of the relative ease by which fluid can pass through a material. Importantly, it governs the level of interstitial fluid flow as well as the interstitial fluid pressurization that is generated in a material during loading. Fluid pressurization is the source of the unique load-bearing and lubrication properties of articular cartilage [1,17] and represents a major component of the in vivo chondrocyte environment. We have previously reported that 2% agarose hydrogels can support fluid pressurization, albeit to a significantly lesser degree than articular cartilage [18]. Interstitial fluid flow gives rise to convective transport of nutrients and ions [6,7] and matrix compaction [9] which may serve as important stimuli to chondrocytes. We report for the first time the strain-dependent hydraulic permeability of 2% agarose hydrogels.


Author(s):  
G A Ateshian ◽  
H Wang

A mechanism which may contribute to the frictional coefficient of diarthrodial joints is the rolling resistance due to hysteretic energy loss of viscoelastic cartilage resulting from interstitial fluid flow. The hypothesis of this study is that rolling resistance contributes significantly to the measured friction coefficient of articular cartilage. Due to the difficulty of testing this hypothesis experimentally, theoretical predictions of the rolling resistance are obtained using the solution for rolling contact of biphasic cylindrical cartilage layers [Ateshian and Wang (1)]. Over a range of rolling velocities, tissue properties and dimensions, it is found that the coefficient of rolling resistance μR varies in magnitude from 10−6 to 10−2; thus, it is generally negligible in comparison with experimental measurements of the cartilage friction coefficient (10−3-10−1) except, possibly, when the tissue is arthritic. Hence, the hypothesis of this study is rejected on the basis of these results.


2001 ◽  
Author(s):  
Yixian Qin ◽  
Anita Saldanha ◽  
Tamara Kaplan

Abstract Load-generated intracortical fluid flow is proposed to be an important mediator for regulating bone mass and morphology [1]. Although the mechanism of cellular response to induced flow parameters, i.e., fluid pressure, pressure gradient, velocity, and fluid shear stress, are not yet clear, interstitial fluid flow driven by loading may be necessary to explain the adaptive response of bone, which is either coupled with load-induced strain magnitude or independent with matrix strain per se [2]. It has been demonstrated that load-induced intracortical fluid flow is contributed by both bone matrix deformation and induced intramedullary (IM) pressure [3]. To examine the hypothesis of fluid flow generated adaptation, it is necessary to test the mechanism under the circumstances of solely fluid induced bone adaptation in the absence of matrix deformation. While our previous data has demonstrated that bone fluid flow and its associated streaming potential product can be influenced by the dynamic IM pressure quantitatively [4], the objective of this study was to evaluate fluid induced bone adaptation in an avian ulna model using oscillatory IM fluid pressure loading in the absence of bone matrix strain. The potential fluid pathway was measured in the model.


2000 ◽  
Vol 123 (2) ◽  
pp. 191-197 ◽  
Author(s):  
Mark R. DiSilvestro ◽  
Qiliang Zhu ◽  
Marcy Wong ◽  
Jukka S. Jurvelin ◽  
Jun-Kyo Francis Suh

This study investigated the ability of the linear biphasic poroelastic (BPE) model and the linear biphasic poroviscoelastic (BPVE) model to simultaneously predict the reaction force and lateral displacement exhibited by articular cartilage during stress relaxation in unconfined compression. Both models consider articular cartilage as a binary mixture of a porous incompressible solid phase and an incompressible inviscid fluid phase. The BPE model assumes the solid phase is elastic, while the BPVE model assumes the solid phase is viscoelastic. In addition, the efficacy of two additional models was also examined, i.e., the transversely isotropic BPE (TIBPE) model, which considers transverse isotropy of the solid matrix within the framework of the linear BPE model assumptions, and a linear viscoelastic solid (LVE) model, which assumes that the viscoelastic behavior of articular cartilage is solely governed by the intrinsic viscoelastic nature of the solid matrix, independent of the interstitial fluid flow. It was found that the BPE model was able to accurately account for the lateral displacement, but unable to fit the short-term reaction force data of all specimens tested. The TIBPE model was able to account for either the lateral displacement or the reaction force, but not both simultaneously. The LVE model was able to account for the complete reaction force, but unable to fit the lateral displacement measured experimentally. The BPVE model was able to completely account for both lateral displacement and reaction force for all specimens tested. These results suggest that both the fluid flow-dependent and fluid flow-independent viscoelastic mechanisms are essential for a complete simulation of the viscoelastic phenomena of articular cartilage.


2000 ◽  
Author(s):  
W. M. Lai ◽  
D. D. Sun ◽  
G. A. Ateshian ◽  
X. E. Guo ◽  
V. C. Mow

Abstract An important step toward understanding the signal transduction mechanisms that modulate cellular activities is the accurate prediction of the mechanical and electro-chemical environment of the cells in well-defined experimental configurations. One such configuration is the steady permeation experiment (e.g., bioreactors) in the open circuit condition. Using our triphasic theory, we have calculated the strain, velocity and the electric potential fields inside a layer of charged articular cartilage, through which a uni-univalent salt (e.g., NaCl) solution permeates under a constant pressure difference across the layer. The fluid flow through the tissue gives rise to an electrical potential difference across the tissue. This potential difference is the well-known “streaming potential” that is measured by Ag/AgCl electrodes placed across the tissue on the outside. Our results show that inside the tissue, in addition to the streaming potential caused by fluid convection, there is also a “diffusion potential” caused by cation and anion concentration gradients that are induced by the gradient of fixed charge density (FCD) inside the tissue. The gradient of FCD may be intrinsic, i.e., the tissue has an inhomogeneous FCD distribution, or it may also be caused by a non-uniform compaction of the solid matrix as is the case in steady permeation where the drag force exerted by the permeating fluid onto the solid matrix causes a compressive strain field inside the tissue. In this experimental configuration, the diffusion potential would compete against the streaming potential. The magnitude and the polarity of the electric field depend, amongst other material parameters, on the compressive stiffness of the tissue. For softer tissue (e.g., aggregate modulus <0.54 MPa for a set of realistic material and testing parameters), the diffusion potential dominates over the streaming potential and vice versa for stiffer tissue. For articular cartilage what the cells see in situ is the combined electrical effect of intrinsic and deformation induced inhomogeneity of FCD. The present results provide not only quantitative information, but also new insight into an important problem in biotechnology. These results also demonstrate that for proper interpretation of the mechano-electrochemical signal transduction mechanisms that is needed for modulating cellular biosynthetic activities, one must not ignore the important effects of diffusion potential.


2000 ◽  
Author(s):  
V. C. Mow ◽  
X. E. Guo ◽  
D. D. Sun ◽  
W. M. Lai

Abstract The objective of this paper is to provide an overall discussion of the biomechanical factors that are required to analyze and interpret data from the explant experiments and to present a description of some of the mechano-electrochemical events in the extracellular matrix (ECM) surrounding chondrocytes occurring within cartilage explants during loading. Five common loading cases of cartilage explants are discussed: hydrostatic pressure, osmotic pressure, permeation, confined compression and unconfined compression. Details of such surface loadings on the internal ECM pressure, fluid and ion flows, deformation and electrical fields are given. Similarities and differences in these quantities due to these five types of loadings are specifically noted. For example, it is noted that there is no practical mechanical loading condition that can be achieved in the laboratory to produce effects that are equal to the effects of osmotic pressure loading within the ECM. Some counter-intuitive effects from these loadings are also described. Further, the significance of flow induced compression of the ECM is emphasized, since this frictional drag effect is likely to be one of the major effects of fluid flow through the porous-permeable ECM. Associated streaming potential and diffusion potential and their dependence on the fixed charge density, are discussed in relation to the fluid flow through the charged ECM and the flow-induced compaction effect. Understanding of the differences among these explant loading cases is important; this can provide clearer understanding of the metabolic responses from chondrocytes in explant loading experiments.


1986 ◽  
Vol 108 (2) ◽  
pp. 123-130 ◽  
Author(s):  
A. F. Mak

Articular cartilage was modeled rheologically as a biphasic poroviscoelastic material. A specific integral-type linear viscoelastic model was used to describe the constitutive relation of the collagen-proteoglycan matrix in shear. For bulk deformation, the matrix was assumed either to be linearly elastic, or viscoelastic with an identical reduced relaxation spectrum as in shear. The interstitial fluid was considered to be incompressible and inviscid. The creep and the rate-controlled stressrelaxation experiments on articular cartilage under confined compression were analyzed using this model. Using the material data available in the literature, it was concluded that both the interstitial fluid flow and the intrinsic matrix viscoelasticity contribute significantly to the apparent viscoelastic behavior of this tissue under confined compression.


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