Electromagnetic Fields - American Chemical Society

Downloaded by COLUMBIA UNIV on July 24, 2012 | http://pubs.acs.org Publication Date: May 5, 1995 | doi: 10.1021/ba-1995-0250.ch008

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Str eaming and Piezoelectric Potentials in Connective Tissues Laura A. MacGinitie Department of Engineering, Pacific Lutheran University, Tacoma, WA 98447

Stress-generated potentials of bone, cartilage, and tendon are reviewed to identify ranges of physiological electricfieldmagnitudes and to relate thesefieldsto tissue properties such as matrix structure and composition, molecular interactions, and interstitialfluid.The range of physiologicalfieldmagnitudes may indicate the range of physiological or externalfieldmagnitudes that can modulate tissue behavior. Because stress-generated potential magnitudes and frequencies depend on tissue properties, potential measurements may be used to assess normal and abnormal tissue properties. Piezoelectric potentials are generated by loading dry tissues, whereas streaming (electrokinetic) potentials (SPs) and currents are generated by loading hydrated tissues. SPs generated by bending cortical bone are 1 order of magnitude smaller, when normalized to strain, and relax 2-4 orders of magnitude faster than SPs generated by compression of cartilage disks. Estimated maximum current densities at cell sites are on the order of 10µA/cm for bone and 1mA/cm for cartilage. These ranges may suggest that external or environmental fields must produce tissue-level current densities of this magnitude to alter connective tissue behavior. Trabecular bone SPs are smaller than cortical bone SPs. Microscopic measurements of bone SPs and models for SP generation in bone and cartilage indicate that field magnitudes andfrequenciesdepend on tissue properties. 2

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0065-2393/95/0250-0125$12.00/0 ©1995 American Chemical Society

In Electromagnetic Fields; Blank, M.; Advances in Chemistry; American Chemical Society: Washington, DC, 1995.

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T

HE STRESS-GENERATED ELECTRIC POTENTIALS that have been observed in a


variety of connective tissues including bone, tendon, and cartilage may provide clues for understanding possible field effects on tissues, as well as con nective tissue anatomy and composition. These endogenous electric fields may be a biological signal regulating growth, remodeling, and repair of connective tissues. The magnitudes and frequencies of endogenous fields may also indicate the range of externally applied field values that could affect the same tissues. In addition, measurement of the endogenous fields in connective tissues can pro vide information regarding the tissue structure, such as channel or pore sizes, matrix and fluid composition, and molecular interactions within the connective tissues. Early investigators attributed the potentials produced by bending dry bone and tendon to piezoelectricity (1-3). Piezoelectric potentials are due to polariza tion produced by mechanical-strain-induced deformation of bonds. Subsequent investigation of stress-generated potentials in hydrated bone, cartilage, and ten don, however, suggested that under physiological conditions, the measured stress-generated potentials are electrokinetic in origin, or "streaming potentials" (4-6). This chapter, therefore, will focus primarily on streaming, rather than on piezoelectric, potentials because these appear to dominate macroscopic meas urements of stress-generated potentials in connective tissues under physiological conditions. Furthermore, these fields produced by streaming may modulate con nective tissue repair and remodeling. Some investigators have suggested (7-9) that piezoelectric fields may also be important to bone remodeling, although these fields have not been measured definitively in moist bone. Streaming potentials (SPs) and currents (SCs) are produced by stressdriven fluid flow past a charged surface. In both bone (5, 6) and cartilage (10), the matrix is negatively charged at physiological p H . Fluid flow in the charge double layer adjacent to the charged matrix produces a convective current in the same direction (Figure 1). The resulting charge separation creates an electric

Figure 1. Schematic of models for streaming potential (SP) generation by (a)flowthrough cylindrical channels (one model for SP generation in bone) and (b)flowpast charged cylindrical rod molecules (one model for SP generation in cartilage). cm (69) vs. approximately 15-55 kQ-cm (70)]. If the intertrabecular spaces in trabecular bone contribute to fluid relaxation as the Haversian canals do in cortical bone, then SPs of trabecular bone (neglecting any contribution by the marrow) would have a similarfrequencyresponse but smaller magnitude compared with SPs of cortical bone. Thus, measured SP magnitude in trabecular bone is approximately as expected on the basis of tra becular structure, but thefrequencyresponse is not. Measured differences in the frequency response between trabecular and cortical bone SPs therefore cannot be explained in terms offluidrelaxation to the Haversian canals or intertrabecular spaces alone.

Stress-Generated Fields of Cartilage SPs of cartilage due to hydrostatic pressure gradients werefirstobserved by Maroudas et al. (71). Subsequently, electric potentials were also measured in re sponse to tissue stress (72, 73). These stress-generated potentials were identified as SPs by Grodzinsky et al. (74), on the basis of their dependence onfluidcon centration, pH, and the similar relaxation behavior of the electric potential and stress. Furthermore, following digestion with hyaluronidase to reduce the net negative matrix charge, the potential decreased. The SPs across disks of cartilage were then more fully characterized by Lee et al. (75) and Frank and Grodzinsky (76) for sinusoidal loading in confined compression, and by Kim et al. (77) for loading in unconfined compression. Macroscopic Streaming Potentials and Currents of Normal Cartilage* SPs generated by compressive loading of articular cartilage are



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MACGINITIE SPS and Piezoelectric Potentials in Connective Tissues

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Figure 4. SP magnitude and phase as a function offrequency of compression across a cartilage disk in 0.001 MNaCl The line indicating theory is thefitob tained using the model of Frank and Grodzinsky; kg is the ratio of the electroki netic coupling coefficient to the electrical conductivity. (Reproduced with pe missionfromreference 82. Copyright Elsevier 1982.)

larger than those generated across bone, whereas the frequency response (Figure 4) is similar in shape to that of SPs generated by bending bone, although the characteristic relaxation time is longer. SPs of cartilage in physiological saline increase monotonically with frequency in the physiological loading range be tween 0.001 and 20 Hz. A t the higher frequencies (e.g., near 10 Hz), SP magni tude is on the order of 20 μΥ/με for confined compressive sinusoidal loading of plugs of articular bovine cartilage 1 mm thick (75). SP phase relative to dis-


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placement decreases monotonically with frequency from a value less than π/2 below 0.01 H z toward an asymptote near zero at higher frequencies. The charac teristic relaxation time, τ = l IH k, where / is a characteristic length, H is the bulk modulus, and k is the permeability, is on the order of 10 min (78) for 1-mm-thick cartilage disks, compared with 0.1-3 s for cortical bone. Streaming current (SC) densities on the order of 1 μΑ/cm were measured for compressive sinusoidal loading of bovine articular cartilage plugs approximately 800 μιη thick in 0.005 M NaCl [for 10 me, near 1 H z (76)]. Because theory predicts that SCs should not depend on NaCl concentration (assuming that ζ potential is in dependent of NaCl concentration), similar currents should be expected at physiological saline concentrations. Frank and Grodzinsky (76) predicted that in vivo currents would be 50-100 times higher because of lower impedance at the articular surface in vivo compared with measurement conditions. 2

k

A


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Macroscopic SPs of Osteoarthritic and Enzymatically Digested Cartilage. SPs have been measured for cartilage taken from a rabbit model for osteoarthritis, and following digestion by trypsin or chondroitinase A B C to model the proteoglycan (PG) loss that accompanies osteoarthritis. Hoch et al. (79) measured SPs of articular cartilage disks cored from rabbit knee joint fol lowing meniscectomy and subjected to a 0.1-Hz sinusoidal compression. The SP of osteoarthritic-like knee cartilage compared with control cartilage followed the same trend with time after surgery as the mechanical stiffness and glycosaminoglycan (GAG) content, as assessed by uronic acid assay. Lee et al. (75) meas ured SPs of articular bovine cartilage in confined compression before and after a 6-h digestion with trypsin to remove G A G and noncollagenous protein. SPs de creased to approximately one-third the initial value following digestion by tryp sin for 6 h. Frank et al. (80, 81) similarly observed that SPs generated by sinu soidal compression of cartilage disks decreased with time as these disks were digested using trypsin, chondroitinase A B C , and hyaluronidase. SPs were

Electromagnetic Fields - American Chemical Society

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