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ELECTRICAL PROPERTIES OF TISSUES AND CELL SUSPENSIONS:

MECHANISMS AND MODELS


H.P. Schwan
Bioengineering Department, University of Pennsylvania
Philadelphia, PA 19 104
ABSTMX.
The electrical properties of tissues and cell
suspensions are most unusu .I. They change with
frequency in three distinct steps and their dielectric
constants reach enormous values at low frequencies.
We concentrate on the linear properties observed
with applied fields less than about 1 V/cm. The linear
properties of interest include the dielectric constant E
and conductivity (T. Extensive measurements have been
carried out over a broad frequency range extending
from less than 1 Hz to many GHz. A number of
mechanism have been identified which explain the
observed data. These mechanisms reflect the various
compartments of the biological material. These include
membranes and their properties, biological
macromolecules and fluid compartments inside and
outside membranes. We summarize the mechanisms
which contribute to the total frequency response.
INTRODUCTKN
The dielectric properties of biological matter
and tissues are unusual for several reasons (Fig.1):
1. The electrical properties display at first glance
characteristics typical of fractal systems. The
frequency dependence of dielectric constant E and
conductivity (T can be approximated by a response
characterized by a frequency independent phase angle
and obeying both the Fricke and Kramers Kronig
relationships.
2. More detailed research revealed that changes with
frequency occur in three distinct major steps at low,
RF and GHz fequencies and termed a. fl and y
dispersions.
3. Dielectric constants reach enormous values of
millions relative to free space at low frequencies.
&DISPERSION.
This dispersion usually occurs in the range 0,l
- 10 MHz. Its mechanism was first analyzed by Hugo
Fricke and K.S Cole [l]. It is caused by the cellular
structure of tissues, with poorly conducting
membranes separating cytoplasm and extracellular
space. It takes time to charge the membranes through
the conducting phases in- and outside the cell
membranes. The time constant of this process is
readily derived from Laplacian potential theory and is
determined by cell membrane capacitance, cell radius
and the fluid resistivities [2,3]. Refinements and
extensions of the theory were developed and applied
to a large number of cell suspensions in order to
extract from AC bioimpedance measurements cellular
parameters such as membrane capacitance and fluid
resistivities in- and outside the cell by Carstensen,
Hanai and Schwan and their coworkers [2,3]. This
effect results from the inhomogeneous structure of
tissues and cell suspensions. Such effects are termed
Maxwell-Wagner effects since Maxwell treated the DC
case and Wagner exctendet it to AC frequencies.
Superimposed on the p-dispersion caused by
the cell are other effects which contribute to to the
tail of the main p-dispersion, including (2-5):
a. Relaxation effects caused by proteins and to a
lesser extend amino acid residues.
b. Smaller Maxwell-Wagner contributions caused by
organelles inside the cell, primarily cell nuclei and
mitochondria.
1 O8
l o5
IO
e
10 i o 6 10 Hz
10
10
CT
( mS / c ml
10
1
Fig.1. Dielectric constant E (decreasing) and
conductivity (T (increasing) as function of frequency.
0-7803-2050-6/94 $4.00 01994 IEEE 70a
y - DISPERSION.
The yeffect was noted for a variety of tissues
and protein solutions above 1 GHr [2-51. This effect
was not unexpected since water relaxes near 20 GHz
and tissues and cells contain much water. A weaker
subsidiary dispersion effect (&dispersion) is due to
protein bound water [2,4]. Such water appears to
display a broad spectrum of dispersions extending
from about 100 MHz to some GHz. It probably overlaps
with the small contributions due to amino acids and
polar subgroups of proteins aforementioned. The
quantitative details of the y -dispersions are fairly
well understood. It is obvious from the dielectric data
that tissue water is identical to normal water except
for the small fraction near proteins.
a -DISPERSION.
The discovery of the a-dispersion came as a
great surprise. I noticed it first with muscle tissue in
1948 and then with colloidal suspensions a few years
later. A multitude of various mechanism contribute
to a-dispersions [5]. The three best established
mechanism are:
a. The work with colloidal solutions indicated the
existence of frequency dependent surface conductances
and capacitances, largely caused by the response of
the counterion atmosphere existing near the charged
cell surface.
b. In muscle tissue the existence of the sarcoplasmic
reticulum appears to be primarily responsible for the
strong dispersion.
c. Cell membranes contain channel proteins whose
conductance varies with frequency. This is predicted
from the Hodgkin-Huxley equations.
The understanding of the a-dispersion remains
incomplete for several reasons:
a. Theories of the counterion atmosphere predict that
the dispersion should occur at lower frequencies than
observed with many cellular systems.
b. Most tissues with high water content display
similar low frequency dispersions, including tissues
without tubular systems. Furthermore, E Coli
suspensions display very high low frequency dielectric
constants, quite comparable to those of tissues.Thus
the effect can not be solely due to such systems as the
tubular system in muscle tissue.
c. The channel conductance effects appear to occur at
lower frequencies than the observed a-effect.
d. Some cells such as erythrocytes display no a-effect
while many other including E. Coli display remarkable
effects. Clearly, more work needs to be done to sort
out the various contributors to the a-response.
The table presents the various mechanisms
participating in the dielectric response of different
biological systems, advancing from simple water to
the complex case of cells with internal organelles,
proteins and charged membranes.
Table. Electrical Dispersions of Biomatter
Water and electrolytes Y
amino acids 6 + Y
proteins P + 6 + Y
Biological Macromolecules:
nucleic acids a + P + G + y
Vesicles, no surface charge II
P + Y
with " a + P + y
Cells with membranes:
+fluids free of protein P + Y
+ protein P + S + Y
+surface charge a + P + y
+membrane relaxation a + P + y
+organelles P + 6 + Y
+tubular system a + P + y
Cells with membranes, surface
charges, organelles, proteins a + P+ G+ y
REFERENCES
[l ] K.S. Cole, Membranes, Ions and Impul ses.
University of California Press, Berkeley and Los
Angeles,l968.
[2] H.P. Schwan, Electrical properties of tissue and
cell suspensions in: Advances in Biological and
Medical Physics . Vo1.5 , Editors: J .H.Lawrence and
C.A.Tobias. Academic Press, New York, pp. 147-209,
1957.
[SI K.R. Foster and H. P. Schwan, Dielectric
properties of tissues and biological materials: A
critical review, CRC Critical Reviews in Biomedical
Engineering 17:1, pp.25-104, 1989.
[4] E.H. Grant, R.J . Sheppard and G.P.South,
Dielectric behavior of biological molecules in solution.
Oxford University Press, Oxford., 1978.
[5] H.P. Schwan and S. Takashima, Electrical
conduction and dielectric behavior in biological
systems, in: Encyclopedia of Applied Physics, Vol.
Biophysics and Medical Physics, Editor: G.L. Trigg,
VCH publishers, New York and Weinheim,l993.
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