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Biophys J, March 2002, p. 1147-1152, Vol. 82, No. 3
Department of Physics, Yale University, New Haven, Connecticut 06520-8121 USA
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ABSTRACT |
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Many biological systems can be expected to exhibit resonance behavior involving the mechanical vibration of system elements. The natural frequencies of such resonances will, generally, be in the microwave frequency range. Some of these systems will be coupled to the electromagnetic field by the charge distributions they carry, thus admitting the possibility that microwave exposures may generate physiological effects in man and other species. However, such microwave excitable resonances are expected to be strongly damped by interaction with their aqueous biological environment. Although those dissipation mechanisms have been studied, the limitations on energy transfers that follow from the limited coupling of these resonances to the electromagnetic field have not generally been considered. We show that this coupling must generally be very small and thus the absorbed energy is so strongly limited that such resonances cannot affect biology significantly even if the systems are much less strongly damped than expected from basic dissipation models.
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RESONANCE ABSORPTION |
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The possibility that biological systems coupled
to the electromagnetic field can exhibit classical resonance at
microwave frequencies has long been of interest (Frölich, 1968
;
Maret et al., 1979
; Adair, 1995
), and that possibility has had an
impact upon microwave regulatory considerations (Stewart, 2000
).
Evidence of such microwave absorption resonances has been reported
(Edwards et al., 1984
; Grundler and Keilman, 1983
), but these results
have not been replicated (Gabriel et al., 1987
; Foster et al., 1987
).
We posit that for resonances to have an important effect on biology,
the system must absorb energy in excess of that from thermal noise. For
elements acting incoherently, that noise energy will be approximately
equal to kT, in which k is Boltzmann's constant and T is the Kelvin temperature. Such a significant energy
transfer requirement demands long relaxation times and significant
coupling strengths to the electromagnetic field. Although the
dissipation mechanisms have been studied extensively (Grundler and
Keilman, 1983
; Dorfman and Van Zandt, 1983
; Van Zandt, 1981
, 1986
),
less attention has been paid to the electromagnetic couplings, which we
consider here in some detail.
Because the biological systems that we consider will be much smaller
than the wavelength of microwave radiation, which is by definition
greater than 1 mm, any absorption of energy by the system must take
place through the interaction of the field with the dipole moment
charge distribution of the system. The absorption of energy by a
resonant system from a electromagnetic plane wave through a dipole
interaction can be expressed in terms of an absorption cross-section,
a in which (Blatt and Weiskopf, 1952
),
|
(1) |
a is the absorption width,
s is the scattering or emission width, and
=
a +
s is
the total width. The resonant frequency is
r,
and
= c/
is the wavelength of the radiation. The
cross-section
a is defined as the power
absorption per unit incident power flux and has the dimensions of area.
The widths,
j = dwj/w, with dimensions of
1/t are equal to the ratios of the energy loss rate,
dwj through the process, j, to the characteristic energy, w.
If the incident power flux is I W/m2,
the power, Pa, absorbed by the system
is,
|
(2) |
w, of the
resonant system where,
|
(3) |
a
s will generally obtain for biological systems
of interest.
Maximal cross-section and energy transfer
Taking
a
s,
the maximal absorption cross-section at
=
r will be
|
(4) |
We can use this relation to estimate a maximal width for a resonance to
generate a biological effect by taking the minimal energy deposition
per oscillator as,
w = kT/N1/2 in which
N is equal to the number of oscillator elements that act
coherently. (For most situations that we consider, N = 1.) Thus,
|
(5) |
Integrated cross-sections
The energy absorption cross-section integrated over all
frequencies,
|
(6) |
Under some circumstances the integrated cross-section lends itself to
useful limits. If the bandwidth of the incident radiation is 
,
the power transmitted to the resonant system,
|
(7) |
Radiative width
Because the biological systems of interest tend to be much smaller
than the microwave wavelengths, which are by definition greater than 1 mm, the coupling of the electric dipole moment to the radiative field
tends to be small, and the maximal absorption by the system will be
small. I estimate
s, the radiative width using
classical electrodynamics. The power P radiated by an
oscillating electric dipole is,
|
(8) |
= 2
c/
is the radial frequency
of the oscillator and d0 = qa is the maximal oscillating dipole moment, which I
describe in terms of an amplitude (a) and charge
(q) of an element with a characteristic mass (m).
With this model, I take the energy of the oscillator as,
|
(9) |
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(10) |
= 10 GHz,
q = e, m = mp = 1.67 × 10
27 kg,
s = 1.34 × 10
6 s
1, and
s = 1/
= 7.5 × 105 s. Even as the lifetime of such states by
radiative decay is very long, the radiative width (and thus coupling to
the electromagnetic field) is very small.
Absorption width: relaxation time
The kinetic energies of moving biological elements will be lost to internal and external dissipative frictions. Moving generally in an aqueous environment such as the cytoplasm or tissue plasma, the characteristic velocities of motion are usually small, and the appropriate Reynold's number is usually much less than one. Thus, the energy transfer to that environment follows largely from viscous friction.
We consider an element with a mass, m, and a characteristic
length, r, vibrating in the liquid with a frequency
=
/2
and an amplitude, a. The energy of the element
will be, w = 1/2
m
2a2. From
Stokes law considerations, the retarding frictional force will be,
|
(11) |
= 1 for a sphere of radius r and µ is taken as the viscosity of water.
The power lost to viscous friction will be
dw/dt = Fd
a, and the time
constant (or lifetime) will be
|
(12) |
(4
/3)r3 and
= 1. Then
|
(13) |
and µ as
the density and viscosity of water, and r is measured in meters.
The oscillatory motion of near-cylindrical elements in the direction of
their axis generates resistive forces. For a cylinder of radius
(r), length (L), oscillating longitudinally with
a frequency
=
/2
, and amplitude (a), the
retarding force can be expressed approximately as
|
(14) |
Taking the mass of the cylinder as
r2L
, in which
is
the density of the cylindrical material,
|
(15) |
9 m, and
and µ taken as that of water,
=
a = 1/
a
10
11 s and such systems will generally be
critically damped at microwave frequencies.
Under some circumstances, a system that oscillates with mechanical
movement will lose energy through the inertial forces exerted in moving
the surrounding liquid and thus generating sound waves. Such inertial
effects can only be expected for systems described by Reynold's
numbers, Re =
rv/µ > 1 in which
r and v are characteristic lengths and velocities
of the object. For most biological systems oscillating at microwave
frequencies, Re
1 and acoustic energy losses will not be important.
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LONGITUDINAL VIBRATIONS IN CYLINDRICAL SYSTEMS |
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DNA
For the candidate resonances that we consider, the elements moving
in their aqueous biological elements will lose energy to the
surrounding liquid through viscous impedance. "Organ pipe" standing
sound waves propagated longitudinally along cylindrical structures,
such as DNA, seemed likely to have the longest relaxation times for
elements in water. However, Dorfman and Van Zandt (1983)
showed that
with plausible assumptions on the character of the viscosity, such a
resonance (and a resonance in any other mode) would be over-damped.
However, in the course of considering resonances in the DNA microwave
absorption spectra reported by Edwards et al. (1984)
and interpreted as
such sound waves, Van Zandt (1986)
revisited the subject and concluded
that relaxation times for such vibrations might be as long as
a
5 ns, a value taken from the narrow
widths,
a
200 MHz, of his calculated
resonances. Even as the theoretical widths were an order of magnitude
smaller than the experimental widths, the calculated value of the
relaxation time was an order of magnitude longer than the times
suggested by the data that the authors (Edwards et al., 1984
) estimated
as
a < 500 ps.
Following this previous work, I consider specifically the DNA strand of
5480 base pairs with a mass of ~106 Daltons and
a length, s, of ~3.3 µm. I assume coupling to the field
through single charges q = e at each end
thus a permanent dipole moment of 5.3 × 10
25 Cm.
For a given value of the relaxation time and the corresponding
absorption width, the maximal resonant cross-section, as calculated from Eqs. 4 and 10, is independent of frequency.
|
(16) |
a = 1/
a = 5 ns, q = e, and an incident microwave power
level I = 100 W/m2 (10 mW/cm2), about the recommended regulatory limit
for general human exposure (IEEE, 1991), the maximal energy stored by
the resonant system would be
w = 1.15 × 10
29 J = 2.8 × 10
9 kT. Thus, the absorption of microwave
radiation by such resonances cannot be expected to affect biology even
if the resonant modes are not so strongly damped. Indeed, the stored
energy can only be large if the state is very long lived and, hence,
very narrow. For
w > kT, when the
incident power density is I = 100 W/m2m then
< 10 kHz.
Although the value q = e, chosen to describe the oscillating dipole moment already implies a very large permanent dipole moment, if the oscillating charge were greater than 2 × 104e, the radiative absorption from the canonical incident microwave power density would be increased to detectable levels if the relaxation time is as large as 5 ns. But so large a charge leads to a moment that seems far outside of our understanding of DNA or any other molecule.
The conclusion that there can be no microwave resonances in DNA in
water is in accord with the results of measurements in three different
laboratories (Gabriel et al., 1987
; Foster et al., 1987
) using
techniques designed to detect resonances with amplitudes less than
1/20th of that reported by Edwards et al. (1984)
.
Voltage-gated ion channels
The voltage-gated ion channels, important in the generation and propagation of action pulses in neurons, are of special interest here because the well-established dipole moments of the protein channel play an essential role in neurophysiology. Hence, any significant effect of the interaction of microwaves with these elements through their dipole moments can be expected to translate directly into physiological effects.
Most varieties of the protein channels that pass cations through the
cell membrane upon changes in the membrane potential appear to be
constructed of four similar segments, conventionally labeled I, II,
III, and IV, each of which crosses the membrane. Each segment seems to
be divided into six sectors, S1, S2, ... S6 (Hille, 1992
; Shepherd,
1994
). The segments, which seem to act nearly independently of each
other, appear to change their configuration from a closed state to an
open state when the potential difference across the membrane changes
from the resting polarization potential, typically near
Vm =
70 mV, to near zero. The
channel is open to ion transmission when four (or, perhaps, three)
segments are in the open state.
The change in the segment configuration appears to result from the
effects of the transmembrane field on dipole moments held in the S4,
"voltage-sensing," sector of each segment. When the channel is
depolarized a "gating-current" flows with a total charge transfer
across the membrane of approximately Q = 6e.
The occupations of the open and closed configurations, as estimated
from statistical mechanics, are consistent with the view that the
energy difference between the open and closed channel configurations is
approximately equal to QVm. Thus, we
tentatively describe dipole moment of each of the four S4 sectors as
d0 = Qdmem/4 = 1.5edmem in which
dmem
7 nm is the membrane thickness.
The mass of each segment appears to be near 75 kD, and we take the
effective moving mass as that of the S4 sector at m
15 kD. (If the moving mass is larger, the absorbed energy will be smaller.)
In each cell or active sector of a cell (e.g., the nodes of Ranvier)
there are very many channels that act together. Moreover, the dynamics
is complicated by positive feedback effects such that the opening of
channels admits ions that change the membrane potential in a manner
that further increase the channel open probability. However, for
standard Hodgkins-Huxley Na channels (Hodgkins and Huxley,
1952
), we know that there is an effective threshold of approximately
Vm
6 mV for the cascade that
results in neuron spike generation (Koch, 1999
). Thus we can take
Q
Vm
kT/3
as a rough measure of the energy threshold, applied to one channel, for
significant effects.
Using the same arguments as for the DNA resonance and thus Eq. 16, we
find that for I = 100 W/m2, and
w = kT/3,
< 225 kHz. Estimating
a = 1/
10 GHz from Eq. 13, we see
that, despite the large uncertainties in the estimates, microwaves of
moderate intensity cannot be expected to effect neurophysiology through
resonant interaction of the S4 voltage-sensor sectors.
Resonances in microtubules
Pokorny and colleagues have argued that microtubules in cells will
exhibit sharp mechanical resonances at megahertz frequencies (Pokorny
et al., 1997
). However, K. R. Foster and J. W. Baish (personal communication) have shown that the resonances would be
strongly damped by viscous processes.
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COHERENT PROCESSES |
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Frölich (1968)
has emphasized the possible importance of the
oscillations of systems where many dipole moments act coherently. In
particular, he has suggested that such oscillations may be generated in
the cell membranes that may affect biology. Following the specific
example he describes, we consider such a membrane normal to the
electric field where internal and external electric charges that
account for the normal Vmem
60 mV
polarization potential across the membrane form dipole moments. The
alternating electric field will induce alternating compressive and
expansive (tension) forces on the membrane through their action on the
charges that bound the membrane.
We can expect a resonance frequency such that
res = vmem/dmem
2 × 1011 Hz, and we estimate
vmem, the speed of sound in the
membrane, as 1500 m/s, the speed of sound in water. The wavelength is
then
= 1.5 mm.
Taking the specific capacity of the membrane as
cm = 0.01 F/m2
(1 µF/cm2) and the resting potential as
Vm =
60 mV, the charge density Q = Vmcm
7 × 10
4 C/m2. Thus the
charge on a characteristic sector of membrane with an area,
A = L2 = 10
10 m2 will be
q
7 × 10
14 C.
We can estimate the mass of the sector as m = L2dmem
7 × 10
16 kg by taking the membrane
element as an area L2 in which
L = 10 µm, a thickness as
dmem = 7 nm, and
= 1000 kg/m3, the density of water.
With these values we find, using Eq. 9,
|
(17) |
We estimate a relevant Reynold's number as Re =
L
a/µ
2 × 104 × a in which a is the
amplitude in nm. If a is large, and Re
1, the vibrating membrane will displace fluid inertially generating acoustic waves.
For a vibrational amplitude a, the energy of membrane
vibration will be, w
(1/8)m(
a)2. The
corresponding acoustic power density will be p = cm × 2
(
a)2 in which
cm
1500 m/s is the velocity of
sound in the liquid bordering the membrane and the factor "2" takes
into account the two sides of the membrane.
The power lost by the membrane, radiating in two directions, will then
be, dw/dt = L2p = cm
L2(
a)2
and the lifetime of the state will be
|
(18) |
m
Because this life time is less than the radiation period,
a = 1/
5 × 10
12 s, the membrane vibrating in water will be
so over-damped that we can expect no resonance.
Taking these values of
s and
a, the incident intensity again as
I = 100 W/m2, and a frequency
= 2 × 1011 Hz from Eq. 4, the
maximal energy deposition will be
|
(19) |
From Eq. 5, we can express the limit for biological potency in terms of
a maximal width (and minimal damping). If the oscillation energy is to
be greater than kT, the resonance width
< 1.4 MHz.
If the amplitudes are small and Re < 1, inertial
effects will be negligible and the vibration will be damped viscously.
Here we estimate the retarding viscous force following the Stokes
recipe for a sphere as F
6
µLv in
which v =
s. The dissipated power will
then be, dw/dt = Fv = 6
µLv2. The lifetime will then be
|
(20) |
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MAGNETOSOME RESONANCES |
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Kirschvink (1996)
has suggested that the resonant interaction of
microwaves with magnetosomes may affect biology through ultrasound emitted by the magnetosomes. Energy absorbed by the domains through the
coupling of their magnetic moment with the radiative field would be
presumed to generate such sound through the known magnetoacoustic effect.
At the resonant frequency, the external AC field generates a precession
in the electrons that contribute to the ferrimagnetism. For an electron
that is not strongly coupled magnetically to its nearby environment
that angular frequency is simply,
= Be/m = 1.76 × 1011 × Bext, in
which e and m are the charge and mass of the
electron and Bext is the external
field imposed on the material. However, in ferromagnetic and
ferrimagnetic materials, that frequency is strongly modified by dipolar
interactions with near neighbors and depends on both the external field
and internal demagnetizing fields present in the magnetic domains. In
turn, those fields depend strongly on the shape of the domain with
respect to the crystal structure (Kittel, 1949
; Kittel and Abrahams,
1953
).
Radiative width
The moment of a single domain magnetosome of volume, v,
is m0 = H'v in
which H' = 4.8 × 105 A/m. Then,
for a cubical magnetosome dm = 50 nm
on a side, m0 = 6 × 10
17 Am2, which we take
as a typical value for a magnetosome. For such a perfect cube, the
resonance frequency,
r, will be ~1.1 GHz (Kittel, 1949
). Shape anisotropies add as much as 8 GHz to this; for
our calculations we chose a canonical frequency of
r = 2 GHz.
The power p radiated by a such a magnetic dipole moment
oscillating at a frequency of
= 2
r = 1.26 × 1010 rad/s is that expressed by
Eq. 8 with the substitution,
d0
m0/c, p
1.1 × 10
25 W.
The frequency is that of the precession of the electrons in the
demagnetizing field (Van Vleck, 1951
). Taking that precession frequency
as
e = Be/m = 1.76 × 1011 × B rad/s, we have
B = 0.0714 T and a characteristic alignment energy,
w = Bµ = 4.3 × 10
18 J. From this, we estimate
s
P/w = 2.6 × 10
8 s
1.
Absorption width
The absorption width, very much greater than the radiative width,
is not as well known. For the purpose of our illustrative calculations,
we take the estimate of Abrahams (Kittel and Abrahams, 1953
) that the
lifetime of ferrimagnetic resonance is likely to be
7 × 10
7 s and then
a
1/
= 1.4 × 106
s
1.
Absorbed power and stored energy
From Eq. 4, the power absorbed by the magnetosome at resonance in
a radiative field of 100 W/m2 power density is,
p = 1.6 × 10
13 W and the
stored energy will be
w = P/
= 1.15 × 10
19 J
25 kT. If this
energy were entirely manifest as heat, the temperature of the
magnetosome would be increased by
T
5 × 10
4 oC, which is, of course, biologically
negligible. If all of the energy were engaged in acoustic vibrations of
the element, we can estimate the velocity of motion of the surface as
v
(2w/m)1/2
0.75 m/s.
Writing Reynold's number in the surrounding fluid as
Re =
dmv/µ
0.05, it is
clear that any vibration will dispense energy in viscous resistance
rather than the mass movement of acoustic radiation.
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CONCLUSIONS |
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There are both theoretical conjectures (Frölich, 1968
; Van
Zandt, 1986
) and experimental results (Edwards et al., 1984
; Grundler and Keilman, 1983
) that suggest that low intensity microwaves fluxes
might affect biology through the excitation of elastic resonances in
biological systems. We extend analyses that suggest that the damping of
the vibratory motion by biological fluids severely restrict such
possibilities (Van Zandt, 1986
) by showing that typical systems will
not be coupled to the electromagnetic fields with sufficient strength
to allow significant energy transfers although the damping constraint
be somewhat relaxed.
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FOOTNOTES |
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.
Address reprint requests to Dr. Adair, Yale University, Department of Physics, 260 Whitney Avenue, JWG 514, New Haven, CT 06520-8121. Tel.: 203-432-3370; Fax: 203-432-6125; E-mail: robert.adair{at}yale.edu.
Submitted March 1, 2001, and accepted for publication May 7, 2001.
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REFERENCES |
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Biophys J, March 2002, p. 1147-1152, Vol. 82, No. 3
© 2002 by the Biophysical Society 0006-3495/02/03/1147/06 $2.00
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