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ISSN 00063509, Biophysics, 2009, Vol. 54, No. 6, pp. 741–747. © Pleiades Publishing, Inc., 2009.
Original Russian Text © G.V. Novikov, V.V. Novikov, E.E. Fesenko, 2009, published in Biofizika, 2009, Vol. 54, No. 6, pp. 1120–1127.
741
INTRODUCTION
In most of the experiments performed with the aim
of studying the influence of weak combined alternat
ing and static magnetic fields (MFs) on biosystems,
use was made of fields where the amplitude of the
alternating component constituted tens of
microteslas, and they were conducted on the back
ground of a static field (SMF) of commensurate mag
nitude. However, there are a number of publications
testifying that alternating fields (AMF) of the nan
otesla range are also capable of inducing pronounced
biological effects [1–11]. It should be noted that in the
absolute majority of cases the experiments with weak
AMF were conducted at the background of the geo
magnetic field (GMF), the induction of which consti
tutes ~50
μ
T. In the given work we consider the action
of a combined field (CMF) comprising a static com
ponent comparable to GMF and a collinear alternat
ing component with induction of tens or hundreds of
nanoteslas. The AMF has a frequency in the range 0.5–
20 Hz, i.e., it is ultraweak and ultralowfrequency.
A phenomenon most surprising and interesting in
the basic and applied aspects is the antitumor effect of
weak and ultraweak MFs and electromagnetic fields
discovered by a number of authors in different ranges
of frequency and intensity [7, 10, 12, 13].
We have earlier disclosed an antitumor activity of
weak CMF tuned to the cyclotron resonance of the
ions of naturally charged amino acids [7, 9, 10, 14]. In
these works, mice with ascites and solid forms of Ehr
lich adenocarcinoma were exposed to a complex
enough multifrequency magnetic signal, being a
superposition of five frequencies corresponding to the
cyclotron frequencies of the ionic forms of tyrosine,
arginine, lysine, glutamic and aspartic amino acids.
A formal basis for testing the biological activity of this
particular signal was the earlier found reaction of the
ion current in water solutions of these amino acids to
the action of CMFs tuned to the cyclotron resonance
of the ions of the corresponding amino acid [15, 16].
In this connection it should be noted that such an
action of weak CMFs was later registered by other
authors as well in water solutions of amino acids by
nonlinear dielectric spectroscopy and voltammetry
[17, 18].
From our results obtained earlier, the following
main conclusions can be made[19]: the action of weak
combined static (42
μ
T) and lowfrequency alternat
ing (3.5–5.0 Hz; 50–100 nT) MF causes an inhibitory
effect on the development of ascites and solid Ehrlich
tumors in mice, which is especially pronounced at the
early stages of tumor development; the action of weak
MFs on mice bearing the Ehrlich ascites tumor (EAT)
initiates a complex of structural alterations in the
tumor tissue including, in particular, chromatin mar
gination (karyorhexis) and pronounced vacuolization
of the cytoplasm; the action of weak MFs on mice
bearing the Ehrlich solid tumor initiates a complex of
structural and ultrastructural alterations in the tumor
tissue, in particular, fragmentation of nuclei and for
mation of bodies of the apoptotic type; the results
Effect of Weak Combined Static and LowFrequency Alternating
Magnetic Fields on the Ehrlich Ascites Carcinoma in Mice
G. V. Novikov, V. V. Novikov, and E. E. Fesenko
Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region, 142290 Russia
Received October 20, 2008
Abstract
—The parameters of the lowfrequency (1, 4.4, 16.5 Hz or the sum of these frequencies) extremely
weak (300, 100, 150–300 nT, according to frequencies) alternating component of combined magnetic fields
have been found, which in combination with a weak collinear static field of 42
µ
T (the induction corresponds
to the range of the geomagnetic field) has a marked antitumor activity. The exposure to these magnetic fields
inhibits the tumor growth in mice with an intraperitoneally transplanted Ehrlich ascites carcinoma. The
effect manifests itself as an increase in the life of tumorbearing animals and in the content of damaged tumor
cells. It was found that the death of tumor cells by the action of weak fields occurs predominantly by the
mechanism of necrosis.
Key words:
weak magnetic fields, malignant tumors, Ehrlich ascites tumor
DOI:
10.1134/S0006350909060141
Editor’s Note:
I certify that this text exactly reproduces the factual
statements and closely conveys the phrasing and style of the origi
nal Russian publication.
A.G.
COMPLEX SYSTEMS
BIOPHYSICS
742
BIOPHYSICS Vol. 54 No. 6 2009
NOVIKOV et al.
obtained testify to a selective damaging action of weak
MFs on tumor cells not affecting the cells of healthy
tissues; MFs at the level of the whole organism activate
its defense functions, which manifests itself as the
reaction from blood cells (some increase in the num
ber of lymphocytes, monocytes, and neutrophils in the
ascitic fluid), activation of the phagocytic function of
macrophages, activation of the synthetic ability of
fibroblasts producing collagen for formation of con
nective tissue capsule delimiting the regions of accu
mulation of tumor cells in tumor nodes.
Further we set ourselves a goal of ascertaining
which of the frequencies of the complex signal possess
preferentially antitumor activity [7]. It was established
that a pronounced inhibitory effect on the tumor pro
cess, greater than the initial complex signal (sum of
five frequencies), is caused by a simple twofrequency
signal being a sum of two frequencies 4.38 and
4.88 Hz, formally corresponding to the cyclotron fre
quencies of the ionic forms of glutamic and aspartic
acids at the used value of the static component
(42
μ
T). It should be noted that none of the monofre
quencies in the range of the complex signal did not
possess pronounced activity at the values of the alter
nating MF component amplitudes studied in the work.
The action of monofrequencies of the AMF compo
nent on the tumor process was clearly studied insuffi
ciently. The only pronounced response was noted at
the monofrequency of 16.5 Hz, formally correspond
ing to the cyclotron frequency of K
+
ions, at the AMF
magnitude equal to 80 nT. This result coincides in the
choice of frequency with the data of Liboff [20] about
the antitumor activity of CMF upon tuning to the
cyclotron resonance of potassium ions.
The solution found by us earlier for the problem of
formation of biological activity of a MF on the basis of
twofrequency signals allowed introducing a known
transform:
to represent the sum of frequencies as the product of
modulating (
ω
1
–
ω
2
/2) and carrier frequencies (
ω
1
+
ω
2
/2) [9]. In this case we experimentally established
the values of effective modulating frequencies at car
rier frequencies in the ranges 3.7–5.2 and 15.5–
17.5 Hz. However, up to the most recent time the fre
quency–amplitude dependences of the antitumor
effect of weak CMFs on monofrequency components
of the alternating MF component have not been
experimentally obtained. It also remained not quite
clear in what way a multifrequency magnetic signal
becomes more biologically active as compared with
the action of the field at monofrequencies.
EXPERIMENTAL
Object of study.
The action of weak MFs on the
development of tumor tissue was studied using tumor
bearing mice with intraperitoneally transplanted EAT
cells. The choice of the given model for experimental
analysis was determined by the circumstance that the
ascites form proved more sensitive to the action of
weak MF as compared with the solid form [19].
During grafting of EAT, each animal (male SHK
mice) was usually injected intraperitoneally with
10
6
tumor cells in 0.5 mL of isotonic solution. At the
given quantity of EAT cells the tumors formed in mice
not exposed to MFs (animals of control groups) in
100% cases. The visual marks of tumor formation were
noted by the sixth–seventh days after inoculation of
tumor cells in the form of an increase in the abdominal
perimeter at the expense of accumulation of ascites
fluid in the peritoneal cavity. At the 13–18th days the
animals of the control group died.
Parameters of MF and method of their formation.
The installation for magnetic exposure of tumorbear
ing animals (Fig. 1) consisted of two pairs of coaxially
positioned Helmholtz coils oriented along the GMF
vector. As the static MF component, we used the local
GMF partly compensated to 42
±
0.1
μ
T with the help
of one of the Helmholtz coil pairs. The alternating
component collinear to the SMD was formed with the
use of the second Helmholtz coil pair. Treatment of
mice with weak MFs was conducted in semitranspar
ent plastic (polypropylene) containers in the light time
of the day under natural illumination. All animals in
each series of experiments were exposed to the action
of the field at one moment. The MF exposure was
conducted at room temperature of 18–22°C.
A0ω1tsin A0ω2tsin+
=
2A0ω1ω2
+()t/2 ω1ω2
–()t/2cossin
PC DAC Amplifier Compensator
MF
Fig. 1.
Block scheme of the experimental installation for
the action of weak MFs on biological objects in the pres
ence of GMF. Biological objects are in the zone of action
of MF formed by Helmholtz coils. The coils are oriented
so that the vector of the artificial MF is parallel to the
GMF vector. To form the preset value of the static MF
component, use is made of a compensator electrically
linked with the Helmholtz coil system. The compensator is
a source of DC. With its help the static component of
GMF is amplified or attenuated, to be used in the experi
ment as the MF static component. A personal computer
(PC) with a digital–analog converter (DAC) generate an
electrical signal with preset frequency–amplitude charac
teristics, which through an amplifier is fed to the coil sys
tem and forms the alternating component of the MF.
BIOPHYSICS Vol. 54 No. 6 2009
EFFECT OF WEAK COMBINED MAGNETIC FIELDS ON ASCITES TUMOR 743
Series of experiments were conducted at the AMF
frequency of 16.5 Hz (frequency corresponds to the
cyclotron frequency of potassium ions at SMF induc
tion of 42
μ
T) in two variants: at monofrequency and
in the presence of a modulating frequency. Use was
made of the following series of intensities: 40, 80, 150,
200, 250, 300, 350, 400, 500 nT (effective values of
AMF amplitude). In the case of using a twofrequency
signal the modulating frequency constituted 0.5 Hz.
This value was chosen on the basis of the results of
work [9]. The next step were the series of experiments
at AMF frequencies of 0.5 and 1 Hz separately (fre
quency of 0.5 Hz corresponds to the optimal value of
modulating frequency found in preceding experi
ments). Use was made of a series of intensities: 40, 80,
150, 200, 250, 300, 350, 400, 500 nT.
Further series of experiments were conducted at an
AMF frequency of 4.4 Hz (frequency corresponds to
the cyclotron frequency of glutamic amino acid at
SMF induction of 42
μ
T). The following series of
AMF intensities was used: 40, 65, 80, 100, 140, 200,
250, 300 nT.
Then experiments were conducted on acting with a
complex magnetic signal representing a sum of three
frequencies (1; 4.4; 16.5 Hz), with optimal intensities
of individual frequencies established in previous
experiments.
Each experiment was repeated not less than three
times, with the number
n
of animals in each experi
ment equal to 10.
The control of the values of the acting fields was
conducted by direct measurement with a ferroprobe
magnetometer Mag03 MS 100 Bartington (Great
Britain). The level of external magnetic interference in
the range of industrial frequency (50 Hz) constituted
10–50 nT. The action was implemented from the first
day after tumor grafting, the duration of one session,
1 h daily; the total number of exposures, 12.
To each series of experiments, there was its own
control group of animals, in which mice were in SMF
with the static component of ~42
μ
T and the same val
ues of magnetic interference as the test groups (mice
were placed into the experimental installation with the
AMF source switched off).
Evaluation of the efficiency of MF action on the
tumor process.
To assess the antitumor effect of MF,
we registered the lifetimes of animals after injection of
tumor cells. We also conducted cytological analysis of
the state of EAT cells isolated from the peritoneal cav
ity of tumorbearing animals. To prepare cytological
specimens, the content of the peritoneal cavity of ani
mals in equal amounts was applied onto glass slides
and smears were made. Assessment of the tumor cell
state was conducted by the method of light microscopy
after preliminary fixation of the smears with 96% ethyl
alcohol and their staining with hematoxylin–eosin by
the Romanovsky–Giemsa method. After visual analy
sis, the relationship was counted of damaged tumor
cells and healthy ones out of the total number (1000)
of cells.
Statistical processing of results.
The results of
investigation were statistically processed with the use
of the Student’s
t
test.
RESULTS AND DISCUSSION
Upon studying the dependence of the intensity of
antitumor effect on the amplitude of the alternating
MF component (at carrier frequency 16.5 Hz and
modulating 0.5 Hz) we noted a growth of the antitu
mor effect in the range of 40–300 nT and subsequent
decline of the activity of the field exposure with a fur
ther increase of the amplitude (Fig. 2). The maximal
antitumor effect in this case is achieved at a value of
AMF amplitude 300 nT.
A natural continuation of investigations came as
determination of the dependence of the antitumor
effect on the amplitude of the monofrequency mag
netic signal at the carrier (16.5 Hz) and modulating
(0.5 Hz) frequencies separately. The data obtained at
the 16.5 Hz frequency are presented in Fig. 3. Note
worthy is the somewhat less pronounced antitumor
activity of MF in this case as compared with preceding
experiments. It is also noted that the magnitude of the
effect remains approximately constant in the ampli
tude range 150–300 nT. In this connection its can be
supposed that the observation of a maximum of the
effect at 300 nT for a twofrequency signal with the use
of a modulating frequency (0.5 Hz) is associated just
with its presence. The results obtained upon conduct
ing further experiments have confirmed this sugges
tion (Fig. 4).
In the given series of experiments, use was made of
two frequencies separately in the range of effective
30
100
Surviving animals, %
40
50
60
70
80
90
20
10
0200 300 400 500
Amplitude, nT
Fig. 2.
Dependence of antitumor activity of weak com
bined collinear MFs (SMF 42
µ
T) on the amplitude of the
alternating component at modulating frequency 0.5 Hz
and carrier frequency 16.5 Hz. Animal survival was esti
mated 1 month after tumor inoculation. In the control, by
day 18 after inoculation all mice died.
744
BIOPHYSICS Vol. 54 No. 6 2009
NOVIKOV et al.
modulating frequencies (0.5 and 1 Hz) and the ampli
tude dependence of the effect at these frequencies was
checked. It was established that frequencies 0.5 and
1 Hz cause a pronounced effect at amplitudes in the
range 250–350 nT. A conclusion can be made that the
larger biological activity of the twofrequency signal is
conditioned by the sum effect of separate frequencies,
in the given case 16.5 Hz and 0.5 Hz (or 1 Hz).
Further we determined the amplitude dependence
of the antitumor effect at a frequency of 4.4 Hz (cyclo
tron frequency of the ionic form of glutamic acid at the
SMF value of 42
μ
T). This frequency was chosen on
the basis of the results of previous experiments, in
which pronounced antitumor activity of CMFs was
determined at cyclotron frequencies of the ionic forms
of amino acid molecules [7, 10]. In Fig. 5 one can see
that the maximal activity of ultraweak AMF at the
4.4 Hz frequency is noted at 100 nT.
In this way, we have determined the optimal ampli
tude ranges at various effective values of the frequen
cies of the ultraweak alternating component of CMF.
Thus in the case of 16.5 Hz the effective amplitudes are
concentrated in the range 150–300 nT; at 0.5 and 1 Hz
the maximum of the effect is noted at 300 nT; at a fre
quency of 4.4 Hz the greatest activity of MF action is
noted at 100 nT.
In the next series of experiments we checked the
biological activity of the summary multifrequency sig
nal including in itself all the three frequencies (1; 4.4;
16.5 Hz) at optimal values of amplitudes (300, 100,
150 nT respectively to frequencies) found by us earlier.
In Figs. 6 and 7 it is seen that the summary multi
frequency signal representing a sum of all effective fre
quencies with experimentally found effective ampli
tudes possesses the greatest antitumor activity as com
pared with the action of MF at separate frequencies at
these amplitudes.
Cytological analysis of the contents of the perito
neal cavity of tumorbearing animals has demon
strated the damaging action of MF on the EAT cells of
30
100
Surviving animals, %
40
50
60
20
10
0200 300 400 500
Amplitude, nT
Fig. 3.
Dependence of antitumor activity of weak com
bined collinear MFs (SMF 42
µ
T) on the amplitude of the
alternating component at the frequency 16.5 Hz. Other
conditions as in the caption to Fig. 2.
30
100
Surviving animals, %
40
50
20
10
0200 300 400 500
Amplitude, nT
12
Fig. 4.
Dependence of antitumor activity of weak com
bined collinear MFs (SMF 42
µ
T) on the amplitude of the
alternating component at frequencies:
1
– 0.5 and
2
– 1 Hz.
Other conditions as in the caption to Fig. 2.
30
100
Surviving animals, %
40
50
60
20
10
0150 200 250 300
Amplitude, nT
70
80
50
Fig. 5.
Dependence of antitumor activity of weak com
bined collinear MFs (SMF 42
µ
T) on the amplitude of the
alternating component at the frequency 4.4 Hz. Other
conditions as in the caption to Fig. 2.
2
Surviving animals, %
40
60
20
03 4
100
1
80
Fig. 6.
The amount of surviving animals (groups 1–4) in
one month of observation at various frequency–amplitude
parameters of the alternating component of MF (SMF
42
µ
T): (1) 1 Hz, 300 nT; (2) 4.4 Hz, 100 nT; (3) 16.5 Hz,
150 nT; (4) sum (1, 2, 3). Other conditions as in the caption
to Fig. 2.
BIOPHYSICS Vol. 54 No. 6 2009
EFFECT OF WEAK COMBINED MAGNETIC FIELDS ON ASCITES TUMOR 745
irradiated animals in contrast to the EAT cells of con
trol group animals (Fig. 8).
Figure 8 presents a large amount of tumor cells of
EAT of different stages of maturity, among them also
mitotic ones, which testifies to pronounced prolifera
tive activity of tumor cells. It should be noted that
among “healthy” tumor cells there is a very insignifi
cant amount (~5%) of degenerative forms. There also
are single lymphocytes, monocytes, neutrophils.
Figures 9 and 10 present tumor cells of experimen
tal EAT (after the action of weak MFs), among which
there is a large amount of degenerative cell forms. On
the basis of the results of cytological analysis it is estab
lished that the death of the cells of experimental EAT
is realized preferentially by the type of necrosis. Possi
bly this process is initiated at the expense of autolytic
enzymes (for example, release of enzymes from lysos
omes upon membrane damage), as a results of the
action of which the cell swells and is subject to lysis.
Probably, the action of MF with the indicated param
eters sharply activates the mechanism accelerating the
process of natural degeneration of tumor cells.
Upon quantitative analysis of the state of EAT
cells, differences are revealed between the types of
magnetic signal used (table). However, qualitative dif
ferences between cytological specimens in the experi
mental groups are absent, i.e. in all these cases we reg
ister just the necrotic death of tumor cells. The most
10
Surviving animals, %
40
60
20
015 20 25
Time, days
80
100
1
2
3
4
5
Fig. 7.
Lifetime of tumorbearing animals at different fre
quency–amplitude parameters of the alternating compo
nent of MF (SMF 42
µ
T):
1
, control;
2
, 1 Hz, 300 nT;
3
, 4.4 Hz, 100 nT;
4
, 16.5 Hz, 150 nT;
5
, sum (
2
,
3
,
4
). On
the abscissa axis, indicated are the terms of observation of
the number of animals in groups after tumor inoculation.
TC
DF
Fig. 8.
Control group. Specimen taken on the 10th day
after tumor injection. Magnification
×
500. TC, tumor cell
of EAT in the norm; DF, degenerative form of a tumor cell
of EAT.
Fig. 9.
Test group (SMF 42
µ
T; AMF 1 Hz, 300 nT; 4.4 Hz,
100 nT; 16.5 Hz, 150 nT). Specimen taken on the 10th day
after tumor injection. Magnification
×
200.
ON1
ON2
Fig. 10.
Test group (SMF 42
µ
T; AMF 1 Hz, 300 nT;
4.4 Hz, 100 nT; 16.5 Hz, 150 nT). Specimen taken on the
10th day after tumor injection. Magnification
×
500.
ON1—onset of necrosis of EAT tumor cell; ON2—pro
nounced necrosis of EAT tumor cell.
746
BIOPHYSICS Vol. 54 No. 6 2009
NOVIKOV et al.
pronounced necrosis in EAT cells is noted upon the
use of the summary multifrequency signal (sum of
effective frequencies at their effective amplitudes). It is
seen that the intensity of the necrotic process in EAT
cells directly correlates with the percentage of survival
of mice in groups (table; F igs. 6; 7). On this basis it can
be taken that cytological analysis of the contents of the
peritoneal cavity is an adequate express method of
estimating the state of tumorbearing animals.
In this way, as a result of the experiments conducted
we have determined the optimal or nearly optimal
parameters of ultralowfrequency (1; 4.4; 16.5 Hz or
sum of these frequencies) ultraweak (300; 100; 150–
300 nT respectively to frequencies) alternating com
ponent of CMFs that at the background of SMF of
42
μ
T (induction value corresponding to the geomag
netic range) possesses pronounced antitumor activity,
and also determined the preferential type of death of
tumor cells (necrosis) upon the action of these effec
tive MF parameters.
The primary target of the action of such fields has
not yet been experimentally established. This situation
is typical of magnetobiological investigations, because
the pathway of realization of a biological effect of a
weak field at the level of a whole organism is compli
cated and hardly yields to study. Earlier in experiments
with water solutions of amino acids [15–18] a change
has been shown in the current strength in solution
under the action of CMFs with AMF in the nanotesla
range. The frequency of the effective alternating field
corresponded in these works to the cyclotron fre
quency of the dissolved amino acid. On this basis it can
be suggested that the magnetic moments created by
ions can serve as primary targets of the external field.
In works [21, 22] a suggestion was made that the pri
mary target of a weak field may be the magnetic
moments of the nuclei of hydrogen atoms. The sugges
tion was tested by the authors of these works experi
mentally, with the use of regenerating planarians as a
test system. Amplified regeneration was shown at fre
quencies of the alternating component of the external
field corresponding to frequencies at which there was
a maximally intense presence of magnetic noise gener
ated by frequencymodulated precession of hydrogen
nuclear spins (calculated in the framework of the given
model). We have obtained experimental data only par
tially corresponding to these calculations. For exam
ple, for the frequency of 4.4 Hz the optimum of the
induction amplitude of the alternating MF compo
nent must constitute 93 nT [21, 22]. We have obtained
the maximal effect at ~100 nT. In this case it must be
taken into account that the value we give corresponds
to the “effective” value of amplitude of the alternating
component (measured with a magnetometer). In two
other cases at 1 Hz and 16.5 Hz we registered the val
ues of effective amplitudes not forecasted in works
[21, 22]. Thus for 1 Hz the value experimentally found
by us for the acting amplitude is more than an order of
magnitude higher than theoretically predicted. At
16.5 Hz the biological activity of MF does not notice
ably change in a broad range of amplitudes, 150–
300 nT. Apparently these data are indicative of the
presence in the real biological system of at least several
receptors for weak MF. It is also possible that the very
mechanism of realization of the biological effect of
these fields has certain frequency–amplitude charac
teristics.
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Dependence of the intensity of necrosis of EAT cells on the parameters of weak MFs
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1 Hz, 300 nT 8.6 ± 0.8* 15.6 ± 1.5* 36.4 ± 3.1* 72.2 ± 6.9*
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