Hindawi Publishing CorporationBioMed Research
InternationalVolume 2013, Article ID 602987, 12
pageshttp://dx.doi.org/10.1155/2013/602987Review ArticleBioeffects
of Static Magnetic Fields: Oxidative Stress, GenotoxicEffects, and
Cancer StudiesSoumaya Ghodbane, Aida Lahbib, Mohsen Sakly, and
Hafedh AbdelmelekUniversit e de Carthage, Laboratoire de
Physiologie Int egr ee, Facult e des Sciences de Bizerte, 7021
Jarzouna, TunisiaCorrespondence should be addressed to Soumaya
Ghodbane; [email protected] 24 April 2013; Revised 11
July 2013; Accepted 11 July 2013Academic Editor: Ali
KhraibiCopyright 2013 Soumaya Ghodbane et al. Tis is an open access
article distributed under the Creative Commons AttributionLicense,
which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properlycited.Te
interaction of static magnetic felds (SMFs) with living organisms
is a rapidly growing feld of investigation. Te magneticfelds (MFs)
efect observed with radical pair recombination is one of the
well-known mechanisms by which MFs interact withbiological systems.
Exposure to SMF can increase the activity, concentration, and life
time of paramagnetic free radicals, whichmight cause oxidative
stress, genetic mutation, and/or apoptosis. Current evidence
suggests that cell proliferation can be infuencedby a treatment
with both SMFs and anticancer drugs. It has been recently found
that SMFs can enhance the anticancer efect ofchemotherapeutic
drugs; this may provide a new strategy for cancer therapy. Tis
review focuses on our own data and other datafrom the literature of
SMFs bioefects. Tree main areas of investigation have been covered:
free radical generation and oxidativestress, apoptosis and
genotoxicity, and cancer. Afer an introduction on SMF classifcation
and medical applications, the basicphenomena to understand the
bioefects are described. Te scientifc literature is summarized,
integrated, and critically analyzedwith the help of authoritative
reviews by recognized experts; international safety guidelines are
also cited.1. IntroductionLiving organisms are continuously exposed
to the naturalgeomagnetic feld of around 2070 T that exists over
thesurface of the Earth and which is implicated inthe
orientationand migration of certain animal species
[1].Duringevolution, livingorganismsdevelopedspecifcmechanisms for
perception of natural electric and magneticfelds.Tese mechanisms
require specifc combinations ofphysical parameters of the applied
feld to be detected bybiological systems. In order words, the
windows are meansby which discrete MFs are detected by biological
systems.Dependingonthe level of structural
organizationthesemechanisms of detection and response may be seen
at difer-ent levels, for example, at membrane, cellular, or tissue
levels.Sometimes the windows function via signal
transductioncascade, brainactivity, orthecentral
nervoussystem[2].Tesensitivityofthebiological
systemstoweakMFhasbeendescribedelsewhere[35],
mainlyinrespecttothedependence of bioefects on the amplitude or the
frequencyof applied felds.Te frequency of exposure to MFs has
increased withrapid advances in science and technology, such as
magneticresonance imaging (MRI) diagnosis, nuclear magnetic
reso-nance (NMR) spectroscopy, and passenger transport systemsthat
are based on magnetic levitation [6]. Terefore, it hasbecome
necessary to systematically elucidate the infuenceof MFs on the
body. In an attempt to explain the biologicalefects of SMFs, it is
useful to classify them as weak (5 T).SMFs are time-independent
felds whose intensity couldbe spatially dependent. Tere are four
SMFparametersrelevant for the interaction with a biological system:
targettissue(s), magnet characteristics, magnet support device,
anddosingregimen[7]. SMFsaredifcult
toshieldandcanfreelypenetratebiological tissues[8]. However, not
onlythefeldintensity, but alsothegradient of thefeldhasimportant
roleinbiological efectsof SMF[9, 10].
SMFcaninteractdirectlywithmovingcharges(ions, proteins,etc.) and
magnetic materials found in tissues through severalphysical
mechanisms [6].2 BioMed Research InternationalPrevious research
showed that SMF infuences biologicalsystemin a way that causes
proinfammatory changes, as wellas an increase in production of
reactive oxygen species (ROS)[11, 12]. Troughout the past decades,
there have been severalexperimental results describing the efects
of MFs on radicalpair recombination.As reviewedrecently by Ueno
andShigemitsu[13], severalbiophysical and biochemical efects can be
expected whenbiological systems are simultaneously exposed to SMFs
andother forms of energy such as light and radiation [14,
15].Although there is much speculation about this role, theprimary
mechanism is thought to be the result of oxidativestress,that
is,free radical generation via Fenton reaction,which is the
iron-catalyzed oxidation of hydrogen peroxide(H2O2) [1618].Recent
advance of biological science and technology canhelp us understand
MF efects more clearly. Studies on thebiological efects of MFs have
resulted in signifcant develop-ments in the medical applications of
SMF as well as EMF, aferthe development of high-strength
superconducting magnets.Te mainstays of such medical applications
are transcranialmagnetic stimulation(TMS) and MRI. Tese techniques
havealsocontributedmuchtotheamazingprogressmadeinunderstanding
brain functions. A guideline for exposure ofthe human body to SMFs
set by the international commissionon nonionizing radiation
protection (ICNIRP) [19] suggests2 T as the ceiling value for body
parts, except for arms andlegs, in occupational exposure. In the
application of clinicalMRI, the current exposure level is
confrmedto be less thanorequal to 2 T. In SMFs at this strength it
is not feasible to obtainresonanceimages, except for hydrogenatoms.
Tereareseveral reports that strong SMF efects play signifcant
rolesin endogenous and exogenous ROS generations. Based onadvanced
studies of SMF efects on oxidative stress reactions,the potentially
hazardous efect of SMF on living organisms isthat exposure to SMF
can increase the activity, concentration,and life time of
paramagnetic free radicals, which might causeoxidativestress,
geneticmutation, and/or apoptosis [2023]. In particular, SMF
exposure initiates an iron-mediatedprocess that increases free
radical formation in brain cells,leading to the breaking of DNA
strands and cell death.Genotoxic efects of exposure to static
magnetic feldshavebeenmostlyexaminedincell cultures[24].
Fewinvivostudies of genotoxicityor possible efects
onothercarcinogenic processes have been carried out. Animal
studiesare ofen used in the evaluation of suspected human
car-cinogens [25] either screening for an increased incidence
ofspontaneous tumors or of the incidence of tumors induced byknown
carcinogens.Te earlier literature has been summarized by
WHO[26],Kowalczuk et al. [27] and ICNIRP [28, 29], Repacholi
andGreenebaum [30], IARC [31], ICNIRP [32], McKinlay et al.[33],
and Dini and Abbro [34] whilst more recent studies havebeen
reviewed by Okano [22], Phillips et al. [35], and Uenoand Okano
[36].Te focus of this review is on recent studies, where pos-sible.
Tese studies are covered under three main sections:free radical
generation and oxidative stress, apoptosis andgenotoxicity, and
cancer.Te objective of this review is to describe and shed lighton
some of the most recent information on the biologicalefects and
medical applications of magnetic felds. A dis-cussion of possible
implications of these efects on biologicalsystems is also
provided.2. Oxidative StressBiological free radicals are most
commonly oxygen ornitrogenbasedwithanunpairedelectron,
leadingtotheterms ROS, such as superoxide anion (O2), hydroxyl
radical(OH) and singlet oxygen (1O2), or reactive nitrogen
species(RNS), such as nitric oxide (NO) [37]. Te ROS and RNS
playsignifcant roles in immunological defense [38],
intracellularsignaling [39], and intercellular communication [40].
It isassumed that SMF could change the lifetime of radical
pairs,yields of cage products, and escape products. If anSMF
afectscells through the radical pair mechanism, an SMF
infuencesthespinof electronsinfreeradicals, whichmayleadtochanges
in chemical reaction kinetics and possibly alteringcellular
function [41].2.1. Moderate-Intensity Static Magnetic Fields and
OxidativeStress. Tere are several reports showing that moderate
SMFcould infuence the ROS modulation
(generation/reduction)fromenzymaticreactionsincell-freesolutions.
TeSMFefects alsoplaysignifcant roles intheendogenous andexogenous
ROS modulation in biological systems, in vitroand in vivo.Amara et
al. [42] investigated the efect of SMF
expo-sureontesticularfunctionandantioxidantstatusinrats.Exposure
toSMF(128 mT; 1 h/day for 30days) has noefect on epididymal sperm
count, spermatozoa motility, andgenital organ weight. In contrast,
SMF induces an increaseof malondialdehyde (MDA) inthe testis. Inthe
gonad,SMF decreases the catalase (CAT), glutathione
peroxidase(GPx), and mitochondrial Mn-superoxide dismutase
(Mn-SOD)activities. However,
cytosolicCuZn-SODactivityisunafected.Telatter
groupalsoinvestigatedtheefects of SMF(128 mT, 1 h/day during 30
consecutive days) exposure on theantioxidative enzymes activity and
MDA concentration inmale rat brain [43]. Te exposure of rats to SMF
decreasedthe GPx, CuZn-SOD, and CAT activities in frontal
cortex.Tesametreatment
decreasedtheCuZn-SODandMn-SODactivitiesinhippocampus. However,
theglutathionelevels remained unchanged in both brain structures.
In thehippocampus, SMF-exposure increased MDAconcentration.Tese
results indicated that exposure to SMF induced oxida-tive stress in
rat hippocampus and frontal cortex.SMF exposure alters antioxidant
enzyme activity and thelabile zinc fraction in THP1 cells (monocyte
line) [44]. Cellculture fasks were exposed to SMF (250 mT) during 1
h, 2 h,and3 h. Cell viabilitywasslightlylowerinSMF-exposedgroups
compared to a sham-exposed group. However, SMFexposure failed to
alter MDA, GPx, CAT, and SOD levelseven by 3 h of exposition.Cells
stained with zinc-specifcfuorescent probes zinpyr-1 showed a
decrease of labile zincBioMed Research International 3fractioninall
groups exposedto SMF. SMFexposure (250 mT,during 3 h) did not cause
oxidative stress in THP1 cells butaltered the intracellular labile
zinc fraction.Chateretal. [45]evaluatedtheefectsofexposuretoSMF on
some parameters indicative of oxidative stress inpregnant
rat.Exposure to SMF (128 mT;1 h/day from day6 to day 19 of
pregnancy) failed to alter plasma MDA andGPx activity. Moreover the
same treatment did not alter liverconcentration of MDAand kidney
activities of GPx CAT andSOD. By contrast, SMF induced an increase
of liver GSHcontent. Similar results were reported by Ghodbane et
al. [46]who show that liver GSH concentrations were
signifcantlyhigher in SMF exposed rats than in the controls,
indicatingan adaptive mechanism to electromagnetic pollution.
GSHlevels canbe increaseddue to anadaptive mechanismto
slightoxidative stress through an increase in its synthesis.
However,a severe oxidative stress may decrease GSH levels due to
theloss of adaptive mechanisms and the oxidation of GSH
toGSSG.Exposure to SMF (128 mT; 1 h/day for 5 days) induces
adecrease of selenium levels in kidney, muscle, and brain witha
decrease of GPx activities inkidney and muscle. By
contrast,SMFexposureincreasedtotal GSHlevelsandtotal SODactivities
in liver, while glutathione reductase (GR) activity isunafected.
Selenium supplementation (Na2SeO3, 0.2 mg/L,in drinking water for 4
weeks) in SMF-exposed rats restoredselenium levels in kidney,
muscle, and brain and elevated theactivities of GPx in kidney and
muscle to those of controlgroup. In the liver, selenium
supplementation failed to bringdown the elevated levels of total
GSH and SOD activities[46]. Tus, subacute exposure to SMF altered
the antioxidantresponse by decreasing tissues seleniumcontents,
whileselenium supplementation ameliorates antioxidant capacityinrat
exposedtoSMF. Regardingthe fate of seleniumadministration in
SMF-exposed rats, it may be assumed thatthis element minimizes the
oxidative stress induced by SMF.Previous data implicated the SMF in
free radical pro-duction, like superoxide anions in diferent cells
and organs[22, 47, 48]. However, Ghodbaneetal. [49]showedthatSMF
exposure failed to alter plasma TBARs and total thiolgroups,
indicating an adaptive mechanism to slight oxidativestress caused
by electromagnetic feld as previously shownby Chater et al. [45].
By contrast, Amara et al. [50] showedanincreaseinMDAlevel
inliverandkidney, indicatingoxidative stress under SMF (128 mT, 1
h/day during 30 con-secutive days).Tis discrepancy may be explained
by theintensity and the duration of the exposure. Te cellular
andmolecular modifcations induced when SMFs interact withbiological
materials are, however, dependent on the durationof exposure,
intensity, tissue penetration, and the type of cells[51].Moreover,
Ghodbane et al. [49] evaluated the efect ofselenium (Se)
supplementation in SMF-exposed rats.Pre-treatment with Se
(Na2SeO3,0.2 mg/L,for 30 consecutivedays, per os) preventedplasma
-tocopherol andretinoldecrease induced by SMF exposure.Amara et al.
[50] examined the efect of zinc supplemen-tation on the antioxidant
enzymatic system, lipid peroxida-tion and DNA oxidation in
SMF-exposed rats. Te exposureof rats to SMF (128 mT, 1 h/day during
30 consecutive days)decreasedtheactivitiesof GPx, CAT,
andSODactivitiesand increased MDA concentration in liver and
kidneys. Zincsupplementation (ZnCl2, 40 mg/L, per os) in
SMF-exposedrats restored the activities of GPx, CAT, and SOD in
liverto those of control group. However, only CAT activity
wasrestored in kidney. Moreover, zinc administration was able
tobring down the elevated levels of MDA in the liver but notin
kidneys. Te authors suggested that zinc supplementationminimizes
oxidative damage induced by SMF in rat tissues.Te mechanism by
which SMF induced oxidative stressin rat tissues is not well
understood. A change in radical pairrecombination rates is one of
the few mechanisms by whichan SMF can interact with biological
systems such as a cell-freesystem. Te SMF increases the
concentration and/or lifetimeof free radicals that escape from the
radical pair so that thecritical radical concentration, needed to
initiate membranedamage and cause cell lysis, is reached sooner
[22].ExposuretoSMF(128 mT, 1 h/day, during5consecu-tivedays)
inducedsympatheticneurons systemhyperac-tivity associated with
hypoxia-like status [52] and
elevatedplasmacorticosteroneandmetallothioneinconcentrationsand
enhanced apoptosis [53, 54]. Hashish et al. [8] indicatethat there
is a relation between the exposure to SMF and theoxidative stress
through distressing redox balance leading tophysiological
disturbances. SMF exposure induced probablythe disruption of
mineral divalent element homeostasis, con-tributing to their
defciency in tissues [43, 44, 46, 50]. Agayet al. [55] have
demonstrated that alteration of antioxidanttraceelements(Zn, Se,
andCu)disruptstheactivitiesofantioxidant enzymes. Dudaet al.
[56]reportedachangeinliverand kidneysconcentration ofcopper,
manganese,cobalt and iron in rats exposed to static and
low-frequencymagneticfelds. SMFprobablyinduces
aconformationalchangeofantioxidantenzymesthatleadstolossoftheircatalytic
activity [56].A few studies concerning the supplemental
antioxidantsvitamins Cand E have focused on the preventive and
curativeproperties in damage induced by SMF exposure [57]. Jajteet
al. [58] reported the efect of melatonin and vitamin Eon the level
of lipid peroxidation in rat blood lymphocytesexposed to iron ions
and/or SMF. When cells were treatedwith melatonin or vitamin E and
then exposed to iron ionsandSMF, thelevel
oflipidperoxidationwassignifcantlyreduced.Sullivanet al. [59]
reportedthat SMF(230250 mT)exposure stimulates ROS
productioninhumanfetal lung cells(WI-38) during the frst 18 h
period when cells are attachingto the culture vessel. Tese results
support the hypothesisthat increased ROS formation may account for
SMF efectson cell attachment. However, SMF decreases growth in
cellwhen the increase in ROS was abated, suggesting that
othermechanisms account for SMF efects on cell growth.Kabuto et al.
[60] showed that an SMF (5300 mT for40
min)hadnoefectontheaccumulationofTBARSinmousebrainhomogenatesinducedbyFeCl3.
Incontrast,whenthehomogenateswereincubatedwithFeCl3inanSMF (24 mT),
the accumulation of TBARS was decreased.Te accumulation of TBARS in
phosphatidylcholine solution4 BioMed Research
InternationalincubatedwithFeCl3andH2O2 was alsoinhibitedby the
SMFexposure. Tese results suggest that the SMF could have
aninhibitory efect on Fe2+-induced lipid peroxidation, and
theefectiveness of this SMF suppression on Fe2+-induced
ROSgeneration is restricted to a window of feld intensity of 2 to4
mT.Currently, environmental and industrial pollution causesmultiple
stress conditions; the combined exposure to mag-netic feld and
other toxic agents is recognized as an impor-tant research area,
with a view to better protecting humanhealthagainst their probable
unfavorable efects. Amaraet al. [61] investigated the efect of
coexposure to SMF andcadmium(Cd) ontheantioxidant enzymes
activityandMDAconcentrationinrat skeletal andcardiac
muscles.Teexposureof rats toSMF(128 mT, 1 h/dayduring30consecutive
days) decreased the activities of GPx and CuZn-SOD in heart muscle.
Exposure to SMF increased the MDAconcentrationinratcardiacmuscle.
Tecombinedefectof SMF and Cd (CdCl2,40 mg/L,per os) disrupted
morethe antioxidant enzymes activity in rat skeletal and
cardiacmuscles.Te combined efect of SMF (128 mT, 1 hour/day for
30consecutivedays)andCdCl2(40 mg/L, peros)decreasedSODactivity
andglutathione level andincreasedMDAconcentrationinfrontal cortex
as comparedwithCd-exposedrats [62].In pregnant rats coexposed to
cadmium (CdCl2,3.0 mg/Kgbodyweight)andSMF(128 mT/1
h/day)for13consecutive days as from the 6th to 19th day of
gestation,no efects on activities of antioxidant were observed in
bothtissues compared to cadmium-treated group [63]. However,the
associationbetweenSMFandCddecreasedplasmaMDA concentration,
suggesting that a homeostatic defensemechanism was activated when
SMF was associated to Cd inpregnant rats.2.2. Strong and
Ultrastrong Static Magnetic Fields and Oxida-tive Stress. Although
strong SMF is supposed to have thepotential to afect biological
systems, the efects have not beenevaluated sufciently.Sirmatel
etal. [64]investigatedtheefectsof ahigh-strength magnetic feld
produced by an MRI apparatus onoxidativestress. Teefectsof SMF(1.50
T) onthetotalantioxidant capacity (TAC), total oxidant status
(TOS), andoxidativestressindex(OSI)inmalesubjectswereinves-tigated.
In this study, 33 male volunteers were exposed toSMFfor ashort
time, andthe TAC, TOS, andOSI
ofeachsubjectweredeterminedusingthemethodsofErel.Magneticfeldexposurewas
providedusingamagneticresonance apparatus; radiofrequency was not
applied. TACshowed a signifcant increase in postexposures compared
topreexposures to the magnetic feld ( < 0.05). OSI and TOSshowed
a signifcant decrease in postexposures compared topreexposures to
SMF (for each of two, < 0.01). Te 1.50 TSMF used in the MRI
apparatus did not yield a negative efect;on the contrary, it
produced the positive efect of decreasingoxidative stress in men
following short-term exposure.TeNakagawaresearchgroup[65,
66]measuredandevaluated a ROS scavenger,metallothionein (MT),a
ROSproduct, and lipid peroxidation in the liver, kidneys,
heart,lung, and brain of 8-week-old male BALB/c mice in vivo.
Temice were exposed to an SMF of 3.0 and 4.70 T for 148 h. A4.70 T
SMF exposure for 648 h increased both MT and lipidperoxidation
levels in the liver alone. A 3.0 T SMF exposurefor 148 h did not
induce any changes in both MT and lipidperoxidation levels in all
the tissues. A single subcutaneousinjection of CCl4 (0.5 mL/kg)
increased both MT and lipidperoxidationlevels intheliver,
andthecombinationofCCl4 administration and a 4.70 T SMF for 24 h
potentiatedbothMTandlipidperoxidationlevels. Te increase
inactivities of both glutamic-oxaloacetic transaminase (GOT)and
glutamic-pyruvic transaminase (GPT) caused by CCl4administration
was also enhanced by the SMF exposure. It isconcluded that exposure
to a high SMF induces the increaseof both MT and lipid peroxidation
levels in the liver of miceand enhances the hepatotoxicity caused
by CCl4 injection.3. Genotoxicity, DNA Damage, and ApoptosisHealth
and environmental concerns have been raised becausethe SMF efects
on oxidative stress leading to genetic muta-tion and
apoptosis/necrosis have been found. It seems to takeplace from free
radical generation.Several experiments have beenshown, and they
discussedhow SMF can infuence the immune function or oxidativeDNA
damage via the ROS formation process.One possibility is that DNA is
damaged by free radicalsthat are formed inside cells. Free radicals
afect cells by dam-aging macromolecules, such as DNA, protein, and
membranelipids. Several reports have indicated that SMF enhances
freeradical activity in cells [6771], particularly via the
Fentonreaction [70]. Te Fenton reaction is a process catalyzed
byironinwhichhydrogenperoxide, aproduct of oxidativerespiration in
the mitochondria, is converted into hydroxylfree radicals, which
are very potent and cytotoxic molecules.3.1.Genotoxic Efects of
Moderate-Intensity Static MagneticFields. Amaraet al. [44]
investigatedthe efect of SMFexposure in DNA damage in THP1 cells
(monocyte line).Cell culture fasks were exposed to SMF (250 mT)
during1 h, 2 h, and 3 h. Te results showed that cell viability
wasslightly lower in SMF-exposed groups compared to a
sham-exposedgroup. DNAanalysis by single cell gel
electrophoresis(comet assay) revealed that SMF exposure did not
exert anyDNA damage by 1 and 2 h. However, it induced a low levelof
DNA single strand breaks in cells afer 3 h of exposition.To further
explore the oxidative DNA damage, cellular DNAwas
isolated,hydrolyzed,and analyzed by HPLC-EC.Televel of
8-oxo-7,8-dihydro-2
-deoxyguanosine (8-oxodGuo)remained unchanged compared to the
sham-exposed group(+6.5%, > 0.05). Te results showed that SMF
exposure(250 mT, during 3 h) did not cause oxidative stress and
DNAdamage in THP1 cells.Exposure of rats toSMF(128 mT, 1
h/dayduring30consecutive days) increased metallothioneins level in
frontalcortex, while the 8-oxodGuo concentration remained
unaf-fected, indicating the absence of DNA oxidation.
Metalloth-ionein induction protected probably DNA against
oxidativeBioMed Research International 5damage [43]. Te same
treatment elevated the 8-oxodGuoin kidneys but not in liver. Zinc
supplementation (ZnCl2,40 mg/L, per os) attenuated DNA oxidation
induced by SMFin kidneys to the control level
[50].Simultaneousexposureof rat lymphocytestoa7 mTSMF and ferrous
chloride (FeCl2) caused an increase in thenumber of cells with
DNAdamage [72, 73]. No signifcant dif-ferences were observed
between unexposed lymphocytes andlymphocytes exposed to a 7 mT SMF
or FeCl2 (10 mg/mL).However, when lymphocytes were exposed to a 7
mT staticmagnetic feld and simultaneously treated with FeCl2,
therewas a signifcant increase in the percentage of apoptotic
andnecrotic cells accompanied by signifcant alterations in
cellviability.However, anincreasingnumberof evidenceindicatesthat
SMFs are capable of altering apoptosis, mainly throughmodulationof
Ca2+infux. Tenuzzoet al. [74] observedthat exposure to a 6-mT SMF
afects the apoptotic rate inisolated human lymphocytes, the
expression and distributionof pro- and antiapoptotic genes, and the
concentration ofintracellular Ca2+. Tey also suggest that
modulation of theapoptotic rate is not a consequence of the direct
physicalinteraction between the feld and the apoptotic inducers
butthe fnal result of multiple perturbations of
Ca2+-regulatedactivity and gene-related transcription factors and
membranecomponents, which collectively afect the apoptotic
response.SMFs above 600 mT were found to decrease the extent ofcell
death by apoptosis induced by several agents in diferenthuman cell
systems of U937 and CEM cells in an intensity-dependent fashion,
reachingaplateauat 6 mT[75]. Teprotective efect was found to be
mediated by the ability of thefelds to enhance Ca2+ infux from the
extracellular medium;accordingly, it was limited to those cell
systems where Ca2+infux was shown to have an antiapoptotic efect.
In additionto the SMF-enhancing efect on [Ca2+]i, as a mechanism
ofthe rescue of damaged cells, it was recently proposed
thatSMF-produced redox alterations may be part of the
signalingpathway leading to apoptosis antagonism [76].Flipo et al.
[77] examined the in vitro efects of SMFson the cellular immune
parameters of the C57BI/6 murinemacrophages, spleen lymphocytes,
and thymic cells. Te cellswereexposedinvitrofor24 hat 37C, 5%CO2,
to25150 mT SMF. Exposure to the SMF resulted in the
decreasedphagocytic uptake of fuorescent latex microspheres,
whichwasaccompaniedbyanincreasedintracellularCa2+levelinmacrophages.
Exposure toSMFdecreasedmitogenicresponses in lymphocytes, as
determined by incorporationof [3H] thymidine into the cells. Tis
was associated withthe increased Ca2+ infux in concanavalin
A-stimulated lym-phocytes. Furthermore, exposure to SMF produced
markedlyincreased apoptosis of thymic cells, as determined by
fowcytometry. Overall, in vitro exposure of immunocompetentcells to
25150 mT SMF altered several functional parametersof
C57BI/6murinemacrophages, thymocytes, andspleenlymphocytes
[77].Apoptosis induced by magnetic feld in female rats
wasinvestigatedby using the Tdt mediateddUTPnick-endlabeling
(TUNEL) assay in thymus, liver, and kidneys [54].Following subacute
exposure to SMF, morphological exami-nations revealed numerous
apoptotic cells in thymus charac-terized by nuclear chromatin
condensation and fragmenta-tion.
Tedensityoftheapoptoticcellswassignifcantincortical zone,
thaninthemedullarzone. Bycontrast,nolabelingwas foundinliver
andkidneys followingSMF-exposure. Tus, it maybeconcludedthat
SMFinducedapoptosis inthymic cell death but not inthe liver and
kidneys.Although the mechanisms by which SMF initiates apoptosisin
thymocytes are presently not known, and reactive oxygenspecies are
likely to play a role.Ishisakaetal.
[78]investigatedtheefectsofanSMF(25 mT for 1 h) on the apoptosis of
human leukemic cell line(HL-60) induced by exogenous H2O2. Te H2O2
induced arapid DNA fragmentation and a slow decrease in viability
ofHL-60 cells. However, the SMF itself (6 mT for 18 h) did notexert
any efect on the H2O2-induced DNA fragmentation orviability.HL-60
cells were exposed to SMF of 6 mTwith or withoutDNA topoisomerase I
inhibitor, camptothecin for 5 h. SMFalone did not produce any
apoptogenic or neurogenic efectin HL-60 cells [79]. SMFs alone or
in combination with cam-ptothecin did not afect overall cell
viability, but they accel-erated the rate of cell transition from
apoptosis to secondarynecrosis afer induction of apoptosis by
camptothecin.In addition, Teodori et al. [80, 81] reported that a
uniformSMF(6 mTfor18 h; 8and30 mTfor3 h)didnot afectviability of
human glioblastoma cells. However, a uniformSMF of 300 mT for 3 h
increased apoptosis. Te interferenceof the SMF (6 mT for 18 h) with
physical(heat shock) orchemical (etoposide, VP16) induced apoptosis
may be relatedto oxidative stress.Potenza et al. [82] describedthe
efects of SMFoncell growthandDNAintegrityof humanumbilical
veinendothelial cells (HUVECs). Te authors investigated thata 4 h
exposure of HUVECs to SMFs of moderate intensity(300 mT) induced a
transient DNA damage both at the nu-clear and mitochondrial levels.
Tis response was par-alleledby increased mitochondrial DNA content
and mitochondrialactivity and by a higher expression of some genes
related tomitochondrial biogenesis 24 h afer SMF exposure.Hao et
al. [83] investigated whether SMFs (8.8 mT, for12 h) can enhance
the killing efect of adriamycin (ADM)in human leukemia cells
(K562). Te authors showed thatSMF exposure enhanced the
cytotoxicity potency of ADMonK562 cells and suggested that the
decrease in P-glycoproteinexpression may be one reason underlying
this efect.Sarvestani et al. [84] evaluated the infuence of an
SMF(15 mT, for 5 h) on the progression of cell cycle in rat
BMSCs.Tecellsweredividedintotwogroups. Onegroupwasexposed to SMF
alone, whereas the other group was exposedto X-rays before SMF
exposure. Te population of cells didnot show any signifcant
diference in the frst
group,butthesecondgroupexposedtoacuteradiationbeforeSMFexposure
showed a signifcant increase in the number of cellsin the G2/M
phase. Te SMF intensifed the efects of X-rayexposure, whereas SMF
alone did not have any detectableinfuence on cell cycle.6 BioMed
Research International3.2. Genotoxic Efects of Strong and
Ultrastrong Static MagneticFields. It is generally accepted that
static felds below 1 T arenot genotoxic [32, 33, 85]. However, a
recent study by Suzukiet al. [86] reported a signifcant, time- and
dose-dependentincrease in micronucleus frequency in mice exposed to
staticmagnetic felds of 2,3,or 4.7 T for 24,48,or 72 h,usinga
standard micronucleus assay. Bone marrow smears
weretakenimmediatelyafer exposure, andthe frequencyofmicronucleated
polychromatic (immature) erythrocytes wasscored. Micronucleus
frequency was signifcantly increasedfollowing exposure to 4.7 T for
all three time periods and to3 T afer exposure for 48 or 72 h,
whereas exposure to 2 Thad no signifcant efect. Te authors suggest
that exposure tohigher felds may have induced a stress reaction or
directlyafectedchromosomestructureor
separationduringcelldivision.Te clinical and preclinical uses of
high-feld intensity(HF, 3 Tandabove)
magneticresonanceimaging(MRI)scanners have signifcantly increased
in the past few years.However, potential health risks are implied
in the MRI andespecially HF MRI environment due to high-static
magneticfelds, fast gradient magneticfelds,
andstrongradiofre-quencyelectromagneticfelds. Tegenotoxicpotential
of3 T clinical MRI scans in cultured human lymphocytes invitro was
investigated by analyzing chromosome aberrations(CA), micronuclei
(MN), and single-cell gel electrophoresis[87]. Human lymphocytes
were exposed to electromagneticfelds generated during MRI scanning
(clinical routine brainexamination protocols: three-channel head
coil) for 22, 45,67, and 89 min. A signifcant increase in the
frequency ofsingle-strand DNA breaks following exposure to a 3 T
MRIwas observed. In addition, the frequency of both CAs andMN in
exposed cells increased in a time-dependent manner.Te frequencies
of MN in lymphocytes exposed to complexelectromagneticfeldsfor0,
22, 45, 67, and89 minwere9.67, 11.67, 14.67, 18.00, and 20.33 per
1000 cells, respectively.Similarly, the frequencies of CAs in
lymphocytes exposed for0, 45, 67, and 89 min were 1.33, 2.33, 3.67,
and 4.67 per 200cells, respectively. Tese results suggest that
exposure to 3 TMRI induces genotoxic efects in human
lymphocytes.Schreiber et al. [88] reported no mutagenic and
comuta-genic efects of magnetic felds used for MRI.Schwenzer et al.
[89] evaluated the efects of the staticmagneticfeldandtypical
imagingsequencesof ahigh-feld magnetic resonance scanner (3 T) on
the induction ofdouble strandbreaks (DSBs) intwo diferent humancell
lines.Human promyelocytic leukemia cells (HL-60) and humanacute
myeloid leukemia cells (KG-1a) were exposed to
theSMFaloneandtoturbospin-echo(TSE) andgradient-echo(GE)sequences.
Flowcytometrywasusedtoquan-tify gammaH2AX expression of
antibody-stained cells as
amarkerfordeoxyribonucleicacidDSBsonehourand24hours afer magnetic
feld exposure. X-ray-treated cells wereused as positive control.
Neither exposure to the SMF
alonenortotheappliedimagingsequencesshowedsignifcantdiferences in
gammaH2AXexpression between exposed andsham-exposed
cells.X-ray-treated cells as positive controlshowed a signifcant
increase in gammaH2AX expression.SMF alone and MRI sequences at 3 T
have no efect on theinduction of DSBs in HL-60 and KG-1a cells.Te
efects of SMF (4.70 T) on the frequency of micronu-cleatedcells
inCHL/IUcells inducedby mitomycinC(MMC) were studied in vitro [90].
Te cells were simulta-neously exposed to SMF and MMC for 6 h, and
then thecells were cultured in normal condition for the
micronucleusexpression up to 66 h. Exposure to SMF for 6 h
signifcantlydecreased the frequency of MMC-induced
micronucleatedcell expression afer culture periods of 18, 42, 54,
and 66 h.Tese results suggested that SMF (4.70 T) might have
exertedan infuence on the DNA damage stage produced by MMCrather
than on the formation of micronuclei during the stagefollowing
MMC-induced DNA damage.Kimura et al. [91] examined the efect of 3
or 5 T SMFongeneexpressionintheexperimental model
metazoanCaenorhabditis elegans. In addition, transient induction
ofhps12 family genes was observed afer SMF exposure. Tesmall-hps
gene, hps16, was alsoinducedbut toamuchlesser extent, and the
lacZ-stained population of hps16-1::lacZtransgenic worms did not
signifcantly increase afer SMFexposure with or without a second
stressor, mild heat shock.Several genes encoding apoptotic cell
death activators andsecretedsurfaceproteins wereupregulatedafer
ionizingradiation (IR), but they were not induced by SMF. Te RT-PCR
analyses for 12 of these genes confrmed the expres-sion diferences
between worms exposed to SMF and thoseexposedto IR. Incontrast to
IR, exposure to high SMFsdidnot induceDNAdouble-strandbreaks or
germlinecell apoptosis during meiosis. Tese results suggest that
theresponse of C. elegans to high SMFs is unique and capable
ofadjustment during long exposure and that this treatment maybe
less hazardous than other invasive treatments and drugs.Koanaetal.
[92]examinedthegenotoxicefectsofa5 T SMF for 24 h in a DNA-repair
defective mutant of D.melanogaster using the somatic mutation and
recombinationtest (SMART) [93] because this test was useful to
detect themutagenic activity of SMF and EMF. Tey reported that
theSMF exposure increased the frequency of mutation in
mei-41heterozygotes and that the increase was suppressed to
controllevels by supplementation with vitamin E, which is a
lipid-soluble antioxidant and a nonspecifc radical scavenger.An
Escherichia coli (E. coli) mutation assay was used toassess the
mutagenic efects of strong static magnetic felds[21]. Various
mutant strains of E. coli were exposed up to 9 Tfor 24 h, and the
frequencies of rifampicin-resistant muta-tions were then
determined. Te expression of the soxS::lacZfusion gene was assessed
by measuring b-galactosidase activ-ity. Te results for survival or
mutation obtained with thewild-type E. coli strain GC4468 and its
derivatives defectivein DNArepair enzymes or redox-regulating
enzymes showednoefect of exposure. Ontheotherhand,
themutationfrequency was signifcantly increased by exposure to SMF
of9 T in soxR and sodAsodB mutants, which are defective indefense
mechanisms against oxidative stress.Ikehataet al. [94]
examinedpossiblemutagenicandcomutagenicefectsof
strongstaticmagneticfeldsusingthe bacterial mutagenicity test. No
mutagenic efect of SMFsupto5 Twas detectedusingfour strains of
SalmonellaBioMed Research International 7typhimuriumandE. coli
WP2uvrA. Te mutationratein the exposed group was signifcantly
higher than inthenonexposedgroupwhencells
weretreatedwithN-ethyl-N0-nitro-N-nitrosoguanidine,
N-methyl-N0-nitro-N-nitrosoguanidine, ethylmethanesulfonate,
4-nitroquinoline-N-oxide,
2-amino-3-methyl-3H-imidazo[4,5-f]quinolone, or2-(2-furyl)-
3-(5-nitro-2-furyl) acrylamide.Long-term exposure to a 10 T SMF for
up to 4 days didnot afect cell growth rate or cell cycle
distribution in Chinesehamster ovary CHO-K1 cells [95]. Exposure to
SMF alonedid not afect micronucleus formation. In X-ray
irradiatedcells, exposure to a 1 T SMF also did not afect
micronucleusformation, but exposure to a 10 TSMF resulted ina
signifcantincreaseinmicronucleusformationinducedafera4 Gyexposure.
One of the mechanisms of this efect is attributableto the 10 T
SMF-induced oxidative DNA damage.4. Cancer StudiesMany researchers
have observed the efects of SMFs on tumorcells, particularly the
inhibiting efects. Tey have used SMFas an entry point for
investigating biological efects. In
ordertoreducethetoxicityandresistanceof singleanticancerdrugs,
avarietyofunifedtreatmentswererequired. Tesynergy of magnetic felds
and anticancer drugs was one ofthe methods that provides a new
strategy for the efectivetreatment of cancer.4.1.
Moderate-IntensityStaticMagneticFields andCancer.Gray et al. [71]
evaluated the efects of non-uniform 110 mTSMF for four 4 h periods,
with 812 h between each exposure,anddoxorubicin(10 mg/kg,
i.p.)onfemaleB6C3F1 micewith transplanted mammary adenocarcinoma.
Teir
resultsrevealedthatthegroupsexposedtoSMFcombinedwithdoxorubicin
achieved signifcantly greater tumor regressionthanthe
grouptreatedwithadriamycin(ADM) alone. Inaninvivo experiment, mice
bearing murine Lewis lung carcinomas(LLCs) weretreatedwith3
mTSMFfor 35 min/dayandcisplatin(3 mg/kg, i.p.) [96]. Te survival
time of micetreated with cisplatin and SMF was signifcantly longer
thanthat of mice treated only with cisplatin or SMF exposure.Tese
results show that SMF can inhibit the proliferation ofcancer cells,
and the killing efects of SMF combined withantineoplastic drugs on
cancer cells are greater than those ofSMFs or anticancer drugs
alone. Tese observations suggest apotential strategy for
chemotherapy, that is, the combinationtherapyof SMFs
andchemotherapeuticdrugs. However,so far it remains unclear which
mechanism underlies thekilling efects of SMFs combined with
chemotherapy drugson cancer cells.Sun et al. [97] evaluated the
ability of 8.8 mT SMFs toenhancetheinvitroactionof
achemotherapeuticagent,paclitaxel, against K562 human leukemia
cells. Te authorsanalyzed the cell proliferation, cell cycle
distribution, DNAdamage, andalterationof cell surfaceandcell
organelleultrastructureaferK562cellswereexposedtopaclitaxelinthe
presence or absence of SMF. the results showedthat, in the presence
of SMF, the efcient concentration ofpaclitaxel on K562 cells was
decreased from 50 to 10 ng/mL.Cell cycleanalysisindicatedthat
K562cellstreatedwithSMF plus paclitaxel were arrested at the G2
phase, whichwas mainly induced by paclitaxel. Trough comet assay,
theauthors found that the cell cycle arrest efect of paclitaxelwith
or without SMF on K562 cells was correlated with DNAdamage. Te
results of atomic force microscopy and trans-mission electron
microscopy observation showed that thecell ultrastructure was
altered in the group treated with thecombination of SMF and
paclitaxel, holes and protuberanceswere observed, and vacuoles in
cytoplasm were augmented.Te authors indicated that the potency of
the combination ofSMF and paclitaxel was greater than that of SMF
or paclitaxelalone on K562 cells, and these efects were correlated
withDNAdamageinducedbySMFandpaclitaxel. Terefore,thealteration
ofcell membrane
permeabilitymaybeoneimportantmechanismunderlyingtheefectsof
SMFandpaclitaxel on K562 cells.Strieth et al. [98] analyzed the
efects of SMF (587 mT)on tumor microcirculation. In vivo
fuorescence microscopywas performed in A-Mel-3 tumors growing in
dorsal skinfoldchamber preparations of hamsters. Short time
exposuretoSMF(150 mT) resultedinasignifcant
reductionofcapillaryredbloodcellsvelocities(vRBC)andsegmentalblood
fow in tumor microvessels. At the maximum strengthof 587 mT,
areversiblereductionof vRBC(40%)andoffunctional vessel densities
(FVD) (15%) was observed. Pro-longation of the exposure time (1
minute to 3 h) resulted inreductions. Microvessel diameters and
leukocyte-endothelialcell interactions
remainedunafectedbySMFexposures.However, in contrast to tumor-free
striated muscle controls,exposure at the maximum fux density of 587
mT induced asignifcant increase in platelet-endothelial cell
adherence ina time-dependent manner that was reversible afer
reducingthestrengthoftheSMF. Teauthorsassumedthatthesereversible
changes may have implications for functionalmeasurements of tumor
microcirculation by MRI and newtherapeutic strategies using strong
SMFs. Te same researchgroupfurther evaluatedthe efects of anSMF(586
mT, for 3 h)on tumor angiogenesis and growth [99]. Analysis of
micro-circulatoryparametersrevealedasignifcant reductionofFVD,
vessel diameters, and RBCvelocity in tumors afer SMFexposure
compared with the control tumors. Tese changesrefect retarded
vessel maturation by antiangiogenesis. Teincreased edema afer
SMF-exposure indicated an increasedtumor microvessel leakiness
possibly enhancing drug uptake.Te authors concluded that SMF
therapy appears to be apromising new anticancer strategy, as an
inhibitor of tumorgrowthandangiogenesisandasapotential
sensitizertochemotherapy.Chen et al. [100] investigated whether 8.8
mT SMFs canenhance the killing potency of cisplatin (DDP) on
humanleukemic cells (K562). Te results show that SMFs enhancedthe
anticancer efect of DDP on K562 cells. Te
mechanismcorrelatedwiththeDNAdamagemodel. Tisstudyalsoshows the
potentiality of SMFs as an adjunctive treatmentmethod for
chemotherapy.Hao et al. [83] investigated whether a
moderate-intensitySMF can enhance the killing efect of ADM on K562
cells8 BioMed Research Internationalandexploretheefectsof
SMFcombinedwithADMonK562 cells. Te authors analyzed the metabolic
activity ofcells, cell cycledistribution, DNAdamage,
changeincellultrastructure, andP-glycoprotein(P-gp)
expressionaferK562 cells were exposed continuously to a uniform 8.8
mTSMF for 12 h, with or without ADM. Teir results showedthat the
SMF combined with ADM (25 ng/mL) signifcantlyinhibited the
metabolic activity of K562 cells, while neitherADM nor the SMF
alone afected the metabolic activity ofthese cells. Cell
ultrastructure was altered in the SMF +ADMgroup. Forexample, cell
membranewasdepressed, someprotuberances wereobservable, and
vacuolesinthe cyto-plasm became larger. Cells were arrested at the
G2/M phaseandDNAdamageincreasedafercellsweretreatedwiththe SMF
+ADM. ADM also induced the P-gp expression. Incontrast, in the SMF
group and SMF +ADM group, the P-gpexpression was decreased compared
with the ADM group.Taken together, these results showed that the
8.8 mT SMFenhanced the cytotoxicity potency of ADMonK562 cells,
andthe decrease inP-gpexpressionmay be one reasonunderlyingthis
efect.Cells were treated with four anticancer drugs followed
bytreatment with a combination of drugs and SMF [101]. Indi-vidual
cells were examined using atomic force microscopy(AFM). Te drugs
were taxol (alkaloid), doxorubicin(anthra-cycline),
cisplatin(platinumcompound), andcyclophos-phamide(alkylatingagent).
Holeswereobservedincellsexposed to SMF but not in control groups.
Te number, size,and shape of the holes were dependent on the drug
type,SMF parameters, and the duration of exposure. Te
resultssuggest that the application of a SMF could alter
membranepermeability, increasing the fowof the anticancer drugs.
Tismay be one of the reasons why SMF can strength then theefect of
anticancer drugs. Observations were also made ofthe efect of using
diferent anticancer drugs. For example,the efect of SMF combined
with taxol or cyclophosphamideon the cells was additive while the
efect of SMF combinedwith cisplatin or doxorubicin was synergistic.
Te target sitesof cisplatinanddoxorubicinarenucleicacids;
continousresearch is required into this important area to ascertain
theefect of SMF on nucleic acids.4.2. Strong and Ultrastrong Static
Magnetic Fields and Cancer.Recently, some studies have suggested
that SMFs have thepotential as an adjunctive treatment method for
chemother-apy, sinceSMFs infuencecell growth, proliferation,
andstructureof cancer cells [98, 99, 102107].
Inparticular,thekillingefect of antineoplasticdrugs oncancer
cellsis enhanced with a combined treatment of SMFs
andchemotherapeutic drugs, indicating that SMFs act synergi-cally
with the pharmacological treatment [71, 96, 108]. Forexample, 64 h
exposure to a 7 T uniform SMF produced areduction in viable cell
number in HTB 63 (melanoma), HTB77 IP3 (ovarian carcinoma), and CCL
86 (lymphoma, Rajicells) cell lines [102].Ghibelli et al. [109]
examined whether exposure to theSMF of NMR(1 T) generated by an
NMRapparatus can
afectapoptosisinducedonreportertumorcellsofhematopoi-eticorigin.
Teimpressiveresultwasthestrongincrease(by 1.82.5-fold) of
damage-induced apoptosis by NMR. Tispotentiationis
duetocytosolicCa2+overloadtoNMR-promoted Ca2+ infux, since it is
prevented by intracellular(BAPTA-AM) and extracellular (EGTA) Ca2+
chelation or byinhibition of plasma membrane L-type Ca2+ channels.
A 3-day followup of treated cultures showed that NMR
decreaseslong-termcell survival, thus increasingthe
efciencyofcytocidal treatments. Mononuclear white blood cells are
notsensitized to apoptosis by NMR,showing that NMR mayincrease the
diferential cytotoxicity of antitumor drugs ontumor versus normal
cells. Te authors suggested that thisstrong, diferential
potentiatingefect of NMRontumorcell apoptosis may have important
implications, as in fact apossible adjuvant for antitumor
therapies.5. Summary and ConclusionsInrecentyears,
anabundanceofresearchpapers, reviewpapers, and books has been
published describing the possiblephysical and biological
interactions of magnetic felds.Considering these articles
comprehensively, the con-clusionsareasfollows: theprimarycauseof
changesincells afer incubation in external SMF is disruption of
freeradical metabolismand elevationof their concentration.
Suchdisruption causes oxidative stress and, as a result,
damagesionchannels, leadingtochangesincell morphologyandexpression
of diferent genes and proteins and also changesin apoptosis and
proliferation. Moreover, based on availabledata, it was concluded
that exposure to SMFs alone has noor extremely small efects on cell
growth and genetic toxicityregardless of the magnetic density.
However, in combinationwith other external factors such as ionizing
radiation andsome chemicals such as cadmium, there is evidence
stronglysuggestingthat anSMFmodifes their efects. Efects ofSMFs on
apoptosis are a potentially interesting phenomenon.However,these
efects ofen depended on a cell type andwere not found in various
types of cells. Many researchershave observed the efects of SMFs on
tumor cells, particularlytheinhibitingefects.
Inordertoreducethetoxicityandresistanceof singleanticancerdrugs,
avarietyof unifedtreatments were required. Te synergy of magnetic
felds andanticancer drugs was one of the methods. It provides a
newstrategy for the efective treatment of cancer.Tese studies
provide valuable insight intothe phe-nomenon of biomagnetism and
open new avenues for thedevelopment of newmedical applications.
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