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Author: Omer
C
elik Mehmet Cemal Kahya Mustafa
Nazroglu
PII:
DOI:
Reference:
S0891-0618(15)00074-5
http://dx.doi.org/doi:10.1016/j.jchemneu.2015.10.005
CHENEU 1344
To appear in:
Received date:
Revised date:
Accepted date:
22-9-2015
15-10-2015
16-10-2015
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Oxidative stress of brain and liver is increased by Wi-Fi (2.45 GHz) exposure of rats
during pregnancy and the development of newborns
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Department of Biophysics, Medicine Faculty, Izmir Katip Celebi University, Izmir, Turkey
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Corresponding authors
Assist. Prof. Dr. mer ELK
Department of Biophysics,
Medicine Faculty,
Sleyman Demirel University,
Isparta, Turkey
Omercelik.vm@gmail.com
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Abstract
An excessive production of reactive oxygen substances (ROS) and reduced antioxidant
defence systems resulting from electromagnetic radiation (EMR) exposure may lead to
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oxidative brain and liver damage and degradation of membranes during pregnancy and
development of rat pups. We aimed to investigate the effects of Wi-Fi-induced EMR on the
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brain and liver antioxidant redox systems in the rat during pregnancy and development.
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Sixteen pregnant rats and their 48 newborns were equally divided into control and
EMR groups. The EMR groups were exposed to 2.45 GHz EMR (1 hour/day for 5 days/week)
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from pregnancy to 3 weeks of age. Brain cortex and liver samples were taken from the
newborns between the first and third weeks. In the EMR groups, lipid peroxidation levels in
the brain and liver were increased following EMR exposure; however, the glutathione
peroxidase (GSH-Px) activity, and vitamin A, vitamin E and -carotene concentrations were
decreased in the brain and liver. Glutathione (GSH) and vitamin C concentrations in the brain
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were also lower in the EMR groups than in the controls; however, their concentrations did not
In conclusion, Wi-Fi-induced oxidative stress in the brain and liver of developing rats
was the result of reduced GSH-Px, GSH and antioxidant vitamin concentrations. Moreover,
the brain seemed to be more sensitive to oxidative injury compared to the liver in the
development of newborns.
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Introduction
There is currently a widespread use of wireless local area network (WLAN) systems (2.45
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GHz) being used as an alternative to wired internet access in many areas including
universities, schools, homes and public areas (Nazrolu et al. 2013; Dasdag et al. 2015).
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Several studies have suggested that biological systems might be sensitive to such forms of
radiation (Otto and von Mhlendahl, 2007; Takahashi et al. 2010; etin et al. 2014; Dasdag et
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al. 2015). Results of epidemiological (McBride et al. 1999; Burch et al. 2002) and
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experimental (Tomruk et al. 2010; zorak et al. 2013; etin et al. 2014) studies have reported
health risks for public exposure to electromagnetic radiation (EMR). These risks need to be
investigated to ensure the safety of women and offspring since these vulnerable individuals
are exposed at the same level of environmental EMR as the general population (Otto and von
Mhlendahl, 2007; Takahashi et al. 2010; etin et al. 2014). During a human pregnancy,
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EMR exposure may interact with the foetus and result in developmental abnormalities that
may potentially cause foetal death or mutations (Mendonca et al. 2011; Nguyen and
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Goodman, 2012). The biological effects of EMR and their consequences are receiving great
interest; however, data on these effects are still scarce and conflicting.
Reactive oxygen substances (ROS) are produced in many physiological functions such
as phagocytic activity and mitochondrial functions. ROS induce oxidative injuries in cellular
biomolecules such as lipids, proteins and nucleic acids (Dasdag et al. 2009; Akdag et al.
2013). The brain consumes the highest amount of oxygen in the human body and has poor
antioxidant levels (Halliwell, 2006). The brain also has high levels of polyunsaturated fatty
acids (PUFAs) that are one of the main targets of ROS (zmen et al. 2007). These three
factors make the brain more sensitive to oxidative damage. Additionally, EMR is mainly
detoxified in the human liver and it induces hepatoxicity (De and Devasagayam, 2011; Ferk et
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al. 2011). The ROS are controlled and scavenged by enzymatic and non-enzymatic
antioxidants. One of most important enzymatic antioxidants is glutathione peroxidase (GSHPx), which converts hydrogen peroxide to water (Nazrolu, 2009). Vitamin E is a hydrophilic
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molecule that can scavenge several radicals within the cells and plasma (Halliwell, 2006), and
it is likely that vitamins C and E act in a synergistic manner (Frei et al. 1989). Reduced
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glutathione (GSH) and -carotene are hydroxyl radical and singlet oxygen scavengers that
participate in a wide range of cellular functions (Halliwell, 2006; Jiang, 2014). ROS may be
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involved in the action of Wi-Fi exposure-induced EMR in the brain and liver of developing
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humans and animals. However, this subject needs to be urgently clarified in an experimental
animal model.
EMR absorption rates in various tissues are affected by dielectric properties and organ
conductivity. Whole-body electrical conductivity increases during pregnancy due to an
increased water content, and this makes pregnant women and their foetuses hypersensitive to
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EMR (Nazrolu et al. 2013). Additionally, Wi-Fi from cell phones and computers are
primarily used near the head and may have harmful effects on the brain. Furthermore, Wi-Fi
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exposure induces oxidative stress resulting in decreased antioxidant levels in the brains of
experimental animals (etin et al. 2014). However, whether EMR changes oxidative stress in
the brain and liver during offspring development remains unclear; therefore, the need to
address this question has formed the basis of this study.
In a recent study (etin et al. 2014), we were unable to observe changes in oxidative
stress values of the brain and liver in 2.45 GHz EMR-exposed newborn rats between the
fourth and sixth weeks following birth because rat brains are developing during the
synaptogenesis period (the first 3 weeks after birth) (Tiwari and Chopra, 2011). Moreover,
reports of EMR exposure on oxidative stress in the brain and liver of rats are conflicting
(Nazrolu and Gmral, 2009; Takahashi et al. 2010; Dasdag et al. 2012; Shahin et al. 2013;
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etin et al. 2014; Ghazizadeh and Nazrolu, 2014; Grler et al. 2014). The present study was
conducted in rats during pregnancy and newborn development between the first and third
weeks to determine the effects of 2.45 GHz exposure on EMR-induced brain and liver
glutathione
(GSH),
malondialdehyde,
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N-hexane,
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oxidative injuries.
1,1,3,3
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and -tocopherol were analytical grade, obtained from Sigma-Aldrich Chemical Inc. (St.
Louis, MO, USA). All solutions, except phosphate buffers, were prepared daily and stored at
+4.0 C. The reagents were allowed to equilibrate at room temperature for at least 30-min
before used for analysis. The phosphate buffers were stable in refrigerator (+4.0 C) for one
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Animals
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month.
We used 16 Wistar albino pregnant dam rats (age, 12 weeks; weight, 190 21 g) and
their 48 newborns. The rats were housed individually in stainless steel cages in a pathogenfree environment at 22 2C, with light exposure from 08.00 to 20.00; the rats were given
free access to water and were fed a commercial diet.
Study groups
The rats were exposed to the EMR radiations during the pregnancy. The 48 newborn
male animals of the rats were selected and randomly divided into two equal groups as follows:
Group A (n=8 pregnant and n=24 newborn): Control rats. The rats exposed to cage stress 60
min/day from pregnancy to 3 weeks old (5 day a week).
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Group B (n=8 pregnant and n=24 newborn): Rats exposed to 2.45 GHz during 60 min/day
from pregnancy to 3 weeks old (Nazrolu et al. 2012a).
Control rats were exposed to cage stress without exposure the radiofrequencies.
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Pregnancy of the rats was detected presence of sperms in vaginal smear. The condition of the
gestation and any malformation or prenatal death of the offspring did not observe during the
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current experiment. After pregnancy, female and male newborn rats were exposed to the EMR
exposures till 3 weeks old. The three weeks of exposure in the newborns were performed in
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cage (total body exposure) although mothers received the EMR exposure in a strainer (Figure
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1). Control pregnant and offspring rats were kept in the same cage stress condition without
The exposure system have been using in our EMR studies routinely and the details of
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the 2.45 GHz exposure system have been described in our previous studies (i.e. Nazrolu et
al. 2012a; Nazrolu et al. 2012b). A generator from Bier Electronic Co, Sakarya (Turkey),
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provided with a half-wave dipole antenna system was used to irradiate the cells with 2.45
GHz radio frequencies with 217 Hz pulses. The electric field density was set at 20 dB and 11
V/m in order to get a 0.1 W/kg whole-body average specific absorption rate (SAR). In a
recent study we observed that oxidative toxic effect of Wi-Fi occurred between 0 and 25 cm
(i and Nazrolu, 2015). Hence, the distance of the antenna from the head of rats for 2.45
GHz exposure was 25 cm (Figure 1). The exposure system was kept a specific room which
was including plastic furniture such as tables and chairs for protecting the rats possible
radiation reflection. Chromium-nickel metals were used for covering walls in order to
protecting the rats from possible outside telemetric exposure. The required electrical field
density (0.1 W/kg whole-body average SAR) for 2.45 GHz exposures, radiation reflection and
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exposure was continuously recorded every 5 minutes using a satellite level meter (EXTECH480836, Extech Instruments Corporation, Nashua, NH, USA) as described a previous study
(i and Nazrolu, 2015).
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The electromagnetic radiation dose was calculated from the measured electric field
density (V/m). Dielectric permittivity and conductivity values of the rat tissues at certain
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frequencies were obtained from the reports of Peyman et al. (2001). The SAR values at the
input 12 W/cm2 power flux density were calculated using software program. The whole
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body SAR values are varied in the 0.01-1.5 W/kg range, representing SAR means values of
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0.20 0.06 W/kg for whole body of 2.45 GHz EMR exposures, with a value of 10 V/m at the
closest point in the body.
The rats of control group were placed in the cylindrical restrainer with the radio
frequency source switched off during times similar to those used for irradiation. The control
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animals were kept in their cage without any treatment or restraint of any kind.
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Under ether inhalation anaesthesia, the rats were decapitated, and their brain and liver
samples were removed. After taking the heads from body and the brain cortex and liver
samples were removed. The cortex was dissected out after the brain was split in the midsagittal plane. Following cortex removal, the brain was dissected from the total brain as
described previously (Btn et al. 2015).
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The brain and liver were weighed, washed twice with cold saline solution, placed into
glass bottles, labelled, and stored in a deep freeze (85C) until processing (maximum 3
weeks). After weighing, half of the brain and liver were cut into small pieces using scissors,
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and homogenized (5 min at 3000 rpm) in 2 ml volumes (1:5, w/v) of ice-cold Tris-HCl buffer
(50 mM, pH 7.4) using an ultrasonic homogenizer (Bandelin-2070, BANDELIN electronic,
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GmbH & Co. KG, Berlin, Germany). All preparation procedures were performed on ice. The
brain and liver homogenate samples were used for measuring the immediate lipid
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peroxidation levels and enzyme activities. Antioxidant vitamins were analysed within 3
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weeks.
Method of Placer et al. (1966) was used for the brain and liver homogenate lipid
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peroxidation values in brain and liver samples were expressed as mol/ g protein.
method of Sedlak and Lindsay (1968). GSH values in brain and liver samples were expressed
as mol/ g protein.
GSH-Px
activities
of
the
brain
and
liver
homogenate
were
measured
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Lowry et al. (1951) with bovine serum albumin as the standard.
Vitamin analyses
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Vitamins A (retinol) (Suzuki and Katoh, 1990) and vitamin E (-tocopherol) (Desai,
1984) determined in the brain and liver samples via heating and KOH modifications. About
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0.5 g of brain and liver samples were saponified by the addition of 0.3 ml 60 percent (w/v in
water) KOH and two ml of one percent (w/v in ethanol) antioxidant pyrogallol, followed by
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heating at 70C for 30 min. After cooling the samples on ice, 2 ml of water and 1 ml of n-
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hexane were added and mixed with the samples and then rested for 10 min to allow phase
separation. An aliquot of 0.5 ml of n-hexane extract was taken and vitamin A levels were
measured at 325 nm. Then reactants were added and the absorbance value of hexane was
measured in a spectrophotometer at 535 nm. Calibration was performed using standard
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Folin phenol reagent technique for the estimation of vitamin C as ascorbic acid in
brain and liver homogenate samples was used according to the method of Jagota and Dani
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(1982). The absorbance of the samples was measured spectrophotometrically at 760 nm.
Statistical analyses
All results are expressed as means standard deviation (SD). To determine the effect
of exposure, data were analyzed using analysis of variance (ANOVA). P-values of less than
0.05 were regarded as significant. Significant values were assessed with least significance test
Mann Whitney U test. Data was analyzed using the SPSS statistical program (version 17.0
software, SPSS Inc. Chicago, IL, USA).
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Results
Lipid peroxidation results in the brain and liver
The mean lipid peroxidation levels of the brain in the three groups are shown in
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Figure 2. The mean brain lipid peroxidation levels (as mol/g protein) at the 1st, 2nd and 3rd
weeks were 8.89, 8.93 and 9.17 in the controls, and 10.6, 10.9 and 11.9, 16.40 in the EMR
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group, respectively. The lipid peroxidation levels in the brain samples were significantly
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The mean lipid peroxidation levels of the liver in the three groups are shown in
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Figure 3. The mean lipid peroxidation levels of the liver (as mol/g protein) at the 1st, 2nd
and 3rd weeks were significantly lower in the controls (15.60, 17.80 and 19.00,
respectively) than in the EMR groups (18.40, 20.90 [p < 0.05] and 23.30 [p < 0.01],
respectively). Hence, oxidative stress levels, as reflected by MDA levels, in the brain and
liver samples were increased in the development of newborn rats by the EMR exposures.
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The mean GSH level and GSH-Px activity of the brain and liver in the three groups
are shown in Tables 1 and 2, respectively. GSH-Px activities and GSH concentrations in the
brain and liver were significantly (p < 0.05) lower in the EMR groups than in the controls.
However, the liver GSH levels of the three groups did not change.
Antioxidant vitamin concentrations in the brain and liver
The mean vitamin A, -carotene, vitamin C and vitamin E concentrations of the brain
and liver in the three groups are shown in Tables 1 and 2. Vitamin A (p < 0.05 and
p < 0.001), -carotene (p < 0.01 for brain and p < 0.05 for liver) and vitamin C (p < 0.01 and
p < 0.001 for brain) concentrations in the brain and liver at three weeks were markedly
lower in the EMR group than in the controls. However, liver vitamin C concentrations were
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not affected by EMR exposure.
Discussion
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length of time and frequency of use, which varies from individual to individual or because of
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specific circumstances. Modern Wi-Fi internet devices work at a frequency of 2.45 GHz,
which was consequently selected for the present study. The brains and livers of newborns
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within the first three weeks of life are very sensitive to oxidative injuries due to poor
antioxidant capacities. Several reports in adults have indicated that EMR exposure modifies
cellular oxidative stress and antioxidant redox systems in the foetus and newborn of animals
(zorak et al. 2013; etin et al. 2014) and humans (Mendonca et al. 2011; Nguyen and
Goodman, 2012). The mechanism by which such effects could occur is not completely
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We observed that brain and liver lipid peroxidation levels in the EMR-exposed groups
were increased compared with controls. Additionally, antioxidant vitamin and GSH
concentrations, and GSH-Px activities, were decreased in the brain and liver of EMR-exposed
groups. Results on the liver and brain of 2.45 GHz EMR-exposed adult rats and neurons
regarding the effects of oxidative stress in the pathogenesis of EMR have been reported
(Nazrolu and Gmral, 2009; Dasdag et al. 2009; Shahin et al. 2013; Nazrolu et al. 2012a;
Ghazizadeh and Nazrolu, 2014; Grler et al. 2014). To the best of our knowledge, the
current study is the first to compare treatment with 2.45 GHz with particular reference to
oxidative stress in brain and liver of EMR-exposed newborn rats.
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Results of numerous studies indicate that the excessive production of ROS occurs
during EMR exposure. It is well known that 7080% of cells contain water. Furthermore, a
foetus is contained within the amniotic fluid as well as having its own cellular water contents.
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The water concentration of a newborn is also higher than in an adult. Newborn brains are
poorly protected from EMR injuries due to their thin skulls (etin et al. 2014). If the water
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will be exposed to EMR decomposition occurs through which a variety of ROS and these
ROS formed in cells contribute EMR oxidative injury in brain and liver of newborns
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(Nazrolu and Gumral, 2009; Selakovi et al. 2013). In addition to ROS production, the
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effects of EMR on oxygen, level and lifetime of free radicals are increased by EMR exposure
(Brocklehurst and McLauchlan, 1996). Furthermore, EMR can increase lipid peroxidation and
decrease antioxidant defence systems in the brain and liver (Nazrolu and Gmral, 2009;
Dasdag et al. 2009; Akdag et al. 2010; Shahin et al. 2013; Nazrolu et al. 2012a; Ghazizadeh
and Nazrolu, 2014; Rau Balind et al. 2014). It also induces DNA damage in brain (Dasdag
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et al. 2015a and 2015b). The EMR-induced ROS are scavenged by enzymatic substances such
as GSH-Px and catalase, and nonenzymatic antioxidants such as vitamins C and E (Halliwell,
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2006; Nazrolu, 2007). Levels of enzymatic and nonenzymatic antioxidants in the brain are
considerably low; however, there are high rates of oxygen metabolism and PUFA contents in
the brain (Halliwell, 2006; zmen et al. 2007). We recently observed that increased Ca2+
entry, through the activation of TRPM2 and TRPV1 channels, induces an overproduction of
ROS in neurons (Nazrolu et al. 2012a; Ghazizadeh and Nazrolu, 2014). Lipid
peroxidation levels in the brain and liver during rat development were increased in the EMR
groups; however, enzymatic and nonenzymatic antioxidant concentrations in the brain and
liver were also increased in the EMR groups. The decreased lipid peroxidation values could
be due to their depletion as a result of an increased production of oxidant radicals and
increased Ca2+ entry into the brain and liver.
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Vitamin E, as -tocopherol, is the most important fat-soluble antioxidant in the lipid
structure of cell membranes and organelles (Halliwell, 2006; Nazrolu, 2007). Vitamin E
has antioxidant and non-antioxidant molecular roles, and the scavenging of ROS is
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performed by the antioxidant role of vitamin E (Jiang, 2014). Vitamin C (ascorbic acid) is a
water-soluble antioxidant, although its concentration is low in the brain compared to its
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plasma and kidney levels (Frei et al. 1989). Oxidized vitamin E is converted to its active
form by vitamin C and GSH (Halliwell, 2006; Nazrolu, 2007). Hydrogen peroxide and
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hydroxyl radicals are detoxified in the brain and liver by the selenium-dependent enzymatic
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antioxidant, GSH-Px (Nazrolu, 2009). Antioxidant levels in the brain are considerably
low. Hence, a low antioxidant ascorbic acid concentration and a high content of PUFA
result in limited antioxidant defences in the brain. The GSH-Px activity; the vitamin A,
-carotene, and vitamin E concentrations in the brain and liver; and the vitamin C and GSH
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concentrations in the brain and liver were increased by the EMR exposure. The decreased
concentrations of the antioxidant vitamins could be due to their depletion or inhibition due
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to the increased production of free radicals. The decrease of GSH-Px, GSH and antioxidant
vitamins in the brain and liver during the development of newborn rats has been attributed
to the induction of ROS and lipid peroxidation. Similarly, we recently observed decreased
vitamin A, -carotene, vitamin E and vitamin C concentrations in the kidneys, brains and
livers of adult rats and newborn rats produced by 2.45 GHz exposure (Nazrolu and
Gumral, 2009; Ozorak et al. 2013; Nazrolu et al. 2012a; etin et al. 2014).
In conclusion, these results demonstrated that Wi-Fi (2.45 GHz) devices might induce
oxidative toxicity through GSH, GSH-Px and antioxidant vitamin concentration decreases in
the brains and livers of rat pups during development. The results of lipid peroxidation and
antioxidant activity indicate that the brain was more sensitive to oxidative injury compared to
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the liver. However, further investigations in humans and babies are needed to clarify the
mechanism of action of the applied EMR exposure and oxidative stress on the rat brain and
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Duality of interest
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The authors declare that there is no duality of interest associated with this manuscript.
Ethical statement
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Pregnant Wistar albino rats weighing 190 21 g at the ages of 10-12 weeks and and
their 48 newborns from Laboratory Animal Resources of Suleyman Demirel University
(SDU) (Isparta, Turkey) were utilized. All animal studies were conducted using approved
protocols and carried out in accordance with the Principles of Laboratory Animal Care (NIH
Publication no. 85-23, revised 1985). All procedures were approved by the Medical Faculty
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Authors contributions
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Mustafa Nazrolu formulated the present hypothesis and was responsible for writing
the report. mer elik was responsible for analysis of the data.
Acknowledgement
The authors thank Assoc. Prof. Dr. Seluk mleki (Electronics and Communication
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Table 1. Effects of Wi-Fi (2.45 GHz) frequencies on glutathione peroxidase (GSH-Px)
activity, reduced glutathione (GSH) and antioxidant vitamin concentrations in brain of
developing newborn rats (n = 8, mean SD).
AGE
1st
(WEEKS)
2nd
3rd
Groups
GSH-Px
(IU/g protein)
Control
EMR
12.49 0.72
10.27 1.62a
12.46 1.33
9.63 1.88a
GSH
(mol/g protein)
Control
EMR
6.97 0.72
6.28 0.38a
7.19 0.38
6.51 0.52a
Vitamin A
(mol/g tissue)
Control
EMR
1.98 0.29
2.16 0.23a
2.11 0.31
2.56 0.31b
2.33 0.28
2.76 0.33a
-carotene
(mol/g tissue)
Control
EMR
0.88 0.14
1.10 0.15b
0.87 0.16
1.15 0.19b
0.89 0.14
1.24 0.16b
Vitamin C
(mol/g tissue)
Control
EMR
30.50 9.57
49.00 8.55b
29.80 9.48
54.60 4.22c
27.00 6.61
45.40 8.58b
Vitamin E
(mol/g tissue)
Control
EMR
13.01 0.70
16.48 0.90a
14.33 1.02
17.77 1.41a
15.58 1.01
18.57 1.45a
cr
6.97 0.78
6.43 0.48a
us
an
13.39 1.21
8.89 1.09b
ip
t
Parameters
Ac
ce
p
te
p<0.05, bp<0.01 and bp<0.001 as compared with group control at same week.
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21
Table 2. Effects of Wi-Fi (2.45 GHz) exposure on glutathione peroxidase (GSH-Px) activity,
reduced glutathione (GSH) and antioxidant vitamin concentrations in liver of developing
newborn rats (n = 8, mean SD).
AGE
1st
(WEEKS)
2nd
3rd
Groups
GSH-Px
(IU/g protein)
Control
EMR
18.49 1.59
16.46 1.34a
19.01 1.60
17.06 1.12a
GSH
(mol/g protein)
Control
EMR
9.99 0.07
9.53 0.14
9.81 0.34
9.45 0.35
Vitamin A
(mol/g tissue)
Control
EMR
5.74 0.37
4.14 0.61a
6.31 0.82
3.63 0.37b
10.90 0.78
4.63 0.43b
-carotene
(mol/g tissue)
Control
EMR
1.30 0.10
1.17 0.17a
1.42 0.18
1.26 0.07a
1.56 0.19
1.41 0.08a
Vitamin C
(mol/g tissue)
Control
EMR
39.70 8.03
38.30 8.91
48.30 8.03
49.70 8.98
58.90 13.60
51.10 10.10
Vitamin E
(mol/g tissue)
Control
EMR
18.04 0.97
15.82 090a
18.18 1.00
14.57 0.68c
19.52 2.08
14.83 1.23a
9.35 0.31
9.07 0.61
cr
us
an
19.25 0.82
17.39 1.17a
ip
t
Parameters
Ac
ce
p
te
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22
Figure 1: The experimental set-up for irradiation of rats (Nazrolu and Gumral, 2009).
Figure 2. Effects of Wi-Fi (2.45 GHz) frequencies on lipid peroxidation levels in brain of
ip
t
cr
Figure 3. Effects of Wi-Fi (2.45 GHz) frequencies on lipid peroxidation levels in liver of
Ac
ce
p
te
an
us
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ed
ce
pt
Ac
us
an
cr
ip
t
Ac
ce
pt
ed
an
us
cr
Figure 1
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Ac
ce
pt
ed
an
us
cr
Figure 2
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Ac
ce
pt
ed
an
us
cr
Figure 3
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Highlights
Oxidative stress plays important role in biology of Wi-Fi (2.45 GHz)> 2.45 GHz increased
oxidative stress in brain and liver pregnant rats and their newborns.> Brain seems sensitive to
Ac
ce
pt
ed
an
us
cr
ip
t
Page 27 of 27