Endocrine

, Volume 52, Issue 2, pp 352–362 | Cite as

Long-term exposure to electromagnetic radiation from mobile phones and Wi-Fi devices decreases plasma prolactin, progesterone, and estrogen levels but increases uterine oxidative stress in pregnant rats and their offspring

  • Murat Yüksel
  • Mustafa Nazıroğlu
  • Mehmet Okan Özkaya
Original Article
First Online:
Received:
Accepted:

Abstract

We investigated the effects of mobile phone (900 and 1800 MHz)- and Wi-Fi (2450 MHz)-induced electromagnetic radiation (EMR) exposure on uterine oxidative stress and plasma hormone levels in pregnant rats and their offspring. Thirty-two rats and their forty newborn offspring were divided into the following four groups according to the type of EMR exposure they were subjected to: the control, 900, 1800, and 2450 MHz groups. Each experimental group was exposed to EMR for 60 min/day during the pregnancy and growth periods. The pregnant rats were allowed to stand for four generations (total 52 weeks) before, plasma and uterine samples were obtained. During the 4th, 5th, and 6th weeks of the experiment, plasma and uterine samples were also obtained from the developing rats. Although uterine lipid peroxidation increased in the EMR groups, uterine glutathione peroxidase activity (4th and 5th weeks) and plasma prolactin levels (6th week) in developing rats decreased in these groups. In the maternal rats, the plasma prolactin, estrogen, and progesterone levels decreased in the EMR groups, while the plasma total oxidant status, and body temperatures increased. There were no changes in the levels of reduced glutathione, total antioxidants, or vitamins A, C, and E in the uterine and plasma samples of maternal rats. In conclusion, although EMR exposure decreased the prolactin, estrogen, and progesterone levels in the plasma of maternal rats and their offspring, EMR-induced oxidative stress in the uteri of maternal rats increased during the development of offspring. Mobile phone- and Wi-Fi-induced EMR may be one cause of increased oxidative uterine injury in growing rats and decreased hormone levels in maternal rats.

Graphical Abstract

TRPV1 cation channels are the possible molecular pathways responsible for changes in the hormone, oxidative stress, and body temperature levels in the uterus of maternal rats following a year-long exposure to electromagnetic radiation exposure from mobile phones and Wi-Fi devices. It is likely that TRPV1-mediated Ca2+ entry in the uterus of pregnant rats involves accumulation of oxidative stress and opening of mitochondrial membrane pores that consequently leads to mitochondrial dysfunction, substantial swelling of the mitochondria with rupture of the outer membrane and release of oxidants such as superoxide (O2−) and hydrogen peroxide (H2O2). The superoxide radical is converted to H2O2 by superoxide dismutase (SOD) enzyme. Glutathione peroxidase (GSH-Px) is an important antioxidant enzyme for removing lipid hydroperoxides and hydrogen peroxide and it catalyzes the reduction of H2O2 to water.

Keywords

Antioxidants Uterine Hormone Growing rat Electromagnetic radiation 

Abbreviations

ELF

Extremely low electrical field

ELISA

Enzyme-linked immunosorbent assay

EMR

Electromagnetic radiation

FSH

Follicle-stimulating hormone

GSH

Reduced glutathione

GSH-Px

Glutathione peroxidase

LH

Luteinizing hormone

NADPH

Nicotinamide adenine dinucleotide phosphate

ROS

Reactive oxygen species

TAS

Total antioxidant status

TOS

Total oxidant status

WLAN

Wireless local area network

References

  1. 1.
    M. Nazıroğlu, M. Yuksel, M.O. Özkaya, S.A. Köse, Effects of Wi-Fi and mobile phone on reproductive systems in female and male. J. Membr. Biol. 246, 869–875 (2013)CrossRefPubMedGoogle Scholar
  2. 2.
    J.B. Burch, J.S. Reif, C.W. Noonan, T. Ichinose, A.M. Bachand, T.L. Koleber, M.G. Yost, Melatonin metabolite excretion among cellular telephone users. Int. J. Radiat. Biol. 78, 1029–1036 (2002)CrossRefPubMedGoogle Scholar
  3. 3.
    E.S. Altpeter, M. Röösli, M. Battaglia, D. Pfluger, C.E. Minder, T. Abelin, Effect of short-wave (6-22 MHz) magnetic fields on sleep quality and melatonin cycle in humans: the Schwarzenburg shut-down study. Bioelectromagnetics. 27, 142–150 (2006)CrossRefPubMedGoogle Scholar
  4. 4.
    International Commission on Non-Ionizing Radiation Protection (ICNIRP), SCI Review mobile phones, brain tumors and the interphone study: where are we now? Environ. Health Perspect. 119, 1534–1538 (2011)CrossRefGoogle Scholar
  5. 5.
    R. de Seze, P. Fabbro-Peray, L. Miro, GSM radiocellular telephones do not disturb the secretion of antepituitary hormones in humans. Bioelectromagnetics 19, 271–278 (1998)CrossRefPubMedGoogle Scholar
  6. 6.
    Y. Djeridane, Y. Touitou, R. de Seze, Influence of electromagnetic fields emitted by GSM-900 cellular telephones on the circadian patterns of gonadal, adrenal and pituitary hormones in men. Radiat. Res. 169, 337–343 (2008)CrossRefPubMedGoogle Scholar
  7. 7.
    M. Woldanska-Okonska, M. Karasek, J. Czernicki, The influence of chronic exposure to low frequency pulsating magnetic fields on concentrations of FSH, LH, prolactin, testosterone and estradiol in men with back pain. Neuroendocrinol. Lett. 25, 201–206 (2004)PubMedGoogle Scholar
  8. 8.
    B. Çiğ, M. Nazıroğlu, Investigation of the effects of distance from sources on apoptosis, oxidative stress and cytosolic calcium accumulation via TRPV1 channels induced by mobile phones and Wi-Fi in breast cancer cells. Biochim. Biophys. Acta 1848, 2756–2765 (2015)CrossRefPubMedGoogle Scholar
  9. 9.
    F. Poulletier de Gannes, B. Billaudel, E. Haro et al., Rat fertility and embryo fetal development: influence of exposure to the Wi-Fi signal. Reprod. Toxicol. 36C, 1–5 (2012)Google Scholar
  10. 10.
    G. Kismali, E. Ozgur, G. Guler, A. Akcay, T. Sel, N. Seyhan, The influence of 1800 MHz GSM-like signals on blood chemistry and oxidative stress in non-pregnant and pregnant rabbits. Int. J. Rad. Biol. 88, 414–419 (2012)CrossRefPubMedGoogle Scholar
  11. 11.
    A.M. Sommer, K. Grote, T. Reinhardt, J. Streckert, V. Hansen, A. Lerchl, Effects of radiofrequency electromagnetic fields (UMTS) on reproduction and development of mice: a multi-generation study. Radiat. Res. 171, 89–95 (2009)CrossRefPubMedGoogle Scholar
  12. 12.
    M.A. Al-Akhras, A. Elbetieha, M.K. Hasan, I. Al-Omari, H. Darmani, B. Albiss, Effects of low-frequency magnetic field on fertility of adult male and female rats. Bioelectromagnetics 22, 340–344 (2001)CrossRefPubMedGoogle Scholar
  13. 13.
    J. Kliukiene, T. Tynes, A. Andersen, Residential and occupational exposures to 50-Hz magnetic fields and breast cancer in women: a population-based study. Am. J. Epidemiol. 159, 852–861 (2004)CrossRefPubMedGoogle Scholar
  14. 14.
    A. Özorak, M. Nazıroğlu, Ö. Çelik, M. Yüksel, D. Özçelik, M.O. Özkaya, H. Çetin, M.C. Kahya, S.A. Kose, Wi-Fi (2.45 GHz) and mobile phone (900 and 1800 MHz)-induced risks on oxidative stress and elements in kidney and testis of rats during pregnancy and the development of newborns. Biol. Trace Elem. Res. 156(1-3), 221–229 (2013)CrossRefPubMedGoogle Scholar
  15. 15.
    Y. Türker, M. Nazıroğlu, N. Gümral et al., Selenium and L-carnitine reduce oxidative stress in the heart of rat induced by 2.45-GHz radiation from wireless devices. Biol. Trace Elem. Res. 143, 1640–1650 (2011)CrossRefPubMedGoogle Scholar
  16. 16.
    Z. Jin, C. Zong, B. Jiang, Z. Zhou, J. Tong, Y. Cao, The effect of combined exposure of 900 MHz radiofrequency fields and doxorubicin in HL-60 cells. PLoS ONE 7(9), e46102 (2012)CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    A. Peyman, A. Rezazadeh, C. Gabriel, Changes in the dielectric properties of rat tissue as a function of age at microwave frequencies. Physics Med. Biol. 46, 1617–1629 (2001)CrossRefGoogle Scholar
  18. 18.
    Z.A. Placer, L. Cushman, B.C. Johnson, Estimation of products of lipid peroxidation (malonyl dialdehyde) in biological fluids. Anal. Biochem. 16, 359–364 (1966)CrossRefPubMedGoogle Scholar
  19. 19.
    O.H. Lowry, N.J. Rosenbrough, A.L. Farr, R.J. Randall, Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)PubMedGoogle Scholar
  20. 20.
    J. Sedlak, R.H.C. Lindsay, Estimation of total, protein bound and non-protein sulfhydryl groups in tissue with Ellmann’s reagent. Anal. Biochem. 25, 192–205 (1968)CrossRefPubMedGoogle Scholar
  21. 21.
    R.A. Lawrence, R.F. Burk, Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 71, 952–958 (1976)CrossRefPubMedGoogle Scholar
  22. 22.
    I.D. Desai, Vitamin E analysis methods for animal tissues. Methods Enzymol. 105, 138–147 (1984)CrossRefPubMedGoogle Scholar
  23. 23.
    J. Suzuki, N. Katoh, A simple and cheap method for measuring vitamin A in cattle using only a spectrophotometer. Jpn. J. Vet. Sci. 52, 1282–1284 (1990)Google Scholar
  24. 24.
    S.K. Jagota, H.M. Dani, A new colorimetric technique for the estimation of vitamin C using Folin phenol reagent. Anal. Biochem. 127, 178–182 (1982)CrossRefPubMedGoogle Scholar
  25. 25.
    O. Erel, A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem. 37, 277–285 (2004)CrossRefPubMedGoogle Scholar
  26. 26.
    S. Seité, E. Popovic, M.P. Verdier, R. Roguet, P. Portes, C. Cohen, A. Fourtanier, J.B. Galey, Iron chelation can modulate UVA-induced lipid peroxidation and ferritin expression in human reconstructed epidermis. Photodermatol. Photoimmunol. Photomed. 20, 47–52 (2004)CrossRefPubMedGoogle Scholar
  27. 27.
    M.Y. Obolenskaya, N.M. Teplyuk, R.L. Divi, M.C. Poirier, N.B. Filimonova, M. Zadrozna, M.J. Pasanen, Human placental glutathione S-transferase activity and polycyclic aromatic hydrocarbon DNA adducts as biomarkers for environmental oxidative stress in placentas from pregnant women living in radioactivity- and chemically-polluted regions. Toxicol. Lett. 196(2), 80–86 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    M. Nazıroğlu, Role of selenium on calcium signaling and oxidative stress- induced molecular pathways in epilepsy. Neurochem. Res. 34, 2181–2191 (2009)CrossRefPubMedGoogle Scholar
  29. 29.
    M.E. Anderson, Glutathione: an overview of biosynthesis and modulation. Chem. Biol. Interact. 111–112, 1–14 (1998)CrossRefPubMedGoogle Scholar
  30. 30.
    I. Belyaev, Non-thermal biological effects of microwaves. Microw. Rev. 11, 13–29 (2005)Google Scholar
  31. 31.
    J.M. Lary, D.L. Conover, P.H. Johnson, R.W. Hornung, Dose-response relationship body temperature and birth defects in radiofrequency-irradiation rats. Bioelectromagnetics 7, 141–149 (1986)CrossRefPubMedGoogle Scholar
  32. 32.
    R.T. Wangemann, S.F. Cleary, The in vivo effects of 2.45 GHz microwave radiation on rabbit serum components and sleeping environmental times. Radiat. Environ. Biophys. 13, 89–103 (1976)CrossRefPubMedGoogle Scholar
  33. 33.
    A. Tomruk, G. Guler, A.S. Dincel, The Influence of 1800 MHz GSM-like signals on hepatic oxidative DNA and lipid damage in nonpregnant, pregnant, and newly born rabbits. Cell Biochem. Biophys. 56, 39–47 (2010)CrossRefPubMedGoogle Scholar
  34. 34.
    H. Çetin, M. Nazıroğlu, Ö. Çelik, M. Yüksel, N. Pastacı, M.O. Özkaya, Liver antioxidant stores protect the brain from electromagnetic radiation (900 and 1800 MHz)-induced oxidative stress in rats during pregnancy and the development of offspring. J. Matern. Fetal. Neonatal. Med. 27, 1915–1921 (2014)CrossRefPubMedGoogle Scholar
  35. 35.
    M. Ozguner, A. Koyu, G. Cesur, M. Ural, F. Ozguner, A. Gokcimen, N. Delibas, Biological and morphological effects on the reproductive organ of rats after exposure to electromagnetic field. Saudi Med. J. 26(3), 405–410 (2005)PubMedGoogle Scholar
  36. 36.
    M.A. Al-Akhras, Influence of 50 Hz magnetic field on sex hormones and body, uterine, and ovarian weights of adult female rats. Electromagn. Biol. Med. 27, 155–163 (2008)CrossRefPubMedGoogle Scholar
  37. 37.
    M. Woldanska-Okonska, M. Karasek, J. Czernicki, The influence of chronic exposure to low frequency pulsating magnetic fields on concentrations of FSH, LH, prolactin, testosterone and estradiol in men with back pain. Neuro Endocrinol. Lett. 25, 201–216 (2004)PubMedGoogle Scholar
  38. 38.
    Y. Kurokawa, H. Nitta, H. Imai, M. Kabuto, Acute exposure to 50 Hz magnetic fields with harmonic and transient components: lack of effects on nighttime hormonal secretion in men. Bioelectromagnetics 24, 12–20 (2003)CrossRefPubMedGoogle Scholar
  39. 39.
    M. Karasek, A. Lerchl, Melatonin and magnetic fields. Neuroendocrinol. Lett. 23(Suppl. 1), 84–87 (2002)PubMedGoogle Scholar
  40. 40.
    J.S. Schiffman, H.M. Lasch, M.D. Rollag, A.E. Flanders, G.C. Brainard, D.L. Burk, Effect of magnetic resonance imaging on the normal human pineal body: measurements of plasma melatonin levels. J. Magn. Reson. Imaging 4, 7–11 (1994)CrossRefPubMedGoogle Scholar
  41. 41.
    G. Yin, T. Zhu, J. Li, M. Chen, S. Yang, X. Zhao, Decreased expression of survivin, estrogen and progesterone receptors in endometrial tissues after radiofrequency treatment of dysfunctional uterine bleeding. World J. Surg. Oncol. 10, 100 (2012)CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Y. Djeridane, Y. Touitou, R. de Seze, Influence of electromagnetic fields emitted by GSM-900 cellular telephones on the circadian patterns of gonadal, adrenal and pituitary hormones in men. Radiat. Res. 169, 337–343 (2008)CrossRefPubMedGoogle Scholar
  43. 43.
    Y. Shi, X. Bao, X. Huo, Z. Shen, T. Song, 50-Hz magnetic field (0.1-mT) alters c-fos mRNA expression of early post implantation mouse embryos and serum estradiol levels of gravid mice. Birth Defects Res. B Dev. Reprod. Toxicol. 74, 196–200 (2005)CrossRefPubMedGoogle Scholar
  44. 44.
    S. Shahin, V.P. Singh, R.K. Shukla, A. Dhawan, R.K. Gangwar, S.P. Singh, C.M. Chaturvedi, 2.45 GHz microwave irradiation-induced oxidative stress affects implantation or pregnancy in mice, Mus musculus. Appl. Biochem. Biotechnol. 169, 1727–1751 (2013)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Murat Yüksel
    • 1
  • Mustafa Nazıroğlu
    • 2
  • Mehmet Okan Özkaya
    • 1
  1. 1.The Department of Obstetrics and Gynecology, Faculty of MedicineSüleyman Demirel UniversityIspartaTurkey
  2. 2.The Department of Biophysics, Faculty of MedicineSüleyman Demirel UniversityIspartaTurkey

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