Effects of prenatal exposure to a 900 MHz electromagnetic field on 60-day-old rat testis and epididymal sperm quality

References

• Agarwal A, Saleh RA, Bedaiwy MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 79: 829–843.
   PubMed Web of Science ®Google Scholar
• Aitken RJ, Bennetts LE, Sawyer D, Wiklendt AM, King BV (2005) Impact of radio frequency electromagnetic radiation on DNA integrity in the male germline. Int. J. Androl. 28: 171–179.
   PubMed Web of Science ®Google Scholar
• Al-Akhras MA, Elbetieha A, Hasan MK, Al-Omari I, Darmani H, Albiss B (2001) Effects of extremely low frequency magnetic field on fertility of adult male and female rats. Bioelectromagnetics 22: 340–344.
   PubMed Web of Science ®Google Scholar
• Aruoma OI, Halliwell B, Dizdaroglu M (1989) Iron ion-dependent modification of bases in DNA by the superoxide radical-generating system hypoxanthine/xanthine oxidase. J. Biol. Chem. 264: 13024–13028.
   PubMed Web of Science ®Google Scholar
• Bas O, Odaci E, Mollaoglu H, Ucok K, Kaplan S (2009a) Chronic prenatal exposure to the 900 megahertz electromagnetic field induces pyramidal cell loss in the hippocampus of newborn rats. Toxicol. Ind. Health 25: 377–384.
   PubMed Web of Science ®Google Scholar
• Bas O, Odaci E, Kaplan S, Acer N, Ucok K, Colakoglu S (2009b) 900 MHz electromagnetic field exposure affects qualitative and quantitative features of hippocampal pyramidal cells in the adult female rat. Brain Res. 1265: 178–185.
   PubMed Web of Science ®Google Scholar
• Baş O, Sönmez OF, Aslan A, İkinci A, Hancı H, Yıldırım M, Kaya H, Akça M, Odacı E (2013) Pyramidal cell loss in the cornu ammonis of 32-day-old female rats following exposure to a 900 megahertz electromagnetic field during prenatal days 13-21. NeuroQuantology 11: 591–599.
   Web of Science ®Google Scholar
• Bernabò N, Tettamanti E, Russo V, Martelli A, Turriani M, Mattoli M, Barboni B (2010) Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model. Theriogenology 73: 1293–1305.
   PubMed Web of Science ®Google Scholar
• Beumer TL, Roepers-Gajadien HL, Gademan IS, Lock TM, Kal HB, De Rooij DG (2000) Apoptosis regulation in the testis: involvement of Bcl-2 family members. Mol. Reprod. Dev. 56: 353–359.
   PubMed Web of Science ®Google Scholar
• Chen H, Ge RS, Zirkin BR (2009) Leydig cells: from stem cells to aging. Mol. Cell Endocrinol. 306: 9–16.
   PubMed Web of Science ®Google Scholar
• Chung MK, Lee SJ, Kim YB, Park SC, Shin DH, Kim SH, Kim JC (2005) Evaluation of spermatogenesis and fertility in F1 male rats after in utero and neonatal exposure to extremely low frequency electromagnetic fields. Asian J. Androl. 7: 189–194.
   PubMed Web of Science ®Google Scholar
• Dasdag S, Akdag MZ, Ulukaya E, Uzunlar AK, Yegin D (2008) Mobile phone exposure does not induce apoptosis on spermatogenesis in rats. Arch. Med. Res. 39: 40–44.
   PubMed Web of Science ®Google Scholar
• Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 186: 421–431.
   PubMed Web of Science ®Google Scholar
• Erogul O, Oztas E, Yildirim I, Kir T, Aydur E, Komesli G, Irkilata HC, Irmak MK, Peker AF (2006) Effects of electromagnetic radiation from a cellular phone on human sperm motility: an in vitro study. Arch. Med. Res. 37: 840–843.
   PubMed Web of Science ®Google Scholar
• Feychting M, Ahlbom A, Kheifets L (2005) EMF and health. Ann. Rev. Public Health 26: 165–189.
   PubMed Web of Science ®Google Scholar
• Fukagawa NK (1999) Aging: is oxidative stress a marker or is it causal? Proc. Soc. Exp. Biol. Med. 222: 293–298.
   PubMed Web of Science ®Google Scholar
• Guler G, Tomruk A, Ozgur E, Seyhan N (2010) The effect of radiofrequency radiation on DNA and lipid damage in non-pregnant and pregnant rabbits and their newborns. Gen. Physiol. Biophys. 29: 59–66.
   PubMed Web of Science ®Google Scholar
• Gye MC, Park CJ (2012) Effect of electromagnetic field exposure on the reproductive system. Clin. Exp. Reprod. Med. 39: 1–9.
   PubMedGoogle Scholar
• Hancı H, Odacı E, Kaya H, Aliyazıcıoğlu Y, Turan I, Demir S, Colakoğlu S (2013) The effect of prenatal exposure to 900-MHz electromagnetic field on the 21-old-day rat testis. Reprod. Toxicol. 42: 203–209.
   PubMed Web of Science ®Google Scholar
• Hancı H, Türedi S, Topal Z, Mercantepe T, Bozkurt I, Kaya H, Ersöz Ş, Ünal B, Odacı E (2015) Can prenatal exposure to a 900 MHz electromagnetic field affect the morphology of the spleen and thymus, and alter biomarkers of oxidative damage in 21-day-old male rats? Biotech. & Histochem. doi:10.3109/10520295.2015.1042051.
   Google Scholar
• Hardell L, Sage C (2008) Biological effects from electromagnetic field exposure and public exposure standards. Biomed. Pharmacother. 62: 104–109.
   PubMed Web of Science ®Google Scholar
• Huuskonen H, Saastamoinen V, Komulainen H, Laitinen J, Juutilainen J (2001) Effects of low-frequency magnetic fields on implantation in rats. Reprod. Toxicol. 15: 49–59.
   PubMed Web of Science ®Google Scholar
• İkinci A, Odacı E, Yıldırım M, Kaya H, Akça M, Hancı H, Aslan A, Sönmez OF, Baş O (2013) The effects of prenatal exposure to a 900 megahertz electromagnetic field on hippocampus morphology and learning behavior in rat pups. NeuroQuantology 11: 582–590.
   Web of Science ®Google Scholar
• Iorio R, Scrimaglio R, Rantucci E, Delle MS, Di Gaetano A, Finetti N, Francavilla F, Santucci R, Tettamanti E, Colonna R (2007) A preliminary study of oscillating electromagnetic field effects on human spermatozoon motility. Bioelectromagnetics 28: 72–75.
   PubMed Web of Science ®Google Scholar
• Kato M, Honma K, Shigemitsu T, Shiga Y (1994) Circularly polarized, sinusoidal, 50 Hz magnetic field exposure does not influence plasma testosterone levels of rats. Bioelectromagnetics 15: 513–518.
   PubMed Web of Science ®Google Scholar
• Kesari KK, Kumar S, Behari J (2011) Effects of radio-frequency electromagnetic wave exposure from cellular phones on the reproductive pattern in male Wistar rats. Appl. Biochem. Biotechnol. 164: 546–559.
   PubMed Web of Science ®Google Scholar
• Khadir R, Morgan JL, Murray JJ (1999) Effects of 60 Hz magnetic field exposure on polymorphonuclear leukocyte activation. Biochim. Biophys. Acta 1472: 359–367.
   PubMed Web of Science ®Google Scholar
• Kim YW, Kim HS, Lee JS, Kim YJ, Lee SK, Seo JN, Jung KC, Kim N, Gimm YM (2009) Effects of 60 Hz 14 microT magnetic field on the apoptosis of testicular germ cell in mice. Bioelectromagnetics 30: 66–72.
   PubMed Web of Science ®Google Scholar
• Kowalczuk CI, Robbins L, Thomas JM, Butland BK, Saunders RD (1994) Effects of prenatal exposure to 50 Hz magnetic fields on development in mice. I. Implantation rate and fetal development. Bioelectromagnetics 15: 349–361.
   PubMed Web of Science ®Google Scholar
• Kumar S, Behari J, Sisodia R (2012) Impact of microwave at X-band in the aetiology of male infertility. Electromag. Biol. Med. 31: 223–232.
   PubMed Web of Science ®Google Scholar
• Leblond CP, Clermont Y (1952). Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann. NY Acad. Sci. 55: 548–573.
   PubMed Web of Science ®Google Scholar
• Lee JS, Ahn SS, Jung KC, Kim YW, Lee SK (2004) Effects of 60 Hz electromagnetic field exposure on testicular germ cell apoptosis in mice. Asian J. Androl. 6: 29–34.
   PubMed Web of Science ®Google Scholar
• Li DK, Yani B, Li Z, Gao E, Miao M, Gong D, Weng X, Ferber JR, Yuan W (2010) Exposure to magnetic fields and the risk of poor sperm quality. Reprod. Toxicol. 29: 86–92.
   PubMed Web of Science ®Google Scholar
• Luo Y, Wang X, Chen Y, Xu S, Ding G, Shi C (2013) Effects of electromagnetic radiation on morphology and TGF-β3 expression in mouse testicular tissue. Toxicology 310: 8–14.
   PubMed Web of Science ®Google Scholar
• Marinelli F, La Sala D, Cicciotti G, Cattini L, Trimarchi C, Putti S, Zamparelli A, Giuliani L, Tomassetti G, Cinti C (2004) Exposure to 900 MHz electromagnetic field induces an unbalance between pro-apoptotic and pro-survival signals in T-lymphoblastoid leukemia CCRF-CEM cells. J. Cell. Physiol. 198: 324–332.
   PubMed Web of Science ®Google Scholar
• Nikolova T, Czyz J, Rolletschek A, Blyszczuk P, Fuchs J, Jovtchev G, Schuderer J, Kuster N, Wobus AM (2005) Electromagnetic fields affect transcript levels of apoptosis-related genes in embryonic stem cell-derived neural progenitor cells. FASEB J. 19: 1686–1688.
   PubMed Web of Science ®Google Scholar
• Odacı E, Özyılmaz C (2015). Exposure to a 900 MHz electromagnetic field for one hour a day over 30 days does change the histopathology and biochemistry of the rat testis. Int. J. Radiat. Biol. DOI:10.3109/09553002.2015.1031850.
   PubMed Web of Science ®Google Scholar
• Odaci E, Bas O, Kaplan S (2008) Effects of prenatal exposure to a 900 MHz electromagnetic field on the dentate gyrus of rats: a stereological and histopathological study. Brain Res. 1238: 224–229.
   PubMed Web of Science ®Google Scholar
• Odacı E, İkinci A, Yıldırım M, Kaya H, Akça M, Hancı H, Sönmez OF, Aslan A, Okuyan M, Baş O (2013) The effects of 900 megahertz electromagnetic field applied in the prenatal period on spinal cord morphology and motor behavior in female rat pups. NeuroQuantology 11: 573–581.
   Web of Science ®Google Scholar
• Odacı E, Ünal D, Mercantepe T, Topal Z, Hancı H, Türedi S, Erol HS, Mungan S, Kaya H, Çolakoğlu S (2015) The pathological effects of prenatal exposure to a 900-MHz electromagnetic field on the 21-day-old male rat kidney. Biotech. & Histochem. 90: 93–101.
   PubMed Web of Science ®Google Scholar
• Ozguner M, Koyu A, Cesur G, Ural M, Ozguner F, Gokcimen A, Delibas N (2005) Biological and morphological effects on the reproductive organ of rats after exposure to electromagnetic field. Saudi Med. J. 26: 405–410.
   PubMed Web of Science ®Google Scholar
• Poulletier de Gannes F, Haro E, Hurtier A, Taxile M, Athane A, Ait-Aissa S, Masuda H, Percherncier Y, Ruffié G, Billaudel B, Dufour P, Veyret B, Lagroye I (2012) Effect of in utero Wi-Fi exposure on the pre- and postnatal development of rats. Birth Def. Res. B. Dev. Reprod. Toxicol. 95: 130–136.
   PubMed Web of Science ®Google Scholar
• Ramadan LA, Abd-Allah AR, Aly HA, Saad-el-Din AA (2002) Testicular toxicity effects of magnetic field exposure and prophylactic role of coenzyme Q10 and L-carnitine in mice. Pharmacol. Res. 46: 363–370.
   PubMed Web of Science ®Google Scholar
• Roychoudhury S, Jedlicka J, Parkanyi V, Rafay J, Ondruska L, Massanyi P, Bulla J (2009) Influence of a 50 Hz extra low frequency electromagnetic field on spermatozoa motility and fertilization rates in rabbits. J. Environ. Sci. Health A Tox. Hazard Subst. Environ. Eng. 44: 1041–1047.
   PubMed Web of Science ®Google Scholar
• Ryan BM, Symanski RR, Pomeranz LE, Johnson TR, Gauger JR, McCormick DL (1999) Multigeneration reproductive toxicity assessment of 60-Hz magnetic fields using a continuous breeding protocol in rats. Teratology 59: 156–162.
   PubMedGoogle Scholar
• Saito K, Suzuki H, Suzuki K (2006) Teratogenic effects of static magnetic field on mouse fetuses. Reprod. Toxicol. 22: 118–124.
   PubMed Web of Science ®Google Scholar
• Sankako MK, Garcia PC, Piffer RC, Dallaqua B, Damasceno DC, Pereira OC (2012) Possible mechanism by which zinc protects the testicular function of rats exposed to cigarette smoke. Pharmacol. Rep. 64: 1537–1546.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Ali S, Behari J (1994) Effect of low power microwave on the mouse genome: a direct DNA analysis. Mutat. Res. 320: 141–147.
   PubMed Web of Science ®Google Scholar
• Saygin M, Caliskan S, Karahan N, Koyu A, Gumral N, Uguz A (2011) Testicular apoptosis and histopathological changes induced by a 2.45 GHz electromagnetic field. Toxicol. Ind. Health 27: 455–463.
   PubMed Web of Science ®Google Scholar
• Shoji H, Koletzko B (2007) Oxidative stress and antioxidant protection in the perinatal period. Curr. Opin. Clin. Nutr. Metab. Care 10: 324–328.
   PubMed Web of Science ®Google Scholar
• Sonmez OF, Odaci E, Bas O, Kaplan S (2010) Purkinje cell number decreases in the adult female rat cerebellum following exposure to 900 MHz electromagnetic field. Brain Res. 1356: 95–101.
   PubMed Web of Science ®Google Scholar
• Tas M, Dasdag S, Akdag MZ, Cirit U, Yegin K, Seker U, Ozmen MF, Eren LB (2014) Long-term effects of 900 MHz radiofrequency radiation emitted from mobile phone on testicular tissue and epididymal semen quality. Electromag. Biol. Med. 33:216–222.
   PubMed Web of Science ®Google Scholar
• Tenorio BM, Jimenez GC, Morais RN, Torres SM, Nogueira RA, Junior VAS (2011) Testicular development evaluation in rats exposed to 60 Hz and 1 mT electro-magnetic field. J. Appl. Toxicol. 31: 223–230.
   PubMed Web of Science ®Google Scholar
• Tenorio BM, Jimenez GC, Morais RN, Peixoto CA, de Albuquerque NR, da Silva VA Jr (2012) Evaluation of testicular degeneration induced by low-frequency electromagnetic fields. J. Appl. Toxicol. 32: 210–218.
   PubMed Web of Science ®Google Scholar
• Topal Z, Hancı H, Mercantepe T, Erol HS, Keleş ON, Kaya H, Mungan S, Odacı E (2014) The effects of prenatal long-duration exposure to 900 megahertz electromagnetic field on the 21-day old newborn male rat liver. Turk. J. Med. Sci. 45:291–297.
   Web of Science ®Google Scholar
• Türedi S, Hancı H, Topal Z, Ünal D, Mercantepe T, Bozkurt İ, Kaya H, Odacı E (2014) The effects of prenatal exposure to a 900-MHz electromagnetic field on the 21-day-old male rat heart. Electromag. Biol. Med. DOI:10.3109/15368378.2014.952742.
   PubMed Web of Science ®Google Scholar
• Uchiyama M, Mihara M (1978) Determination of malondialdehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem. 86: 271–278.
   PubMed Web of Science ®Google Scholar
• Urso ML, Clarkson PM (2003) Oxidative stress, exercise, and antioxidant supplementation. Toxicology 189: 41–54.
   PubMed Web of Science ®Google Scholar
• Wiseman H, Halliwell B (1996) Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J. 313: 17–29.
   PubMed Web of Science ®Google Scholar
• Yagi K (1994) Lipid peroxides and related radicals in clinical medicine. In: Armstrong D, Ed., Free Radicals in Diagnostic Medicine. Plenum Press, New York. pp. 1–15.
   Google Scholar
• Yin Y, Hawkins KL, Devvolf WC, Morgantaler A (1997) Heat stress causes testicular germ cell apoptosis in adult mice. J. Androl. 18: 159–165.
   PubMed Web of Science ®Google Scholar
• Zhao TY, Zou SP, Knapp PE (2007) Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. Neurosci. Lett. 412: 34–38.
   PubMed Web of Science ®Google Scholar