DOI: http://dx.doi.org/10.14704/nq.2013.11.4.699
http://www.neuroquantology.com/index.php/journal/article/view/699
The Effects of Prenatal Exposure to a 900 Megahertz Electromagnetic Field on Hippocampus Morphology and Learning Behavior in Rat Pups
Abstract
The purpose of this study was to examine the effect on hippocampus morphology and learning behavior in rat pups following prenatal exposure to a 900 megahertz (MHz) electromagnetic field (EMF). Female Sprague Dawley rats weighing 180-250 g were left to mate with males. The following day, pregnant rats identified as such by the vaginal smear test were divided into two groups, control (n=3) and EMF (n=3). No procedures were performed on the control group. The rats in the EMF group were exposed to 900 MHz EMF on days 13 to 21 of pregnancy, for 1 h a day. Female rat pups were removed from their mothers at 22 days old. We then established two newborn rat groups, a 13 member control group and a 10 member EMF group. Radial arm maze and passive avoidance tests were used to measure rat pups’ learning and memory performance. All rats were decapitated on the postnatal 32nd day. Routine histological procedures were performed on the brain tissues, and sections were stained with Cresyl fast violet. The radial arm maze (p=0.007) and passive avoidance (p=0.032) tests were administered to both groups under identical conditions, and compromised learning behavior was determined in the EMF group rats. Morphological compromise was also determined in the EMF group sections. Our results show that the application of a 900 MHz EMF in the prenatal period adversely affected female pups’ learning behavior and also resulted in histopathological changes appearing in the hippocampus.
NeuroQuantology | December 2013 | Volume 11 | Issue 4 | Page 582-590
NeuroQuantology | December 2013 | Volume 11 | Issue 4 | Page 582-590
Keywords
newborn female rats; hippocampus; electromagnetic field; learning behavior
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References
Aktürk Z, Odacı E, İkinci A, Baş O, Canpolat S, Çolakoğlu S, Sönmez OF. Effect of Ginkgo biloba on brain volume after carotid artery occlusion in rats: a stereological and histopathological study. Turk J Med Sci DOI: 10.3906/sag-1305-40.
Ammari M, Jacquet A, Lecomte A, Sakly M, Abdelmelek H, de Seze R. Effect of head-only sub-chronic and chronic exposure to 900-MHz GSMelectromagnetic fields on spatial memory in rats. Brain Inj 2008; 22(13-14): 1021-9.
Barcal J, Vozeh F. Effect of whole-body exposure to high-frequency electromagnetic field on the brain cortical and hippocampal activity in mouse experimental model. Neuroquantology 2007; l5(3): 292-302.
Bas O, Odaci E, Kaplan S, Acer N, Ucok K, Colakoglu S. 900 MHz electromagnetic field exposure affects qualitative and quantitative features of hippocampal pyramidal cells in the adult female rat. Brain Res 2009a; 1265: 178-85.
Bas O, Odaci E, Mollaoglu H, Ucok K, Kaplan S. Chronic prenatal exposure to the 900 megahertz electromagnetic field induces pyramidal cell loss in the hippocampus of newborn rats. Toxicol Ind Health 2009b; 25(6): 377-84.
Bornhausen M, Scheingraber H. Prenatal exposure to 900 MHz, cell-phone electromagnetic fields had no effect on operant-behavior performances of adult rats. Bioelectromagnetics 2000; 21(8): 566-74.
Christ A, Gosselin MC, Christopoulou M, Kuhn S, Kuster N. Age-dependent tissue-specific exposure of cell phone users. Phys Med Biol 2010; 55(7): 1767-1783.
Corle C, Makale M, Kesari S. Cell phones and glioma risk: a review of the evidence. J Neurooncol 2012; 106(1): 1-13.
Dobbing J. Undernutrition and the developing brain: the relevance of animal models to the human problem. Am J Dis Child 1970; 120: 411-415.
Dobbing J, Sands J. Quantitative growth and development of human brain. Arch Dis Child 1973; 48: 757-767.
Dubreuil D, Jay T, Edeline JM. Does head-only exposure to GSM-900 electromagnetic fields affect the performance of rats in spatial learning tasks? Behav Brain Res 2002; 129(1-2): 203-10.
Dubreuil D, Jay T, Edeline JM. Head-only exposure to GSM 900-MHz electromagnetic fields does not alter rat’s memory in spatial and non-spatial tasks. Behav Brain Res 2003; 145: 51-61.
Hancı H, Odacı E, Kaya H, Aliyazıcıoğlu Y, Turan I, Demir S, Colakoğlu S. The effect of prenatal exposure to 900-MHz electromagnetic field on the 21-old-day rat testicle. Reprod Toxicol 2013;42C:203-209. doi: 10.1016/j.reprotox.2013.09.006.
Hardell L, Näsman A, Påhlson A, Hallquist A, Hansson Mild K. Use of cellular telephones and the risk for brain tumours: a case-control study. Int J Oncol 1999; 15(1); 113-116.
Hardell L, Carlberg M, Hansson Mild K. Pooled analysis of two case-control studies on use of cellular and cordless telephones and the risk for malignant brain tumours diagnosed in 1997–2003. Int Arch Occup Environ Health 2006; 79(8): 630-9.
Hardell L, Carlberg M, Söderqvist F, Mild KH, Morgan LL. Long-term use of cellular phones and brain tumours: increased risk associated with use for Nor =10 years. Occup Environ Med 2007; 64(9): 626-32.
Hietanen M. Establishing the health risks of exposure to radiofrequency fields requires multidisciplinary research. Scand J Work Environ Health 2006; 32(3): 169-70.
Hao D, Yang L, Chen S, Tong J, Tian Y, Su B, Wu S, Zeng Y. Effects of long-term electromagnetic field exposure on spatial learning and memory in rats. Neurol Sci 2013; 34(2): 157-64.
İkinci A, Odacı E, Baş O. Effects of ethyl pyruvate administration on female rats’ pyramidal cells of cornu ammonis after brain ischemia: a stereological and histopathological study. Turk J Med Sci 2013; 43(3): 354-361.
Jacobson M. Histogenesis and morphogenesis of cortical structures. In: Jacobson, M (ed), Developmental Neurobiology. Third ed. New York: Plenum Press 1991; 401-451.
Kaplan S, Odacı E, Canan S, Onger ME, Aslan H, Ünal B. The Disector counting technique. Neuroquantology 2012a; 10: 44-53.
Kaplan S, Canan S, Altunkaynak ME, Odacı E, Aslan H, Unal B. An unbiased way to estimate total quantities: the fractionator technique. Neuroquantology 2012b; 10: 54-65.
Koyu A, Cesur G, Ozguner F, Akdogan M, Mollaoglu H, Ozen S. Effects of 900 MHz electromagnetic field on TSH and thyroid hormones in rats. Toxicol Lett 2005; 157(3): 257-62.
Kumlin T, Iivonen H, Miettinen P, Juvonen A, van Groen T, Puranen L, Pitkäaho R, Juutilainen J, Tanila H. Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat Res 2007; 168(4): 471-9.
Lenhart A, Ling R, Campbell SW, Purcell K. Teens and mobile phones. A project of the Pew Research Center and the University of Michigan. Available at http://www.pewinternet.org/ Reports/2010/Teens-and-Mobile-Phones.aspx
Maskey D, Kim M, Aryal B, Pradhan J, Choi IY, Park KS, Son T, Hong SY, Kim SB, Kim HG, Kim MJ. Effect of 835 MHz radiofrequency radiation exposure on calcium binding proteins in the hippocampus of the mouse brain. Brain Res 2010; 1313: 232-41.
Mausset AL, de Seze R, Montpeyroux F, Privat A. Effects of radiofrequency exposure on the GABAergic system in the rat cerebellum: clues from semiquantitative immunohistochemistry. Brain Res 2001; 912: 33-46.
Mausset AL, Hirbec H, Bonnefont X, Privat A, Vignon J, de Seze R. Acute exposure to GSM 900-MHz electromagnetic fields induces glial reactivity and biochemical modifications in the rat brain. Neurobiol Dis 2004; 17: 445-454.
Narayanan SN, Kumar RS, Potu BK, Nayak S, Mailankot M. Spatial memory performance of Wistar rats exposed to mobile phone. Clinics (Sao Paulo) 2009; 64(3): 231-4.
Nittby H, Grafström G, Tian DP, Malmgren L, Brun A, Persson BR, Salford LG, Eberhardt J. Cognitive impairment in rats after long-term exposure to GSM-900 mobile phone radiation. Bioelectromagnetics 2008; 29(3): 219-32.
Odaci E, Kaplan S, Sahin B, Bas O, Gevrek F, Aygun D, Unal B, Sonmez OF, Colakoglu S, Bilgic S. Effects of low-dose oxcarbazepine administration on developing cerebellum in newborn rat: A stereological study. Neuroscience Research Communications 2004; 34(1): 28-36.
Odaci E, Bas O, Kaplan S. Effects of prenatal exposure to a 900 MHz electromagnetic field on the dentate gyrus of rats: a stereological and histopathological study. Brain Res 2008; 1238: 224-9.
Panagopoulos DJ, Chavdoula ED, Nezis IP, Margaritis LH. Cell death induced by GSM 900-MHz and DCS 1800-MHz mobile telephony radiation. Mutat Res 2007; 626(1-2): 69-78.
Rodier PM. Chronology of neuron development: animal studies and their clinical implications. Dev Med Child Neurol 1980; 22(4): 525-45.
Sakatani S, Okada YC, Hirose A. A quantitative evaluation of dominant membrane potential in generation of magnetic field using a pyramidal cell model at hippocampus CA3. Neurocomputing 2002; 44: 153-160.
Salford LG, Brun AE, Eberhardt JL, Malmgren L, Persson BR. Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ Health Perspect 2003; 111: 881-883.
Savignac HM, Dinan TG, Cryan JF. Resistance to early-life stress in mice: effects of genetic background and stress duration. Front Behav Neurosci 2011; 5: 13.
Sienkiewicz ZJ, Blackwell RP, Haylock RG, Saunders RD, Cobb BL. Low-level exposure to pulsed 900 MHz microwave radiation does not cause deficits in the performance of a spatial learning task in mice. Bioelectromagnetics 2000; 21(3): 151-8.
Sonmez OF, Odaci E, Bas O, Kaplan S. Purkinje cell number decreases in the adult female rat cerebellum following exposure to 900 MHz electromagnetic field. Brain Res 2010; 1356: 95-101.
Tunc AT, Aslan H, Turgut M, Ekici F, Odaci E, Kaplan S. Inhibitory effect of pinealectomy on the development of cerebellar granule cells in the chick: a stereological study. Brain Res 2007; 1138: 214-220.
Yildirim M, Abidin I, Cansu A. Effects of chronic treatment with commonly used antiepileptic drugs on passive avoidance learning in prepubertal rats. J Exp Clin Med 2013; 30: 57-61.
Yildirim M, Marangoz C. Effects of nitric oxide on passive avoidance learning in rats. Int J Neurosci 2004; 114(5): 597-606.
Weinstock M. Alterations induced by gestational stres in brain morphology and behaviour of the offspring. Prog Neurobiol 2001; 65(5): 427-51.
Wigle DT, Arbuckle TE, Turner MC, Brub A, Yang Q, Liu S, Krewski D. Epidemiologic Evidence of Relationships Between Reproductive and Child Health Outcomes and Environmental. Chemical Contaminants, Journal of Toxicology and Environmental Health, Part B: Critical Reviews 2008; 11: 5-6, 373-517.
Aktürk Z, Odacı E, İkinci A, Baş O, Canpolat S, Çolakoğlu S, Sönmez OF. Effect of Ginkgo biloba on brain volume after carotid artery occlusion in rats: a stereological and histopathological study. Turk J Med Sci DOI: 10.3906/sag-1305-40.
Ammari M, Jacquet A, Lecomte A, Sakly M, Abdelmelek H, de Seze R. Effect of head-only sub-chronic and chronic exposure to 900-MHz GSMelectromagnetic fields on spatial memory in rats. Brain Inj 2008; 22(13-14): 1021-9.
Barcal J, Vozeh F. Effect of whole-body exposure to high-frequency electromagnetic field on the brain cortical and hippocampal activity in mouse experimental model. Neuroquantology 2007; l5(3): 292-302.
Bas O, Odaci E, Kaplan S, Acer N, Ucok K, Colakoglu S. 900 MHz electromagnetic field exposure affects qualitative and quantitative features of hippocampal pyramidal cells in the adult female rat. Brain Res 2009a; 1265: 178-85.
Bas O, Odaci E, Mollaoglu H, Ucok K, Kaplan S. Chronic prenatal exposure to the 900 megahertz electromagnetic field induces pyramidal cell loss in the hippocampus of newborn rats. Toxicol Ind Health 2009b; 25(6): 377-84.
Bornhausen M, Scheingraber H. Prenatal exposure to 900 MHz, cell-phone electromagnetic fields had no effect on operant-behavior performances of adult rats. Bioelectromagnetics 2000; 21(8): 566-74.
Christ A, Gosselin MC, Christopoulou M, Kuhn S, Kuster N. Age-dependent tissue-specific exposure of cell phone users. Phys Med Biol 2010; 55(7): 1767-1783.
Corle C, Makale M, Kesari S. Cell phones and glioma risk: a review of the evidence. J Neurooncol 2012; 106(1): 1-13.
Dobbing J. Undernutrition and the developing brain: the relevance of animal models to the human problem. Am J Dis Child 1970; 120: 411-415.
Dobbing J, Sands J. Quantitative growth and development of human brain. Arch Dis Child 1973; 48: 757-767.
Dubreuil D, Jay T, Edeline JM. Does head-only exposure to GSM-900 electromagnetic fields affect the performance of rats in spatial learning tasks? Behav Brain Res 2002; 129(1-2): 203-10.
Dubreuil D, Jay T, Edeline JM. Head-only exposure to GSM 900-MHz electromagnetic fields does not alter rat’s memory in spatial and non-spatial tasks. Behav Brain Res 2003; 145: 51-61.
Hancı H, Odacı E, Kaya H, Aliyazıcıoğlu Y, Turan I, Demir S, Colakoğlu S. The effect of prenatal exposure to 900-MHz electromagnetic field on the 21-old-day rat testicle. Reprod Toxicol 2013;42C:203-209. doi: 10.1016/j.reprotox.2013.09.006.
Hardell L, Näsman A, Påhlson A, Hallquist A, Hansson Mild K. Use of cellular telephones and the risk for brain tumours: a case-control study. Int J Oncol 1999; 15(1); 113-116.
Hardell L, Carlberg M, Hansson Mild K. Pooled analysis of two case-control studies on use of cellular and cordless telephones and the risk for malignant brain tumours diagnosed in 1997–2003. Int Arch Occup Environ Health 2006; 79(8): 630-9.
Hardell L, Carlberg M, Söderqvist F, Mild KH, Morgan LL. Long-term use of cellular phones and brain tumours: increased risk associated with use for Nor =10 years. Occup Environ Med 2007; 64(9): 626-32.
Hietanen M. Establishing the health risks of exposure to radiofrequency fields requires multidisciplinary research. Scand J Work Environ Health 2006; 32(3): 169-70.
Hao D, Yang L, Chen S, Tong J, Tian Y, Su B, Wu S, Zeng Y. Effects of long-term electromagnetic field exposure on spatial learning and memory in rats. Neurol Sci 2013; 34(2): 157-64.
İkinci A, Odacı E, Baş O. Effects of ethyl pyruvate administration on female rats’ pyramidal cells of cornu ammonis after brain ischemia: a stereological and histopathological study. Turk J Med Sci 2013; 43(3): 354-361.
Jacobson M. Histogenesis and morphogenesis of cortical structures. In: Jacobson, M (ed), Developmental Neurobiology. Third ed. New York: Plenum Press 1991; 401-451.
Kaplan S, Odacı E, Canan S, Onger ME, Aslan H, Ünal B. The Disector counting technique. Neuroquantology 2012a; 10: 44-53.
Kaplan S, Canan S, Altunkaynak ME, Odacı E, Aslan H, Unal B. An unbiased way to estimate total quantities: the fractionator technique. Neuroquantology 2012b; 10: 54-65.
Koyu A, Cesur G, Ozguner F, Akdogan M, Mollaoglu H, Ozen S. Effects of 900 MHz electromagnetic field on TSH and thyroid hormones in rats. Toxicol Lett 2005; 157(3): 257-62.
Kumlin T, Iivonen H, Miettinen P, Juvonen A, van Groen T, Puranen L, Pitkäaho R, Juutilainen J, Tanila H. Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat Res 2007; 168(4): 471-9.
Lenhart A, Ling R, Campbell SW, Purcell K. Teens and mobile phones. A project of the Pew Research Center and the University of Michigan. Available at http://www.pewinternet.org/ Reports/2010/Teens-and-Mobile-Phones.aspx
Maskey D, Kim M, Aryal B, Pradhan J, Choi IY, Park KS, Son T, Hong SY, Kim SB, Kim HG, Kim MJ. Effect of 835 MHz radiofrequency radiation exposure on calcium binding proteins in the hippocampus of the mouse brain. Brain Res 2010; 1313: 232-41.
Mausset AL, de Seze R, Montpeyroux F, Privat A. Effects of radiofrequency exposure on the GABAergic system in the rat cerebellum: clues from semiquantitative immunohistochemistry. Brain Res 2001; 912: 33-46.
Mausset AL, Hirbec H, Bonnefont X, Privat A, Vignon J, de Seze R. Acute exposure to GSM 900-MHz electromagnetic fields induces glial reactivity and biochemical modifications in the rat brain. Neurobiol Dis 2004; 17: 445-454.
Narayanan SN, Kumar RS, Potu BK, Nayak S, Mailankot M. Spatial memory performance of Wistar rats exposed to mobile phone. Clinics (Sao Paulo) 2009; 64(3): 231-4.
Nittby H, Grafström G, Tian DP, Malmgren L, Brun A, Persson BR, Salford LG, Eberhardt J. Cognitive impairment in rats after long-term exposure to GSM-900 mobile phone radiation. Bioelectromagnetics 2008; 29(3): 219-32.
Odaci E, Kaplan S, Sahin B, Bas O, Gevrek F, Aygun D, Unal B, Sonmez OF, Colakoglu S, Bilgic S. Effects of low-dose oxcarbazepine administration on developing cerebellum in newborn rat: A stereological study. Neuroscience Research Communications 2004; 34(1): 28-36.
Odaci E, Bas O, Kaplan S. Effects of prenatal exposure to a 900 MHz electromagnetic field on the dentate gyrus of rats: a stereological and histopathological study. Brain Res 2008; 1238: 224-9.
Panagopoulos DJ, Chavdoula ED, Nezis IP, Margaritis LH. Cell death induced by GSM 900-MHz and DCS 1800-MHz mobile telephony radiation. Mutat Res 2007; 626(1-2): 69-78.
Rodier PM. Chronology of neuron development: animal studies and their clinical implications. Dev Med Child Neurol 1980; 22(4): 525-45.
Sakatani S, Okada YC, Hirose A. A quantitative evaluation of dominant membrane potential in generation of magnetic field using a pyramidal cell model at hippocampus CA3. Neurocomputing 2002; 44: 153-160.
Salford LG, Brun AE, Eberhardt JL, Malmgren L, Persson BR. Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ Health Perspect 2003; 111: 881-883.
Savignac HM, Dinan TG, Cryan JF. Resistance to early-life stress in mice: effects of genetic background and stress duration. Front Behav Neurosci 2011; 5: 13.
Sienkiewicz ZJ, Blackwell RP, Haylock RG, Saunders RD, Cobb BL. Low-level exposure to pulsed 900 MHz microwave radiation does not cause deficits in the performance of a spatial learning task in mice. Bioelectromagnetics 2000; 21(3): 151-8.
Sonmez OF, Odaci E, Bas O, Kaplan S. Purkinje cell number decreases in the adult female rat cerebellum following exposure to 900 MHz electromagnetic field. Brain Res 2010; 1356: 95-101.
Tunc AT, Aslan H, Turgut M, Ekici F, Odaci E, Kaplan S. Inhibitory effect of pinealectomy on the development of cerebellar granule cells in the chick: a stereological study. Brain Res 2007; 1138: 214-220.
Yildirim M, Abidin I, Cansu A. Effects of chronic treatment with commonly used antiepileptic drugs on passive avoidance learning in prepubertal rats. J Exp Clin Med 2013; 30: 57-61.
Yildirim M, Marangoz C. Effects of nitric oxide on passive avoidance learning in rats. Int J Neurosci 2004; 114(5): 597-606.
Weinstock M. Alterations induced by gestational stres in brain morphology and behaviour of the offspring. Prog Neurobiol 2001; 65(5): 427-51.
Wigle DT, Arbuckle TE, Turner MC, Brub A, Yang Q, Liu S, Krewski D. Epidemiologic Evidence of Relationships Between Reproductive and Child Health Outcomes and Environmental. Chemical Contaminants, Journal of Toxicology and Environmental Health, Part B: Critical Reviews 2008; 11: 5-6, 373-517.
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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.http://www.neuroquantology.com/index.php/journal/article/view/699
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