Research Article
Testicular development evaluation in rats exposed to 60 Hz and 1 mT electromagnetic field
Bruno Mendes Tenorio,
George Chaves Jimenez,
Rosana Nogueira Morais,
Sandra Maria Torres,
Romildo Albuquerque Nogueira,
Valdemiro Amaro Silva Junior,
Bruno Mendes Tenorio
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorGeorge Chaves Jimenez
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorRosana Nogueira Morais
Federal University of Paraná, Department of Physiology, Curitiba, Brazil
Search for more papers by this authorSandra Maria Torres
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorRomildo Albuquerque Nogueira
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorCorresponding Author
Valdemiro Amaro Silva Junior
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, BrazilSearch for more papers by this author
Bruno Mendes Tenorio,
George Chaves Jimenez,
Rosana Nogueira Morais,
Sandra Maria Torres,
Romildo Albuquerque Nogueira,
Valdemiro Amaro Silva Junior,
Bruno Mendes Tenorio
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorGeorge Chaves Jimenez
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorRosana Nogueira Morais
Federal University of Paraná, Department of Physiology, Curitiba, Brazil
Search for more papers by this authorSandra Maria Torres
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorRomildo Albuquerque Nogueira
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Search for more papers by this authorCorresponding Author
Valdemiro Amaro Silva Junior
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, Brazil
Federal Rural University of Pernambuco, Department of Animal Morphology and Physiology, Recife, BrazilSearch for more papers by this authorAbstract
Society has been increasingly exposed to low-frequency electromagnetic fields (EMF), mainly from electricity distribution networks and electro-electronic devices. Aiming to clarify the extension of possible interactions between EMF and testicular development, this study evaluated the effects of exposure to 60 Hz and 1 mT EMF in the maturation of testicular components. Wistar rats were exposed to EMF three times per day for 30 min, between the 13th day of gestation and the 21st postnatal day. Results showed a decrease in the following parameters: tubular diameter and seminiferous tubules area; seminiferous epithelium height; total volume of seminiferous tubule; tubular lumen; seminiferous epithelium; and Leydig cells. On the other hand, an increase was observed in connective tissue cells and blood vessels volume. Plasma testosterone, Sertoli cells population, tubular length and gonadosomatic index did not change when exposed to EMF. Histomorphometric analysis showed that exposure to EMF can promote a delay in testicular development. Copyright © 2010 John Wiley & Sons, Ltd.
REFERENCES
- 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.
- Al-Akhras MA, Darmani H, Elbetieha A. 2006. Influence of 50 Hz magnetic field on sex hormones and other fertility parameters of adult male rats. Bioelectromagnetics 27: 127–131.
- Aydin M, Turk G, Yuksel M, Cevik A, Apaydin, AM, Yilmaz S. 2007. Effect of electromagnetic field on the sperm characteristics and histopathological status of testis in rats. Medyc. Weteryn. 63: 178–183.
- Boorman GA, Mccormick DL, Findlay JC, Hailey JR, Gauger JR, Johnson TR, Kovatch RM, Sills RC, Haseman JK. 1999. Chronic toxicity/oncogenicity evaluation of 60 Hz (power frequency) magnetic fields in F344/N rats. Toxicol. Pathol. 27: 267–278.
- Brown J, Walker SE, Steinmain K. 2004. Endocrine Manual for the Reproductive Assessment of Domestic and Non-domestic Species. Smithsonian's National Zoological Park, Front Royal: Virginia–EUA.
- Cecconi S, Gualtieri G, Di Bartolomeo A, Troiani G, Cifone MG, Canipari R. 2000. Evaluation of effects of extremely low frequency electromagnetic fields on mammalian follicle development. Hum. Reprod. 15: 2319–2325.
- Chung MK, Kim JC, Myung SH, Lee DI. 2003. Developmental toxicity evaluation of ELF magnetic fields in Sprague–Dawley Rats. Bioelectromagnetics. 24: 231–240.
- 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.
- De Vita R, Cavallo D, Raganella L, Eleuteri P, Grollino MG, Calugi A. 1995. Effects of 50 Hz magnetic field on mouse spermatogenesis monitored by flow cytometric analysis. Bioelectromagnetics. 16: 330–334.
- Ewing LL, Keeney DS. 1993. Leydig cell: structure and function. In Cell and Molecular Biology of the Testis, C Desjardins, LL Ewing (eds). Oxford University Press: New York; 137–165.
- Forgács Z, Somosy Z, Kubinyi G, Sinay H, Bakos J, Thuróczy G, Surján A, Hudák A, Olajos F, Lázár P. 2004. Effects of whole-body 50-Hz magnetic field exposure on mouse Leydig cells. Sci. World J. 4: 83–90.
- França LR, Chiarini-Garcia H. 2005. Célula de Sertoli. In Células uma abordagem multidisciplinar, Carvalho HF, Collares-Buzato CB (eds). Editora Manole: Barueri-SP; 302–324.
- França LR, Avelar GF, Almeida FFL. 2005. Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63: 300–318.
- Gassler N, Rohr C, Schnneider A, Kartembeck J, Bach A, Obermuller N, Otto HF, Autschbach F. 2001. Inflammatory bowel disease is associated with changes of enterocytic junctions. Am. J. Physiol. Gastrointest. Liver Physiol. 281: 216–228.
- Griswold MD. 1998. The central role of Sertoli cells in spermatogenesis. Cell Devl. Biol. 9: 411–416.
- Heredia-Rojas JA, Caballero-Hernandez DE, Rodriguez AOLF, Ramos-Alfano G, Rodriguez-Flores LE. 2004. Lack of alterations on meiotic chromosomes and morphological characteristics of male germ cells in mice exposed to a 60 Hz and 2.0 mT magnetic field. Bioelectromagnetics. 25: 63–68.
- Holstein AF, Schulze W, Davidoff M. 2003. Understanding spermatogenesis is a prerequisite for treatment. Reprod. Biol. Endocrinol. 1: 107.
- 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.
- Jegóu B. 1992. The Sertoli cell in vivo and in vitro. Cell Biol. Toxicol. 8: 49–54.
- Kato M, Honma K, Shigemitsu T, Shiga Y. 1994. Circularly polarized, sinuzoidal, 50 Hz magnetic field exposure does not influence plasma testosterone levels of rats. Bioelectromagnetics 15: 513–518.
- Kheifets L, Repacholi K, Saunders R, Van Deventer E. 2005. The sensitivity of children to electromagnetic fields. Pediatrics 116: 303–313.
- Kim YW, Kim HS, Lee JS, Kim YJ, Lee, SK, Seo JN, Jung KC, Kim N, Gimm YM. 2009. Effects of 60 Hz 14 mT magnetic field on the apoptosis of testicular germ cell in mice. Bioelectromagnetics 30: 66–72.
- Kumar S. 2004. Occupational exposure associated with reproductive dysfunction. J. Occup. Health 46: 1–19.
- Kwee S, Raskmark P. 1998. Changes in cell proliferation due to environmental non-ionizing radiation 2. Microwave radiation. Bioelectrochem. Bioenerg. 44: 251–255.
- Lednev VV. 1995. Interference with the vibrational energy sublevels of ions bound in calcium-binding proteins as the basis for the interaction of weak magnetic fields with biological systems. In On the Nature of Electromagnetic Field Interactions with Biological Systems, AH Frey. (ed.). Springer-Verlaag: New York; 59–72.
- 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.
- Li DK, Yan B, Li Z, Gao E, Miao M, Gong D, Weng XP, Ferber JR, Yuan W. 2010. Exposure to magnetic fields and the risk of poor sperm quality. Reprod. Toxicol. 29: 86–92.
- Manikonda PK, Rajendra P, Devendranath D, Gunasekaran B, Channakeshava, Aradhya RSS, Sashidhar RB, Subramanyam C. 2007. Influence of extremely low frequency magnetic fields on Ca2+ signaling and NMDA receptor functions in rat hippocampus. Neurosci. Lett. 413: 145–149.
- McGivern RF, Sokol RZ, Adey WR. 1990. Prenatal exposure to a low-frequency electromagnetic field demasculinizes adult scent marking behavior and increases accessory sex organ weights in rats. Teratology 41: 1–8.
- Mendis-Hadagama SMLC, Zirkin BR, Ewing LL. 1988. Comparison of components of the interstitium with testosterone secretion in hamster; rat and guinea pig testes perfused in vitro. Am. J. Anat. 181: 12–22.
- Negishi T, Imai S, Itabashi M, Nishimura I, Sasano T. 2002. Studies of 50 Hz circularly polarized magnetic fields of up to 350 µT on reproduction and embryo-fetal development in rats: exposure during organogenesis or during preimplantation. Bioelectromagnetics. 23: 369–389.
- Nusrat A, Parkos CA, Verkade P, Foley CS, Liang TW, Innis-Whitehouse W, Eastburn KK, Madara JL. 2000a. Tight junctions are membrane microdomains. J. Cell Sci. 113: 1771–1781.
- Nusrat A, Turner JR, Madara JL. 2000b. Regulation of tigth junctions by extracelular stimuli: nutrients, cytokines, and immune cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279: 851–857.
- Orth J. 1982. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative and autoradiographic study. Anat. Rec. 203: 485–492.
- Orth JM. 1993. Cell biology of testicular development in fetus and neonate. In Cell and Molecular Biology of the Testis, C Desjardins, LL Ewing (eds), 1st edn. Oxford University Press: New York; 3–42.
- Pelletier RM. 1998. Blood–tissue barriers in the male reproductive system. In Male Reproduction: a Multidisciplinary Overview, FM Martínez-García, J Regadera (eds). Churchill Communications Europe España: Madrid; 183–195.
- Ramadan LA, Abd-Allah ARA, Aly HAA, Saad-El-Din AA. 2002. Testicular toxicity effects of magnetic field exposure and prophylactic role of coenzime q10 and l-carnitine in mice. Pharmacol. Res. 46: 363–370.
- Robert, R. 2003. Bobina de Helmholtz. Rev. Bras. Ens. Fís. 25: 40–44.
10.1590/S1806-11172003000100005 Google Scholar
- Rocha DCM, Debeljuk L, França LR. 1999. Exposure to constant light during testis development increase daily sperm production in adult Wistar rats. Tissue Cell 31: 372–379.
- Ross AJ, Capel B. 2005. Signaling at the crossroads of gonad development. Trends Endocrinol. Metab. 16: 19–25.
- Rusovan A, Kanje M. 1992. D600, a Ca++ antagonist, prevents stimulation of nerve regeneration by magnetic fields. Neuroreport 3: 813–814.
- Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. 1990. Mammalian spermatogenesis. In Histological and Histopathological Evaluation of the Testis, LD Russell, RA Ettlin, AP Sinha Hikim, ED Clegg (eds). Cache River Press: Bolesta; 1–40.
- Russell LD, França LR. 1995. Building a testis. Tissue Cell 27: 129–147.
- 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.
10.1002/(SICI)1096-9926(199903)59:3<156::AID-TERA7>3.0.CO;2-B CASPubMedWeb of Science®Google Scholar
- Saha C, Nigan SK, Denker BM. 2001. Expanding role of G proteins in tigth junction regulation: Galpha(s) stimulates Tj assembly. Biochem. Biophys. Res. Commun. 13: 25–66.
- Saito K, Suzuki H, Suzuki K. 2006. Teratogenic effects of static magnetic field on mouse fetuses. Reprod. Toxicol. 22: 118–124.
- Silva Jr VA, Vieira ACS, Pinto CF, De Paula TAR, Palma MB, Amorin MJAAL, AA Amorin Jr AA, Manhães-De-Castro R. 2006. Neonatal treatment with naloxone increases the population of sertoli cells and sperm production in adult rats. Reprod. Nutr. Dev. 46: 157–166.
- Sliney DH, Patterson RM. 2010. Guidelines for exposure to sub-radiofrequency electric and magnetic fields; http://www.irpa.net/irpa8/cdrom/vol.1/m1_228.pdf [23.02.2010] 925–928.
- Somosy Z, Forgács Z, Bognár G, Horváth K, Horváth G. 2004. Alteration of tight and adherens junctions on 50-Hz magnetic field exposure in Madin Darby canine kidney (MDCK) cells. Sci. World J. 4: 75–82.
- Tablado L, Soler C, Núñez M, Núñez J, Pérez-Sánchez F. 2000. Development of mouse testis and epididymis following intrauterine exposure to a static magnetic field. Bioelectromagnetics 21: 19–24.
- Tepper OM, Callaghan EI, Chang RD, Galiano DK, Bhatt KA, Baharestani S, Gan J, Simon B, Hooper A, Levile JP, Gurtner GC. 2004. Electromagnetic fields increase in-vitro and in-vivo angiogenesis through endothelial release of FGF-2. FASEB J.; doi: n.10.1096/fj.03-0847fje.
- Tonini R, Baroni MD, Masala E, Micheletti M, Ferroni A, Mazzanti M. 2001. Calcium protects differentiating neuroblastoma cells during 50 Hz electromagnetic radiation. Biophys. J. 81: 2580–2589.
- Usami M, Muraki K, Iwamoto M, Ohata A, Matsushita E, Miki A. 2001. Effect of eicosanpentaenoic acid (EPA) on tigth junction permeability in intestinal monolayer cells. Clin. Nutr. 20: 351–359.
- Van Itallie CM, Balda MS, Anderson JM. 1995. Epidermal growth factor induces tyrosine phosphorylation and reorganization of the tigth junctions protein- ZO-1 in A341 cells. J. Cell Sci. 108: 1835–1842.
- Wang XW, Ding GR, Shi CH, Zhao T, Zhang J, Zeng LH, Guo GZ. 2008. Effect of electromagnetic pulse exposure on permeability of blood–testicle barrier in mice. Biomed. Environ. Sci. 21: 218–221.
- Zirkin BR, Ewing LL, Kromann N. 1980. Testosterone secretion by rat, rabbit, guinea pig, dog and hamster testes perfused in vitro: correlation with Leydig cell ultrastructure. Endocrinology 107: 1867–1874.
