938
Views
2
CrossRef citations to date
0
Altmetric
Review Article

The role of non-ionizing electromagnetic radiation on female fertility: A review

, , & ORCID Icon
Pages 358-373 | Received 07 Jul 2021, Accepted 13 Jan 2022, Published online: 08 Feb 2022

References

  • Aburawi S, Abusaida H, El Jaafari H, Alkayed F, Shibani N, Dali A, Shalabi, S, Ayad, M, Altaboni O. 2020. Effect of mobile phone radiation on reproductive system and behavior using female albino mice. doi:10.5281/zenodo.4289221–AJMAS.
  • Ahmadi SS, Khaki AA, Ainehchi N, Alihemmati A, Khatooni AA, Khaki A, Asghari A. 2016. Effect of non-ionizing electromagnetic field on the alteration of ovarian follicles in rats. Electron Physician. 8(3):2168–2174. doi:10.19082/2168.
  • Ahmadi SS, Khaki AA, Alihemmati A, Rajabzadeh A, Giasi GS. 2017. The effects of 50 Hz electromagnetic fields induction of apoptosis in rat follicles. Crescent J Med Biol Sci. 4:64–68.
  • Al-Akhras MA. 2008. Influence of 50 Hz magnetic field on sex hormones and body, uterine, and ovarian weights of adult female rats. Electromagn Biol Med. 27(2):155–163. doi:10.1080/15368370802072125.
  • 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(5):340–344. doi:10.1002/bem.59.
  • Al-Asmakh M. 2007. Reproductive functions of progesterone. Middle East Fertil Soc J. 12(3):147.
  • Alekperov SI, Suetov AA, Efremov VI, Kimstach AN, Lavrenenok LV. 2019. The effect of electromagnetic fields of extremely low frequency 30 Hz on rat ovaries. Bull Exp Biol Med. 166(5):704–707. doi:10.1007/s10517-019-04422-2.
  • Asghari A, Khaki AA, Rajabzadeh A, Khaki A. 2016. A review on Electromagnetic fields (EMFs) and the reproductive system. Electron Physician. 8(7):2655–2662. doi:10.19082/2655.
  • Aydin M, Cevik A, Kandemir FM, Yuksel M, Apaydin AM. 2009. Evaluation of hormonal change, biochemical parameters, and histopathological status of uterus in rats exposed to 50-Hz electromagnetic field. Toxicol Ind Health. 25(3):153–158. doi:10.1177/0748233709102717.
  • Azimipour F, Zavareh S, Lashkarbolouki T. 2020. The effect of radiation emitted by cell phone on the gelatinolytic activity of matrix metalloproteinase-2 and -9 of mouse pre-antral follicles during in vitro culture. Cell J. 22(1):1–8. doi:10.22074/cellj.2020.6548.
  • Bagavandoss P. 1998. Differential distribution of gelatinases and tissue inhibitor of metalloproteinase-1 in the rat ovary. J Endocrinol. 158(2):221–228. doi:10.1677/joe.0.1580221.
  • Bakacak M, Bostancı MS, Attar R, Yıldırım ÖK, Yıldırım G, Bakacak Z, Sayar H, Han A. 2015. The effects of electromagnetic fields on the number of ovarian primordial follicles: an experimental study. Kaohsiung J Med Sci. 31(6):287–292. doi:10.1016/j.kjms.2015.03.004.
  • Belyaev I. 2005. Nonthermal biological effects of microwaves: current knowledge, further perspective, and urgent needs. Electromagn Biol Med. 24(3):375–403. doi:10.1080/15368370500381844.
  • 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(9):1293–1305. doi:10.1016/j.theriogenology.2009.12.010.
  • Biri A, Bozkurt N, Turp A, Kavutcu M, Himmetoglu Ö, Durak İ. 2007. Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Invest. 64(4):187–192. doi:10.1159/000106488.
  • Borhani N, Rajaei F, Salehi Z, Javadi A. 2011. Analysis of DNA fragmentation in mouse embryos exposed to an extremely low-frequency electromagnetic field. Electromagn Biol Med. 30(4):246–252. doi:10.3109/15368378.2011.589556.
  • Budani MC, Tiboni GM. 2021. Novel insights on the role of nitric oxide in the ovary: a review of the literature. Int J Environ Res Public Health. 18(3):980. doi:10.3390/ijerph18030980.
  • Burchard JF, Nguyen DH, Block E. 1998. Progesterone concentrations during estrous cycle of dairy cows exposed to electric and magnetic fields. Bioelectromagnetics. 19(7):438–443. doi:10.1002/(SICI)1521-186X(1998)19:7<438:AID-BEM6>3.0.CO;2-2.
  • Burcu A, Nevin E, Ilkay A, Amac K, Alper BH, Muge K. 2020. The effects of prenatal and postnatal exposure to electromagnetic field on rat ovarian tissue. Toxicol Ind Health. 36(12):1010–1018. doi:10.1177/0748233720973136.
  • Cao Y-N, Zhang Y, Liu Y. 2006. Effects of exposure to extremely low frequency electromagnetic fields on reproduction of female mice and development of offsprings. Chin J Ind Hyg Occup Dis. 24(8):468–470.
  • Cecconi S, Gualtieri G, Di Bartolomeo A, Troiani G, Cifone MG, Canipari R. 2000. Evaluation of the effects of extremely low frequency electromagnetic fields on mammalian follicle development. Hum Reprod. 15(11):2319–2325. doi:10.1093/humrep/15.11.2319.
  • Cinelli MA, Do HT, Miley GP, Silverman RB. 2020. Inducible nitric oxide synthase: Regulation, structure, and inhibition. Med Res Rev. 40(1):158–189. doi:10.1002/med.21599.
  • Cooke RG 3rd, Nothnick WB, Komar C, Burns P, Curry TE Jr. 1999. Collagenase and gelatinase messenger ribonucleic acid expression and activity during follicular development in the rat ovary. Biol Reprod. 61(5):1309–1316. doi:10.1095/biolreprod61.5.1309.
  • D'Ambrosio G, Massa R, Scarfi MR, Zeni O 2002. Cytogenetic damage in human lymphocytes following GMSK phase modulated microwave exposure. Bioelectromagnetics. 23(1):7–13. doi:10.1002/bem.93.
  • Dasdag S, Taş M, Akdag MZ, Yegin K. 2015. Effect of long-term exposure of 2.4 ghz radiofrequency radiation emitted from Wi-Fi equipment on testes functions. Electromagn Biol Med. 34(1):37–42. doi:10.3109/15368378.2013.869752.
  • Dawson BV, Robertson IG, Wilson WR, Zwi LJ, Boys JT, Green AW. 1998. Evaluation of potential health effects of 10 kHz magnetic fields: a rodent reproductive study. Bioelectromagnetics. 19(3):162–171. doi:10.1002/(SICI)1521-186X(1998)19:3%3C162::AID-BEM4%3E3.0.CO;2-%23.
  • Demirel S, Doganay S, Turkoz Y, Dogan Z, Turan B, Firat PG. 2012. Effects of third generation mobile phone-emitted electromagnetic radiation on oxidative stress parameters in eye tissue and blood of rats. Cutan Ocul Toxicol. 31(2):89–94. doi:10.3109/15569527.2012.657725.
  • Diem E, Schwarz C, Adlkofer F, Jahn O, Rüdiger H. 2005. Non-Thermal DNA breakage by mobile-phone radiation (1800 MHz) in human fibroblasts and in transformed GFSH-R17 rat granulosa cells in vitro. Mutat Res. 583(2):178–183. doi:10.1016/j.mrgentox.2005.03.006.
  • Drummond AE, Findlay JK. 1999. The role of estrogen in folliculogenesis. Mol Cell Endocrinol. 151(1–2):57–64. doi:10.1016/s0303-7207(99)00038-6.
  • Durusoy R, Hassoy H, Özkurt A, Karababa AO. 2017. Mobile phone use, school electromagnetic field levels and related symptoms: a cross-sectional survey among 2150 high school students in Izmir. Environ Health. 16(1):51. doi:10.1186/s12940-017-0257-x.
  • Eskander EF, Estefan SF, Abd-Rabou AA. 2012. How does long term exposure to base stations and mobile phones affect human hormone profiles? Clin Biochem. 45(1–2):157–161. doi:10.1016/j.clinbiochem.2011.11.006.
  • Esmailzadeh S, Delavar MA, Aleyassin A, Gholamian SA, Ahmadi A. 2019. Exposure to electromagnetic fields of high voltage overhead power lines and female infertility. Int J Occup Environ Med. 10(1):11–16. doi:10.15171/ijoem.2019.1429.
  • Gul A, Celebi H, Uğraş S. 2009. The effects of microwave emitted by cellular phones on ovarian follicles in rats. Arch Gynecol Obstet. 280(5):729–733. doi:10.1007/s00404-009-0972-9.
  • Guney M, Ozguner F, Oral B, Karahan N, Mungan T. 2007. 900 MHz radiofrequency-induced histopathologic changes and oxidative stress in rat endometrium: protection by vitamins E and C. Toxicol Ind Health. 23(7):411–420. doi:10.1177/0748233707080906.
  • Gupta S, Agarwal A, Banerjee J, Alvarez JG. 2007. The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systematic review. Obstet Gynecol Surv. 62(5):335–354. doi:10.1097/01.ogx.0000261644.89300.df.
  • Gupta S, Sharma RS, Singh R. 2020. Non-Ionizing radiation as possible carcinogen. Int J Environ Health Res. 1–25 . Advance online publication. doi:10.1080/09603123.2020.1806212.
  • Gye MC, Park CJ. 2012. Effect of electromagnetic field exposure on the reproductive system. Clin Exp Reprod Med. 39(1):1–9. doi:10.5653/cerm.2012.39.1.1.
  • Han J, Cao Z, Liu X, Zhang W, Zhang S. 2010. Effect of early pregnancy electromagnetic field exposure on embryo growth ceasing. J Hyg Res. 39(3):349–352.
  • IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. 2013. Non-Ionizing radiation, part 2: radiofrequency electromagnetic fields. IARC Monogr Eval Carcinog Risks Hum. 102(Pt 2):1–460.
  • International Commission on Non-Ionizing Radiation Protection. 2020. Guidelines for limiting exposure to electromagnetic fields (100 kHz to 300 GHz). Health Phys. 118(5):483–524. doi:10.1097/HP.0000000000001210.
  • Jackson LW, Schisterman EF, Dey-Rao R, Browne R, Armstrong D. 2005. Oxidative stress and endometriosis. Hum Reprod. 20(7):2014–2020. doi:10.1093/humrep/dei001.
  • Jung KA, Ahn HS, Lee YS, Gye MC. 2007. Effect of a 20 kHz sawtooth magnetic field exposure on the estrous cycle in mice. J Microbiol Biotechnol. 17(3):398–402.
  • Juutilainen J. 2005. Developmental effects of electromagnetic fields. Bioelectromagnetics. Suppl 26(S7):S107–S115. https://doi.org/10.1002/bem.20125.
  • Kesari KK, Agarwal A, Henkel R. 2018. Radiations and male fertility. Reprod Biol Endocrinol. 16(1):118. doi:10.1186/s12958-018-0431-1.
  • Khaki AA, Khaki A, Ahmadi SS. 2016. The effect of non- ionizing electromagnetic field with a frequency of 50 Hz in rat ovary: a transmission electron microscopy study. Int J Reprod Biomed. 14(2):125–132.
  • Khalil AM, Abu Khadra KM, Aljaberi AM, Gagaa MH, Issa HS. 2014. Assessment of oxidant/antioxidant status in saliva of cell phone users. Electromagn Biol Med. 33(2):92–97. doi:10.3109/15368378.2013.783855.
  • Kim SH, Song JE, Kim SR, Oh H, Gimm YM, Yoo DS, Pack JK, Lee YS. 2004. Teratological studies of prenatal exposure of mice to a 20 kHz sawtooth magnetic field. Bioelectromagnetics. 25(2):114–117. doi:10.1002/bem.10164.
  • Lasley BL, Wang CF, Yen SS. 1975. The effects of estrogen and progesterone on the functional capacity of the gonadotrophs. J Clin Endocrinol Metab. 41(5):820–826. doi:10.1210/jcem-41-5-820.
  • Lewis RC, Hauser R, Maynard AD, Neitzel RL, Wang L, Kavet R, Meeker JD. 2016. Exposure to power-frequency magnetic fields and the risk of infertility and adverse pregnancy outcomes: update on the human evidence and recommendations for future study designs. J Toxicol Environ Health Part B. 19(1):29–45. https://doi.org/10.1080/10937404.2015.1134370.
  • Marci R, Mallozzi M, Di Benedetto L, Schimberni M, Mossa S, Soave I, Palomba S, Caserta D. 2018. Radiations and female fertility. Reprod Biol Endocrinol. 16(1):112. doi:10.1186/s12958-018-0432-0.
  • Mitchell LM, Kennedy CR, Hartshorne GM. 2004. Expression of nitric oxide synthase and effect of substrate manipulation of the nitric oxide pathway in mouse ovarian follicles. Hum Reprod. 19(1):30–40. doi:10.1093/humrep/deh032.
  • Negi P, Singh R. 2021. Association between reproductive health and nonionizing radiation exposure. Electromagn Biol Med. 40(1):92–102. doi:10.1080/15368378.2021.1874973.
  • Ohnishi Y, Mizuno F, Sato T, Yasui M, Kikuchi T, Ogawa M. 2002. Effects of power frequency alternating magnetic fields on reproduction and pre-natal development of mice. J Toxicol Sci. 27(3):131–138. doi:10.2131/jts.27.131.
  • Okatan DÖ, Kaya H, Aliyazıcıoğlu Y, Demir S, Çolakoğlu S, Odacı E. 2018. Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat. Int J Radiat Biol. 94(2):186–198. doi:10.1080/09553002.2018.1420924.
  • Oral B, Guney M, Ozguner F, Karahan N, Mungan T, Comlekci S, Cesur G. 2006. Endometrial apoptosis induced by a 900-MHz mobile phone: preventive effects of vitamins E and C. Adv Ther. 23(6):957–973. doi:10.1007/BF02850217.
  • Panagopoulos DJ, Chavdoula ED, Nezis IP, Margaritis LH. 2007. Cell death induced by GSM 900-MHz and DCS 1800-MHz mobile telephony radiation. Mutat Res. 626(1–2):69–78. doi:10.1016/j.mrgentox.2006.08.008.
  • Panagopoulos DJ, Karabarbounis A, Margaritis LH. 2004. Effect of GSM 900-MHz mobile phone radiation on the reproductive capacity of Drosophila melanogaster. Electromagn Biol Med. 23(1):29–43. doi:10.1081/JBC-120039350.
  • Poulletier de Gannes F, Billaudel B, Haro E, Taxile M, Le Montagner L, Hurtier A, Ait Aissa S, Masuda H, Percherancier Y, Ruffié G, et al. 2013. Rat fertility and embryo fetal development: influence of exposure to the Wi-Fi signal. Reprod Toxicol. 36:1–5. doi:10.1016/j.reprotox.2012.11.003.
  • Rezk AY, Abdulqawi K, Mustafa RM, Abo El-Azm TM, Al-Inany H. 2008. Fetal and neonatal responses following maternal exposure to mobile phones. Saudi Med J. 29(2):218–223.
  • Rodriguez M, Petitclerc D, Burchard JF, Nguyen DH, Block E. 2004. Blood melatonin and prolactin concentrations in dairy cows exposed to 60 Hz electric and magnetic fields during 8 h photoperiods. Bioelectromagnetics. 25(7):508–515. doi:10.1002/bem.20024.
  • Rodriguez M, Petitclerc D, Burchard JF, Nguyen DH, Block E, Downey BR. 2003. Responses of the estrous cycle in dairy cows exposed to electric and magnetic fields (60 Hz) during 8-h photoperiods. Anim Reprod Sci. 77(1–2):11–20. doi:10.1016/s0378-4320(02)00273-7.
  • Roshangar L, Hamdi BA, Khaki AA, Rad JS, Soleimani-Rad S. 2014. Effect of low-frequency electromagnetic field exposure on oocyte differentiation and follicular development. Adv Biomed Res. 3(1):76. https://doi.org/10.4103/2277-9175.125874.
  • Roushangar L, Rad JS. 2007. Ultrastructural alterations and occurrence of apoptosis in developing follicles exposed to low frequency electromagnetic field in rat ovary. Pak J Biol Sci. 10(24):4413–4419. doi:10.3923/pjbs.2007.4413.4419.
  • Sadeghi T, Ahmadi A, Javadian M, Gholamian SA, Delavar MA, Esmailzadeh S, Ahmadi B, Hadighi M. 2017. Preterm birth among women living within 600 meters of high voltage overhead power lines: a case-control study. Rom J Intern Med. 55(3):145–150. doi:10.1515/rjim-2017-0017.
  • Sagioglou NE, Manta AK, Giannarakis IK, Skouroliakou AS, Margaritis LH. 2016. Apoptotic cell death during Drosophila oogenesis is differentially increased by electromagnetic radiation depending on modulation, intensity and duration of exposure. Electromagn Biol Med. 35(1):40–53. doi:10.3109/15368378.2014.971959.
  • Sangun O, Dundar B, Darici H, Comlekci S, Doguc DK, Celik S. 2015. The effects of long-term exposure to a 2450 mhz electromagnetic field on growth and pubertal development in female Wistar rats. Electromagn Biol Med. 34(1):63–71. doi:10.3109/15368378.2013.871619.
  • Shahin S, Singh SP, Chaturvedi CM. 2017. Mobile phone (1800mhz) radiation impairs female reproduction in mice, Mus musculus, through stress induced inhibition of ovarian and uterine activity. Reprod Toxicol. 73:41–60. doi:10.1016/j.reprotox.2017.08.001.
  • Shirai T, Wang J, Kawabe M, Wake K, Watanabe SI, Takahashi S, Fujiwara O. 2017. No adverse effects detected for simultaneous whole-body exposure to multiple-frequency radiofrequency electromagnetic fields for rats in the intrauterine and pre- and post-weaning periods. J Radiat Res. 58(1):48–58. doi:10.1093/jrr/rrw085.
  • Singh R, Nath R, Mathur AK, Sharma RS. 2018. Effect of radiofrequency radiation on reproductive health. Indian J Med Res. 148(Suppl):S92–S99 . PMID: 30964085; PMCID: PMC6469375. doi:10.4103/ijmr.IJMR_1056_18.
  • Tenorio FD, Simões M, Teixeira VW, Teixeira ÁA. 2015. Effects of melatonin and prolactin in reproduction: review of literature. Rev Assoc Med Bras. 61(3):269–274. doi:10.1590/1806-9282.61.03.269.
  • Türedi S, Hancı H, Çolakoğlu S, Kaya H, Odacı E. 2016. Disruption of the ovarian follicle reservoir of prepubertal rats following prenatal exposure to a continuous 900-MHz electromagnetic field. Int J Radiat Biol. 92(6):329–337. doi:10.3109/09553002.2016.1152415.
  • Xu YQ, Zheng NX, Li BH, Zhang WC, Lin XG, Wang JL, Chen GX. 2009. Zhonghua lao dong wei sheng zhi ye bing za zhi = Zhonghua laodong weisheng zhiyebing zazhi =. Chin J Ind Hyg Occup Dis. 27(9):544–548.
  • Yadav H, Rai U, Singh R. 2021. Radiofrequency radiation: a possible threat to male fertility. Reprod Toxicol. 100:90–100. doi:10.1016/j.reprotox.2021.01.007.
  • Yamashita H, Hata K, Yamaguchi H, Tsurita G, Wake K, Watanabe S, Taki M, Ueno S, Nagawa H. 2010. Short-Term exposure to a 1439-MHz TDMA signal exerts no estrogenic effect in rats. Bioelectromagnetics. 31(7):573–575. doi:10.1002/bem.20593.
  • Yüksel M, Nazıroğlu M, Özkaya MO. 2016. 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. Endocrine. 52(2):352–362. doi:10.1007/s12020-015-0795-3.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.