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Effects of mobile phone radiofrequency radiation on sperm quality

Published online by Cambridge University Press:  13 August 2021

Romualdo Sciorio*
Affiliation:
Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, Edinburgh, Scotland, UK
Luca Tramontano
Affiliation:
Dèpartement de la Femme, de l’Enfant et de l’Adolescent, Hopitaux Universitaires de Genève, Genève, Switzerland
Sandro C. Esteves
Affiliation:
ANDROFERT, Andrology and Human Reproduction Clinic, Campinas, Brazil Department of Surgery (Division of Urology), University of Campinas (UNICAMP), Campinas, Brazil Faculty of Health, Aarhus University, Aarhus, Denmark
*
Author for correspondence: Romualdo Sciorio. Edinburgh Assisted Conception Programme, EFREC, Royal Infirmary of Edinburgh, 51 Little France Crescent, Old Dalkeith Road, Edinburgh, Scotland, EH16 4SA, UK. E-mail: sciorioromualdo@hotmail.com

Summary

In the last decades, the universal use of mobile phones has contributed to radiofrequency electromagnetic radiation environmental pollution. The steady growth in mobile phone usage has raised concerns about the effects of phone radiation on male reproductive health. Epidemiological studies report a sharp decline in sperm counts in developing countries, and worldwide with c. 14% of couples having difficulties to conceive, many of which are attributed to a male infertility factor. Environment and lifestyle factors are known to contribute to male infertility. Exposure to heat, radiation, or radioactivity might induce damage to biological tissue organs, including the testis. Given the ubiquitous use of mobile phones, the potential adverse effects of the resulting environmental radiation needs to be elucidated further. It seems to be an apparent relationship between the increased exposure to mobile phone radiofrequency and sperm quality decline, but the evidence is not conclusive. Our review summarizes the evidence concerning the possible adverse effects of cell phone radiation on the male reproductive system, with a focus on sperm quality. Also, we critically analyze the effects of elevated testicular temperature and oxidative stress on male fertility and how these factors could interfere with the physiological activities of the testis.

Type
Review Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Adams, JA, Galloway, TS, Mondal, D, Esteves, SC and Mathews, F (2014). Effect of mobile telephones on sperm quality: a systematic review and meta-analysis. Environ Int 70, 106–12.CrossRefGoogle ScholarPubMed
Agarwal, A, Deepinder, F, Sharma, RK, Ranga, G and Li, J (2008). Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril 89, 124–8.CrossRefGoogle ScholarPubMed
Agarwal, A, Desai, NR, Makker, K, Varghese, A, Mouradi, R, Sabanegh, E and Sharma, R (2009). Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril 92, 1318–25.CrossRefGoogle ScholarPubMed
Agarwal, A, Singh, A, Hamada, A and Kesari, K (2011). Cell phones and male infertility: a review of recent innovations in technology and consequences. Int Braz J Urol 37, 432–54.Google ScholarPubMed
Agarwal, A, Virk, G, Ong, C and du Plessis, SS (2014). Effect of oxidative stress on male reproduction. World J Mens Health 32, 117.Google ScholarPubMed
Aitken, RJ and Curry, BJ (2011). Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal 14, 367–81.CrossRefGoogle Scholar
Aitken, RJ, De Iuliis, GN and McLachlan, RI (2009). Biological and clinical significance of DNA damage in the male germ line. Int J Androl 32, 46–56.CrossRefGoogle ScholarPubMed
Aitken, RJ, Jones, KT and Robertson, SA (2012). Reactive oxygen species and review sperm function—in sickness and in health. J Androl 33, 1096–106.CrossRefGoogle ScholarPubMed
Almášiová, V, Holovská, K, Šimaiová, V, Beňová, K, Raček, A, Račeková, E, Martončíková, M, Mihálik, J, Horváthová, F, Tarabová, L, Slanina, T and Cigánková, V (2018). The thermal effect of 2.45-GHz microwave radiation on rat testes. Acta Vet Brno 86, 413–9.CrossRefGoogle Scholar
Atasoy, HI, Gunal, MY, Atasoy, P, Elgun, S and Bugdayci, G (2013). Immunohistopathologic demonstration of deleterious effects on growing rat testes of radiofrequency waves emitted from conventional Wi-Fi devices. J Pediatr Urol 9, 223–9.CrossRefGoogle ScholarPubMed
Avendaño, C, Mata, A, Sanchez Sarmiento, CA and Doncel, GF (2012). Use of laptop computers connected to internet through Wi-Fi decreases human sperm motility and increases sperm DNA fragmentation. Fertil Steril 97, 3945.e2.CrossRefGoogle ScholarPubMed
Awanti, SM, Ingin, JB, Jeevangi, SR, Patil, GA and Awanti, BS (2010 ). The effect of radio-frequency radiation emitted from mobile phones on plasma oxidants and antioxidants in mobile phone users. J Clin Diagn Res 4, 2758–61.Google Scholar
Baan, R, Grosse, Y, Lauby-Secretan, B, El Ghissassi, F, Bouvard, V, Benbrahim-Tallaa, L, Guha, N, Islami, F, Galichet, L, Straif, K; WHO International Agency for Research on Cancer Monograph Working Group (2011). Carcinogenicity of radiofrequency electromagnetic fields. Lancet Oncol 12, 624–6.Google ScholarPubMed
Baverstock, K (2000). Radiation-induced genomic instability: a paradigm-breaking phenomenon and its relevance to environmentally induced cancer. Mut Res 454(1–2), 89109.CrossRefGoogle ScholarPubMed
Bechoua, S, Hamamah, S and Scalici, E (2016). Male infertility: an obstacle to sexuality? Andrology 4, 395403.CrossRefGoogle ScholarPubMed
Berensztein, EB, Sciara, MI, Rivarola, MA and Belgorosky, A (2002). Apoptosis and proliferation of human testicular somatic and germ cells during prepuberty: High rate of testicular growth in newborns mediated by decreased apoptosis. J Clin Endocrinol Metab 87, 5113–8.CrossRefGoogle ScholarPubMed
Blanco-Rodríguez, J (1998). A matter of death and life: the significance of germ cell death during spermatogenesis. Int J Androl 21, 236–48.CrossRefGoogle ScholarPubMed
Braune, S, Wrocklage, C, Raczek, J, Gailus, T and Lücking, CH (1998). Resting blood pressure increase during exposure to a radio-frequency electromagnetic field. Lancet, 351, 1857–8.CrossRefGoogle ScholarPubMed
Carlsen, E, Andersson, AM, Petersen, JH and Skakkebaek, NE (2003). History of febrile illness and variation in semen quality. Hum Reprod 18, 2089–92.Google ScholarPubMed
Challis, LJ (2005). Mechanisms for interaction between RF fields and biological tissue. Bioelectromagnetics Suppl 7, S98–S106.CrossRefGoogle Scholar
Coulton, LA, Harris, PA, Barker, AT and Pockley, AG (2004). Effect of 50-Hz electromagnetic fields on the induction of heat-shock protein gene expression in human leukocytes. Radiat Res 161, 430–4.CrossRefGoogle ScholarPubMed
Dasdag, S, Zulkuf Akdag, M, Aksen, F, Yilmaz, F, Bashan, M, Mutlu Dasdag, MM and Salih Celik, M (2003). Whole body exposure of rats to microwaves emitted from a cell phone does not affect the testes. Bioelectromagnetics 24, 182–8.Google Scholar
De Geyter, C, Calhaz-Jorge, C, Kupka, MS, Wyns, C, Mocanu, E, Motrenko, T, Scaravelli, G, Smeenk, J, Vidakovic, S, Goossens, V; European IVF-monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE) (2018). ART in Europe, 2014: results generated from European registries by ESHRE: The European IVF-monitoring Consortium (EIM) for the European Society of Human Reproduction and Embryology (ESHRE). Hum Reprod 33, 1586–601.CrossRefGoogle Scholar
De Iuliis, GN, Newey, RJ, King, BV and Aitken, RJ (2009). Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro . PLoS One 4, e6446.CrossRefGoogle ScholarPubMed
Deepinder, F, Makker, K and Agarwal, A (2007). Cell phones and male infertility: dissecting the relationship. Reprod Biomed Online 15, 266–70.Google ScholarPubMed
Desai, N, Sharma, R, Makker, K, Sabanegh, E and Agarwal, A (2009). Physiologic and pathologic levels of reactive oxygen species in neat semen of infertile men. Fertil Steril 92, 1626–31.CrossRefGoogle ScholarPubMed
Ding, SS, Ping, S and Hong, T (2018). Association between daily exposure to electromagnetic radiation from 4G smartphone and 2.45-GHz Wi-Fi and oxidative damage to semen of males attending a genetics clinic: a primary study. Int J Clin Exp Med 11, 2821–30.Google Scholar
Durairajanayagam, D, Agarwal, A and Ong, C (2015). Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online 30, 14–27.CrossRefGoogle ScholarPubMed
Eghlidospour, M, Ghanbari, A, Mortazavi, SMJ and Azari, H (2017). Effects of radiofrequency exposure emitted from a GSM mobile phone on proliferation, differentiation, and apoptosis of neural stem cells. Anat Cell Biol 50, 115–23.CrossRefGoogle ScholarPubMed
Elsayed, NM (2001). Antioxidant mobilization in response to oxidative stress: a dynamic environmental nutritional interaction. Nutrition 17, 828–34.CrossRefGoogle ScholarPubMed
Erogul, O, Oztas, E, Yildirim, I, Kir, T, Aydur, E, Komesli, G, Irkilata, HC, Irmak, MK and Peker, AF (2006). Effects of electromagnetic radiation from a cellular phone on human sperm motility: an in vitro study. Arch Med Res 37, 840–3.CrossRefGoogle Scholar
Esteves, SC, Santi, D and Simoni, M (2020). An update on clinical and surgical interventions to reduce sperm DNA fragmentation in infertile men. Andrology 8, 5381.Google ScholarPubMed
Falzone, N, Huyser, C, Fourie, F, Toivo, T, Leszczynski, D and Franken, D (2008). In vitro effect of pulsed 900 MHz GSM radiation on mitochondrial membrane potential and motility of human spermatozoa. Bioelectromagnetics 29, 268–76.CrossRefGoogle ScholarPubMed
Falzone, N, Huyser, C, Becker, P, Leszczynski, D and Franken, DR (2011). The effect of pulsed 900-MHz GSM mobile phone radiation on the acrosome reaction, head morphometry and zona binding of human spermatozoa. Int J Androl 34, 20–6.CrossRefGoogle ScholarPubMed
Fejes, I, Závaczki, Z, Szöllosi, J, Koloszár, S, Daru, J, Kovács, L and Pál, A (2005). Is there a relationship between cell phone use and semen quality? Arch Androl 51, 385–93.CrossRefGoogle Scholar
Foster, K and Colombi, D (2017). Thermal response of tissue to RF exposure from canonical dipoles at frequencies for future mobile communication systems. Electron Lett 53, 360–2.CrossRefGoogle Scholar
Fraga, CG, Motchnik, PA, Shigenaga, MK, Helbock, HJ, Jacob, RA and Ames, BN (1991). Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 88, 11003–6.CrossRefGoogle ScholarPubMed
Garrido, N, Meseguer, M, Alvarez, J, Simón, C, Pellicer, A and Remohí, J (2004). Relationship among standard semen parameters, glutathione peroxidase/glutathione reductase activity, and mRNA expression and reduced glutathione content in ejaculated spermatozoa from fertile and infertile men. Fertil Steril 82(Suppl. 3), 1059–66.CrossRefGoogle ScholarPubMed
Gatimel, N, Moreau, J, Parinaud, J and Léandri, RD (2017). Sperm morphology: assessment, pathophysiology, clinical relevance, and state of the art in 2017. Andrology 5, 845–62.CrossRefGoogle ScholarPubMed
Gorpinchenko, I, Nikitin, O, Banyra, O and Shulyak, A (2014). The influence of direct mobile phone radiation on sperm quality. Cent Eur J Urol 67, 6571.Google ScholarPubMed
Grell, K, Frederiksen, K, Schüz, J, Cardis, E, Armstrong, B, Siemiatycki, J (2016). The intracranial distribution of gliomas in relation to exposure from mobile phones: analyses from the INTERPHONE study. Am J Epidemiol 184, 818–28.CrossRefGoogle ScholarPubMed
Guz, J, Gackowski, D, Foksinski, M, Rozalski, R, Zarakowska, E, Siomek, A, Szpila, A, Kotzbach, M, Kotzbach, R and Olinski, R (2013). Comparison of oxidative stress/DNA damage in semen and blood of fertile and infertile men. PLoS One 8, e68490.CrossRefGoogle ScholarPubMed
Ha, M, Im, H, Lee, M, Kim, HJ, Kim, BC, Gimm, YM and Pack, JK (2007). Radio-frequency radiation exposure from AM radio transmitters and childhood leukemia and brain cancer. Am J Epidemiol 166, 270–9.CrossRefGoogle Scholar
Hardell, L, Eriksson, M, Carlberg, M, Sundström, C and Mild, KH (2005). Use of cellular or cordless telephones and the risk for non-Hodgkin's lymphoma. Int Arch Occup Environ Health 78, 625–32.CrossRefGoogle ScholarPubMed
Hjollund, NH, Storgaard, L, Ernst, E, Bonde, JP and Olsen, J (2002). Impact of diurnal scrotal temperature on semen quality. Reprod Toxicol 16, 215–21.CrossRefGoogle ScholarPubMed
Huber, R, Graf, T, Cote, KA, Wittmann, L, Gallmann, E, Matter, D, Schuderer, J, Kuster, N, Borbély, AA and Achermann, P (2000). Exposure to pulsed high frequency electromagnetic field during waking affects human sleep EEG. NeuroReport 11, 3321–5.CrossRefGoogle ScholarPubMed
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2013). Non-ionizing radiation, Part 2: Radio frequency electromagnetic fields IARC Monogr Eval Carcinog Risks Hum 102, 1460.Google Scholar
Ikeda, M, Kodama, H, Fukuda, J, Shimizu, Y, Murata, M, Kumagai, J and Tanaka, T (1999). Role of radical oxygen species in rat testicular germ cell apoptosis induced by heat stress. Biol Reprod 61, 393–9.CrossRefGoogle ScholarPubMed
International Commission on Non-Ionizing Radiation Protection (2010). Guidelines for limiting exposure to time-varying electric and magnetic fields (1 Hz TO 100 kHz). Health Physics 99, 818–36.CrossRefGoogle Scholar
Jamaludin, N, Abdul Razak, SSA, Jaffar, FHF, Osman, K and Ibrahim, SF (2017). The effect of smartphone’s radiation frequency and exposure duration on NADPH oxidase 5 (NOX5) level in sperm parameters. Sains Malays 46, 1597–602.CrossRefGoogle Scholar
Jensen, TK, Andersson, AM, Hjollund, NH, Scheike, T, Kolstad, H, Giwercman, A, Henriksen, TB, Ernst, E, Bonde, JP, Olsen, J, McNeilly, A, Groome, NP and Skakkebaek, NE (1997). Inhibin B as a serum marker of spermatogenesis: correlation to differences in sperm concentration and follicle-stimulating hormone levels. A study of 349 Danish men. J Clin Endocrinol Metab 82, 4059–63.Google Scholar
Jung, A and Schill, WB (2000). Male infertility. Current life style could be responsible for infertility. MMW Fortschr Med 142, 31–3.Google ScholarPubMed
Kandeel, FR and Swerdloff, RS (1988). Role of temperature in regulation of spermatogenesis and the use of heating as a method for contraception. Fertil Steril 49, 123.Google Scholar
Kesari, KK and Behari, J (2010). Effects of microwave at 2.45-GHz radiations on reproductive system of male rats. Toxicol Environ Chem 92, 1135–47.CrossRefGoogle Scholar
Kesari, KK and Behari, J (2012). Evidence for mobile phone radiation exposure effects on reproductive pattern of male rats: role of ROS. Electromagn Biol Med 31, 213–22.CrossRefGoogle ScholarPubMed
Kesari, KK, Kumar, S and Behari, J (2011a). 900-MHz microwave radiation promotes oxidation in rat brain. Electromagn Biol Med 30, 219–34.CrossRefGoogle ScholarPubMed
Kesari, KK, Kumar, S and Behari, J (2011b). Effects of radiofrequency electromagnetic wave exposure from cellular phones on the reproductive pattern in male Wistar rats. Appl Biochem Biotechnol 164, 546–59.CrossRefGoogle ScholarPubMed
Kesari, KK, Siddiqui, MH, Meena, R, Verma, HN and Kumar, S (2013). Cell phone radiation exposure on brain and associated biological systems. Indian J Exp Biol 51, 187–200.Google ScholarPubMed
Kesari, KK, Agarwal, AA and Henkel, R (2018). Radiations and male fertility. Reprod Biol Endocrinol 16, 118.CrossRefGoogle ScholarPubMed
Kilgallon, SJ and Simmons, LW (2005). Image content influences men's semen quality. Biol Lett 1, 253–5.CrossRefGoogle ScholarPubMed
Kowalczuk, CI, Saunders, RD and Stapleton, HR (1983). Sperm count and sperm abnormality in male mice after exposure to 2.45-GHz microwave radiation. Mutat Res 122, 155–61.CrossRefGoogle ScholarPubMed
Kumar, S, Kesari, KK and Behari, J (2010). Evaluation of genotoxic effects in male Wistar rats following microwave exposure. Indian J Exp Biol 48, 586–92.Google ScholarPubMed
Kumar, S, Kesari, KK and Behari, J (2011). The therapeutic effect of a pulsed electromagnetic field on the reproductive patterns of male Wistar rats exposed to a 2.45-GHz microwave field. Clinics (São Paulo) 66, 1237–45.CrossRefGoogle ScholarPubMed
Kumar, S, Nirala, JP, Behari, J and Paulraj, R (2014). Effect of electromagnetic irradiation produced by 3G mobile phone on male rat reproductive system in a simulated scenario. Indian J Exp Biol 52, 890–7.Google Scholar
La Vignera, S, Condorelli, RA, Vicari, E, D’Agata, R and Calogero, AE (2012). Effects of the exposure to mobile phones on male reproduction: a review of the literature. J Androl 33, 350–6.CrossRefGoogle ScholarPubMed
Liu, K, Zhang, G, Liu, J, Cao, J, Ao, L and Zhang, S (2014). Association between mobile phone use and semen quality: a systemic review and meta-analysis. Andrology 2, 491–501.CrossRefGoogle ScholarPubMed
Lue, YH, Hikim, AP, Swerdloff, RS, Im, P, Taing, KS, Bui, T, Leung, A and Wang, C (1999). Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinology 140, 1709–17.CrossRefGoogle ScholarPubMed
Mailankot, M, Kunnath, AP, Jayalekshmi, H, Koduru, B and Valsalan, R (2009). Radio frequency electromagnetic radiation (RF-EMR) from GSM (0.9/1.8 GHz) mobile phones induces oxidative stress and reduces sperm motility in rats. Clinics (São Paulo) 64, 561–5.CrossRefGoogle ScholarPubMed
Martin, RH, Hildebrand, K, Yamamoto, J, Rademaker, A, Barnes, M, Douglas, G, Arthur, K, Ringrose, T and Brown, IS (1986). An increased frequency of human sperm chromosomal abnormalities after radiotherapy. Mutat Res 174, 219–25.CrossRefGoogle ScholarPubMed
Martín, M, Macías, M, Escames, G, León, J and Acuña-Castroviejo, D (2000). Melatonin but not vitamins C and E maintains glutathione homeostasis in tert-butyl hydroperoxide induced mitochondrial oxidative stress. FASEB J 14, 1677–9.CrossRefGoogle ScholarPubMed
McClelland, S and Jaboin, JJ (2018). The radiation safety of 5G Wi-Fi: reassuring or Russian roulette? Int J Radiat Oncol Biol Phys 101, 1274–5.CrossRefGoogle ScholarPubMed
McGill, JJ and Agarwal, A (2014). The impact of cell phone, laptop computer and microwave oven usage on male fertility. In: du Plessis, SS, Agarwal, A and Sabanegh, ES Jr (Eds.) Male Infertility: A Complete Guide to Lifestyle and Environmental Factors, pp. 161–77. New York: Springer.CrossRefGoogle Scholar
Meena, R, Kumari, K, Kumar, J, Rajamani, P, Verma, HN and Kesari, KK (2014). Therapeutic approaches of melatonin in microwave radiations-induced oxidative stress mediated toxicity on male fertility pattern of Wistar rats. Electromagn Biol Med 33, 8191.CrossRefGoogle ScholarPubMed
Meo, SA, Al-Drees, AM, Husain, S, Khan, MM and Imran, MB (2010). Effects of mobile phone radiation on serum testosterone in Wistar albino rats. Saudi Med J 31, 869–73.Google ScholarPubMed
Meo, SA, Arif, M, Rashied, S, Khan, MM, Vohra, MS, Usmani, AM, Imran, MB, Al-Drees, AM (2011). Hypospermatogenesis and spermatozoa maturation arrest in rats induced by mobile phone radiation. J Coll Physicians Surg Pak 21, 262–5.Google ScholarPubMed
Merhi, ZO (2012). Challenging cell phone impact on reproduction: a review. J Assist Reprod Genet 29, 293–7.CrossRefGoogle ScholarPubMed
Moein, MR, Dehghani, VO, Tabibnejad, N and Vahidi, S (2007). Reactive oxygen species (ROS) level in seminal plasma of infertile men and healthy donors. Iran J Reprod Med 5, 51–5.Google Scholar
Munkelwitz, R and Gilbert, BR (1998). Are boxer shorts really better? A critical analysis of the role of underwear type in male subfertility. J Urol 160, 1329–33.CrossRefGoogle Scholar
National Radiological Protection Board (NRBP) (2004). Review of the scientific evidence for limiting exposure to electromagnetic fields (0–300 GHz) Documents of NRPB [monograph on the Internet], 15. Available at: National Radiological Protection Board (NRPB). Didcot, Oxon, UK: Chilton: NRPB. Retrieved from http://www.hpa.org.uk/web/HPAwebFile/HPAweb_C/1194947383619 Google Scholar
Nikolova, T, Czyz, J, Rolletschek, A, Blyszczuk, P, Fuchs, J, Jovtchev, G, Schuderer, J, Kuster, N and Wobus, AM (2005). Electromagnetic fields affect transcript levels of apoptosis-related genes in embryonic stem cell-derived neural progenitor cells. FASEB J 19, 1686–8.CrossRefGoogle ScholarPubMed
Odacı, E and Özyılmaz, C (2015). Exposure to a 900-MHz electromagnetic field for 1 hour a day over 30 days does change the histopathology and biochemistry of the rat testis. Int J Rad Biol 91, 547–54.CrossRefGoogle Scholar
Oftedal, G, Wilen, J, Sandstrom, M and Mild, KH (2000). Symptoms experiences in connection with mobile phone use. Occup Med (Lond) 50, 237–45. doi: 10.1093/occmed/50.4.237 CrossRefGoogle Scholar
Oksay, T, Naziroğlu, M, Doğan, S, Güzel, A, Gümral, N and Koşar, PA (2014). Protective effects of melatonin against oxidative injury in rat testis induced by wireless (2.45 GHz) devices. Andrologia 46, 6572.CrossRefGoogle ScholarPubMed
Oni, OM, Amuda, DB and Gilbert, CE (2011). Effects of radio-frequency radiation from WiFi devices on human ejaculated semen. Int J Res Rev Appl Sci 9, 292–4.Google Scholar
Othman, H, Ammari, M, Sakly, M and Abdelmelek, H (2017). Effects of prenatal exposure to WIFI signal (2.45 GHz) on postnatal development and behavior in rat: Influence of maternal restraint. Behav Brain Res 326, 291302.CrossRefGoogle Scholar
Ozguner, F, Bardak, Y and Comlekci, S (2006). Protective effects of melatonin and caffeic acid phenethyl ester against retinal oxidative stress in long-term use of mobile phone: a comparative study. Mol Cell Biochem 282 (1–2), 83–8.CrossRefGoogle ScholarPubMed
Pandey, N, Giri, S, Das, S and Upadhaya, P (2017). Radio-frequency radiation (900 MHz)-induced DNA damage and cell cycle arrest in testicular germ cells in swiss albino mice. Toxicol Ind Health 33, 373–84.CrossRefGoogle Scholar
Pelliccione, F, Micillo, A, Cordeschi, G, D’Angeli, A, Necozione, S, Gandini, L, Lenzi, A, Francavilla, F and Francavilla, S (2011). Altered ultrastructure of mitochondrial membranes is strongly associated with unexplained asthenozoospermia. Fertil Steril 95, 641–6.CrossRefGoogle ScholarPubMed
Prausnitz, S and Susskind, C (1962). Effects of chronic microwave irradiation on mice. Ire Trans Biomed Electron 9, 104–8.CrossRefGoogle ScholarPubMed
Reiter, R, Tang, L, Garcia, JJ and Muñoz-Hoyos, A (1997). Pharmacological actions of melatonin in oxygen radical pathophysiology. Life Sci 60, 22552271.CrossRefGoogle ScholarPubMed
Reiter, RJ, Tan, DX and Acuna-Castroviejo, D (2000). Melatonin: mechanisms and actions as an antioxidant. Curr Top Biophys 24, 171–83.Google Scholar
Reiter, RJ, Mayo, JC, Tan, DX, Sainz, RM, Alatorre-Jimenez, M and Qin, L (2016). Melatonin as an antioxidant: under promises but over delivers. J Pineal Res 61, 253–78.CrossRefGoogle Scholar
Rodriguez, C, Mayo, JC, Sainz, RM, Antolín, I, Herrera, F, Martín, V and Reiter, RJ (2004). Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 36, 19.CrossRefGoogle ScholarPubMed
Roque, M and Esteves, SC (2018). Effect of varicocele repair on sperm DNA fragmentation: a review. Int Urol Nephrol 50, 583603.CrossRefGoogle ScholarPubMed
Sage, C and Burgio, E (2018). Electromagnetic fields, pulsed radiofrequency radiation, and epigenetics: how wireless technologies may affect childhood development. Child Dev 89, 129–36.CrossRefGoogle ScholarPubMed
Saygin, M, Caliskan, S, Karahan, N, Koyu, A, Gumral, N and Uguz, A (2011). Testicular apoptosis and histopathological changes induced by a 2.45-GHz electromagnetic field. Toxicol Ind Health 27, 455–63.CrossRefGoogle ScholarPubMed
Sciorio, R and Smith, GD (2019). Embryo culture at a reduced oxygen concentration of 5%: a mini review. Zygote 27, 355–61.CrossRefGoogle Scholar
Shahin, S, Mishra, V, Singh, SP and Chaturvedi, CM (2014). 2.45-GHz microwave irradiation adversely affects reproductive function in male mouse, Mus musculus by inducing oxidative and nitrosative stress. Free Radic Res 48, 511–25.CrossRefGoogle ScholarPubMed
Sheikh, N, Amiri, I, Farimani, M, Najafi, R and Hadeie, J (2008). Correlation between sperm parameters and sperm DNA fragmentation in fertile and infertile men. Iran J Reprod Med 6, 13–8.Google Scholar
Shi, TY, Chen, G, Huang, X, Yuan, Y, Wu, X, Wu, B, Li, Z, Shun, F, Chen, H and Shi, H (2012). Effects of reactive oxygen species from activated leucocytes on human sperm motility, viability and morphology. Andrologia 44 Suppl. 1, 696703.CrossRefGoogle ScholarPubMed
Shiraishi, K, Matsuyama, H and Takihara, H (2012). Pathophysiology of varicocele in male infertility in the era of assisted reproductive technology. Int J Urol 19, 538–50.CrossRefGoogle ScholarPubMed
Shokri, S, Soltani, A, Kazemi, M, Sardari, D and Mofrad, FB (2015). Effects of Wi-Fi (2.45 GHz) exposure on apoptosis, sperm parameters and testicular histomorphometry in rats: a time course study. Cell J 17, 322–31.Google ScholarPubMed
Sullivan, R and Mieusset, R (2016). The human epididymis: its function in sperm maturation. Hum Reprod Update 22, 574–87.CrossRefGoogle ScholarPubMed
Teepen, JC and van Dijck, JA (2012). Impact of high electromagnetic field levels on childhood leukemia incidence. Int J Cancer 131, 769–78.CrossRefGoogle ScholarPubMed
Teixeira, T and Hasan, SF (2016). Assessing electromagnetic radiation in our environment. IEEE Potentials 35, 22–5.CrossRefGoogle Scholar
The Institute of Electrical and Electronics Engineers (IEEE) (1992). IEEE standard for safety levels with respect to human exposure to radio frequency electromagnetic fields, 3 kHz to 300 GHz. In: IEEE Std C95.1-1991, pp. 1–76.Google Scholar
Thoma, ME, McLain, AC, Louis, JF, King, RB, Trumble, AC, Sundaram, R and Buck Louis, GM (2013). Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach. Fertil Steril 99, 1324–31.e1.CrossRefGoogle Scholar
Tök, L, Nazıroğlu, M, Doğan, S, Kahya, MC and Tök, O (2014). Effects of melatonin on Wi-Fi-induced oxidative stress in lens of rats. Indian J Ophthalmol 62, 12–5.Google ScholarPubMed
Varma, MM and Traboulay, EA Jr, Jr (1975). Biological effects of microwave radiation on the testes of Swiss mice. Experientia 31, 301–2.CrossRefGoogle ScholarPubMed
Wall, S, Wang, ZM, Kendig, T, Dobraca, D and Lipsett, M (2019). Real world cell phone radio frequency electromagnetic field exposures. Environ Res 171, 581–92.CrossRefGoogle Scholar
Wdowiak, A, Wdowiak, L and Wiktor, H (2007). Evaluation of the effect of using mobile phones on male fertility. Ann Agric Environ Med 14, 169–72.Google ScholarPubMed
Wiesner, C, Nabha, SM, Dos Santos, EB, Yamamoto, H, Meng, H, Melchior, SW, Bittinger, F, Thüroff, JW, Vessella, RL, Cher, ML and Bonfil, RD (2008). c-kit and its ligand stem cell factor: potential contribution to prostate cancer bone metastasis. Neoplasia 10, 9961003.CrossRefGoogle ScholarPubMed
Wilkes, S, Chinn, DJ, Murdoch, A and Rubin, G (2009). Epidemiology and management of infertility: a population-based study in UK primary care. Fam Pract 26, 269–74.CrossRefGoogle ScholarPubMed
Xu, G, Intano, GW, McCarrey, JR, Walter, RB, McMahan, CA and Walter, CA (2008). Recovery of a low mutant frequency after ionizing radiation-induced mutagenesis during spermatogenesis. Mutat Res 654, 150–7.CrossRefGoogle ScholarPubMed
Yan, JG, Agresti, M, Bruce, T, Yan, YH, Granlund, A and Matloub, HS (2007). Effects of cellular phone emissions on sperm motility in rats. Fertil Steril 88, 957–64.CrossRefGoogle ScholarPubMed
Yin, Y, Hawkins, KL, DeWolf, WC and Morgentaler, A (1997). Heat stress causes testicular germ cell apoptosis in adult mice. J Androl 18, 159–65.Google ScholarPubMed
Zalata, A, El-Samanoudy, AZ, Shaalan, D, El-Baiomy, Y and Mostafa, T (2015). In vitro effect of cell phone radiation on motility, DNA fragmentation and clusterin gene expression in human sperm. Int J Fertil Steril 9, 129–36.Google ScholarPubMed
Zhang, M, Jiang, M, Bi, Y, Zhu, H, Zhou, Z and Sha, J (2012). Autophagy and apoptosis act as partners to induce germ cell death after heat stress in mice. PLoS One 7, e41412.CrossRefGoogle ScholarPubMed
Zhang, X, Cui, W, Wang, K, Chen, R, Chen, M, Lan, K, Wei, Y, Pan, C and Lan, X (2020). Chlorpyrifos inhibits sperm maturation and induces a decrease in mouse male fertility. Environ Res 188, 109785.CrossRefGoogle ScholarPubMed