Fertility and Sterility
Volume 92, Issue 4 , Pages 1318-1325 , October 2009

Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study

  • Ashok Agarwal, Ph.D.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
    • Obstetrics and Gynecology and Women's Health Institute, Cleveland Clinic, Cleveland, Ohio
    • Corresponding Author InformationReprint requests: Ashok Agarwal, Ph.D., H.C.L.D., Professor and Director, Center for Reproductive Medicine, Cleveland Clinic, 9500 Euclid Avenue, Desk A19.1, Cleveland, OH 44195 (FAX: 216-636-3118, 216-445-6049).
  • ,
  • Nisarg R. Desai, M.D.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Kartikeya Makker, M.D.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Alex Varghese, Ph.D.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Rand Mouradi, M.S.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Edmund Sabanegh, M.D.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Rakesh Sharma, Ph.D.

      Affiliations

    • Center for Reproductive Medicine, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio
    • Obstetrics and Gynecology and Women's Health Institute, Cleveland Clinic, Cleveland, Ohio

Received 4 June 2008 ,Revised 31 July 2008 ,Accepted 7 August 2008.

References 

  1. Repacholi MH. Low-level exposure to radiofrequency electromagnetic fields: health effects and research needs. Bioelectromagnetics. 1998;19:1–19
  2. Agarwal A, Deepinder F, Sharma RK, Ranga G, Li J. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril. 2008;89:124–128
  3. Davoudi M, Brossner C, Kuber W. The influence of electromagnetic waves on sperm motility. Urol Urogynecol. 2002;19:18–32
  4. Fejes I, Zavaczki Z, Szollosi J, Koloszar S, Daru J, Kovacs L, et al. Is there a relationship between cell phone use and semen quality?. Arch Androl. 2005;51:385–393
  5. Wdowiak A, Wdowiak L, Wiktor H. Evaluation of the effect of using mobile phones on male fertility. Ann Agric Environ Med. 2007;14:169–172
  6. Baste V, Riise T, Moen BE. Radiofrequency electromagnetic fields; male infertility and sex ratio of offspring. Eur J Epidemiol. 2008;23:369–377
  7. Oktem F, Ozguner F, Mollaoglu H, Koyu A, Uz E. Oxidative damage in the kidney induced by 900-MHz-emitted mobile phone: protection by melatonin. Arch Med Res. 2005;36:350–355
  8. Ozguner F, Bardak Y, Comlekci S. 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. 2006;282:83–88
  9. Ozguner M, Koyu A, Cesur G, Ural M, Ozguner F, Gokcimen A, et al. Biological and morphological effects on the reproductive organ of rats after exposure to electromagnetic field. Saudi Med J. 2005;26:405–410
  10. Balci M, Devrim E, Durak I. Effects of mobile phones on oxidant/antioxidant balance in cornea and lens of rats. Curr Eye Res. 2007;32:21–25
  11. Meral I, Mert H, Mert N, Deger Y, Yoruk I, Yetkin A, et al. Effects of 900-MHz electromagnetic field emitted from cellular phone on brain oxidative stress and some vitamin levels of guinea pigs. Brain Res. 2007;1169:120–124
  12. Ozguner F, Altinbas A, Ozaydin M, Dogan A, Vural H, Kisioglu AN, et al. Mobile phone-induced myocardial oxidative stress: protection by a novel antioxidant agent caffeic acid phenethyl ester. Toxicol Ind Health. 2005;21:223–230
  13. Oral B, Guney M, Ozguner F, Karahan N, Mungan T, Comlekci S, et al. Endometrial apoptosis induced by a 900-MHz mobile phone: preventive effects of vitamins E and C. Adv Ther. 2006;23:957–973
  14. Forgacs Z, Somosy Z, Kubinyi G, Bakos J, Hudak A, Surjan A, et al. Effect of whole-body 1800MHz GSM-like microwave exposure on testicular steroidogenesis and histology in mice. Reprod Toxicol. 2006;22:111–117
  15. Aitken RJ, Bennetts LE, Sawyer D, Wiklendt AM, King BV. Impact of radio frequency electromagnetic radiation on DNA integrity in the male germline. Int J Androl. 2005;28:171–179
  16. Dasdag S, Ketani MA, Akdag Z, Ersay AR, Sari I, Demirtas OC, et al. Whole-body microwave exposure emitted by cellular phones and testicular function of rats. Urol Res. 1999;27:219–223
  17. Dasdag S, Zulkuf Akdag M, Aksen F, Yilmaz F, Bashan M, Mutlu Dasdag M, et al. Whole body exposure of rats to microwaves emitted from a cell phone does not affect the testes. Bioelectromagnetics. 2003;24:182–188
  18. Ribeiro EP, Rhoden EL, Horn MM, Rhoden C, Lima LP, Toniolo L. Effects of subchronic exposure to radio frequency from a conventional cellular telephone on testicular function in adult rats. J Urol. 2007;177:395–399
  19. Yan JG, Agresti M, Bruce T, Yan YH, Granlund A, Matloub HS. Effects of cellular phone emissions on sperm motility in rats. Fertil Steril. 2007;88:957–964
  20. Cairnie AB, Harding RK. Cytological studies in mouse testis irradiated with 2.45-GHz continuous-wave microwaves. Radiat Res. 1981;87:100–108
  21. World Health Organization. WHO research agenda for radio frequency fields. Available at: www.who.int/peh-emf/research/rf_research_agenda_2006.pdf.
  22. Erogul O, Oztas E, Yildirim I, Kir T, Aydur E, Komesli G, et al. Effects of electromagnetic radiation from a cellular phone on human sperm motility: an in vitro study. Arch Med Res. 2006;37:840–843
  23. Falzone N, Huyser C, Fourie F, Toivo T, Leszczynski D, Franken D. In vitro effect of pulsed 900 MHz GSM radiation on mitochondrial membrane potential and motility of human spermatozoa. Bioelectromagnetics. 2007;
  24. International Commission on Non-Ionizing Radiation Protection. Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz). Health Phys. 1998;74:494–522
  25. Federal Communications Commission. Questions and answers about biological effects and potential hazards of radiofrequency electromagnetic fields. Available at: www.fcc.gov/Bureaus/Engineering_Technology/Documents/bulletins/oet56/oet56e4.pdf.
  26. World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucous interaction. New York: Cambridge University Press; 1999;
  27. Kobayashi H, Gil-Guzman E, Mahran AM, Sharma RK, Nelson DR, Thomas AJ, et al. Quality control of reactive oxygen species measurement by luminol-dependent chemiluminescence assay. J Androl. 2001;22:568–574
  28. Rice-Evans C, Miller NJ. Total antioxidant status in plasma and body fluids. Methods Enzymol. 1994;234:279–293
  29. Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ, Agarwal A. The reactive oxygen species–total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod. 1999;14:2801–2807
  30. Gorczyca W, Gong J, Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 1993;53:1945–1951
  31. Said TM, Agarwal A, Sharma RK, Thomas AJ, Sikka SC. Impact of sperm morphology on DNA damage caused by oxidative stress induced by beta-nicotinamide adenine dinucleotide phosphate. Fertil Steril. 2005;83:95–103
  32. Said TM, Aziz N, Sharma RK, Lewis-Jones I, Thomas AJ, Agarwal A. Novel association between sperm deformity index and oxidative stress–induced DNA damage in infertile male patients. Asian J Androl. 2005;7:121–126
  33. Friedman J, Kraus S, Hauptman Y, Schiff Y, Seger R. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochem J. 2007;405:559–568
  34. Berridge MV, Tan AS. Cell-surface NAD(P)H-oxidase: relationship to trans-plasma membrane NADH-oxidoreductase and a potential source of circulating NADH-oxidase. Antioxid Redox Signal. 2000;2:277–288
  35. Berridge MV, Tan AS. High-capacity redox control at the plasma membrane of mammalian cells: trans-membrane, cell surface, and serum NADH-oxidases. Antioxid Redox Signal. 2000;2:231–242
  36. Aitken RJ, Ryan AL, Curry BJ, Baker MA. Multiple forms of redox activity in populations of human spermatozoa. Mol Hum Reprod. 2003;9:645–661
  37. Aitken RJ, Buckingham DW, West KM. Reactive oxygen species and human spermatozoa: analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence. J Cell Physiol. 1992;151:466–477
  38. Irmak MK, Fadillioglu E, Gulec M, Erdogan H, Yagmurca M, Akyol O. Effects of electromagnetic radiation from a cellular telephone on the oxidant and antioxidant levels in rabbits. Cell Biochem Funct. 2002;20:279–283
  39. Stopczyk D, Gnitecki W, Buczynski A, Markuszewski L, Buczynski J. [Effect of electromagnetic field produced by mobile phones on the activity of superoxide dismutase (SOD-1) and the level of malonyldialdehyde (MDA)—in vitro study]. Med Pr. 2002;53:311–314Polish
  40. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol. 2008;59:2–11
  41. Henkel R, Kierspel E, Stalf T, Mehnert C, Menkveld R, Tinneberg HR, et al. Effect of reactive oxygen species produced by spermatozoa and leukocytes on sperm functions in nonleukocytospermic patients. Fertil Steril. 2005;83:635–642
  42. French DB, Desai NR, Agarwal A. Varicocele repair: does it still have a role in infertility treatment?. Curr Opin Obstet Gynecol. 2008;20:269–274
  43. Stronati L, Testa A, Moquet J, Edwards A, Cordelli E, Villani P, et al. 935 MHz cellular phone radiation. An in vitro study of genotoxicity in human lymphocytes. Int J Radiat Biol. 2006;82:339–346
  44. Lai H, Singh NP. Single- and double-strand DNA breaks in rat brain cells after acute exposure to radiofrequency electromagnetic radiation. Int J Radiat Biol. 1996;69:513–521
  45. Lixia S, Yao K, Kaijun W, Deqiang L, Huajun H, Xiangwei G, et al. Effects of 1.8 GHz radiofrequency field on DNA damage and expression of heat shock protein 70 in human lens epithelial cells. Mutat Res. 2006;602:135–142
  46. McNamee JP, Bellier PV, Gajda GB, Lavallee BF, Marro L, Lemay E, et al. No evidence for genotoxic effects from 24 h exposure of human leukocytes to 1.9 GHz radiofrequency fields. Radiat Res. 2003;159:693–697
  47. McNamee JP, Bellier PV, Gajda GB, Miller SM, Lemay EP, Lavallee BF, et al. DNA damage and micronucleus induction in human leukocytes after acute in vitro exposure to a 1.9 GHz continuous-wave radiofrequency field. Radiat Res. 2002;158:523–533
  48. Sakuma N, Komatsubara Y, Takeda H, Hirose H, Sekijima M, Nojima T, et al. DNA strand breaks are not induced in human cells exposed to 2.1425 GHz band CW and W-CDMA modulated radiofrequency fields allocated to mobile radio base stations. Bioelectromagnetics. 2006;27:51–57
  49. Tice RR, Hook GG, Donner M, McRee DI, Guy AW. Genotoxicity of radiofrequency signals. I. Investigation of DNA damage and micronuclei induction in cultured human blood cells. Bioelectromagnetics. 2002;23:113–126
  50. Vijayalaxmi Bisht KS, Pickard WF, Meltz ML, Roti Roti JL, Moros EG. Chromosome damage and micronucleus formation in human blood lymphocytes exposed in vitro to radiofrequency radiation at a cellular telephone frequency (847.74 MHz, CDMA). Radiat Res. 2001;156:430–432
  51. Belyaev IY, Koch CB, Terenius O, Roxstrom-Lindquist K, Malmgren LO, Sommer W, et al. Exposure of rat brain to 915 MHz GSM microwaves induces changes in gene expression but not double stranded DNA breaks or effects on chromatin conformation. Bioelectromagnetics. 2006;27:295–306
  52. Paulraj R, Behari J. Single strand DNA breaks in rat brain cells exposed to microwave radiation. Mutat Res. 2006;596:76–80
  53. Leszczynski D, Joenvaara S, Reivinen J, Kuokka R. Non-thermal activation of the hsp27/p38MAPK stress pathway by mobile phone radiation in human endothelial cells: molecular mechanism for cancer- and blood-brain barrier–related effects. Differentiation. 2002;70:120–129
  54. Blank M, Goodman R. A mechanism for stimulation of biosynthesis by electromagnetic fields: charge transfer in DNA and base pair separation. J Cell Physiol. 2008;214:20–26
  55. Nylund R, Leszczynski D. Proteomics analysis of human endothelial cell line EA.hy926 after exposure to GSM 900 radiation. Proteomics. 2004;4:1359–1365
  56. Moskovtsev SI, Willis J, White J, Mullen JB. Leukocytospermia: relationship to sperm deoxyribonucleic acid integrity in patients evaluated for male factor infertility. Fertil Steril. 2007;88:737–740
  57. Capri M, Scarcella E, Fumelli C, Bianchi E, Salvioli S, Mesirca P, et al. In vitro exposure of human lymphocytes to 900 MHz CW and GSM modulated radiofrequency: studies of proliferation, apoptosis and mitochondrial membrane potential. Radiat Res. 2004;162:211–218
  58. Lantow M, Lupke M, Frahm J, Mattsson MO, Kuster N, Simko M. ROS release and Hsp70 expression after exposure to 1,800 MHz radiofrequency electromagnetic fields in primary human monocytes and lymphocytes. Radiat Environ Biophys. 2006;45:55–62
  59. Lantow M, Schuderer J, Hartwig C, Simko M. Free radical release and HSP70 expression in two human immune-relevant cell lines after exposure to 1800 MHz radiofrequency radiation. Radiat Res. 2006;165:88–94
  60. Simko M, Hartwig C, Lantow M, Lupke M, Mattsson MO, Rahman Q, et al. Hsp70 expression and free radical release after exposure to nonthermal radio-frequency electromagnetic fields and ultrafine particles in human Mono Mac 6 cells. Toxicol Lett. 2006;161:73–82
  61. Frahm J, Lantow M, Lupke M, Weiss DG, Simko M. Alteration in cellular functions in mouse macrophages after exposure to 50 Hz magnetic fields. J Cell Biochem. 2006;99:168–177
  62. Simko M, Droste S, Kriehuber R, Weiss DG. Stimulation of phagocytosis and free radical production in murine macrophages by 50 Hz electromagnetic fields. Eur J Cell Biol. 2001;80:562–566
  63. Esfandiari N, Saleh RA, Blaut AP, Sharma RK, Nelson DR, Thomas AJ, et al. Effects of temperature on sperm motion characteristics and reactive oxygen species. Int J Fertil Womens Med. 2002;47:227–233
  64. Kuster N, Schuderer J, Christ A, Futter P, Ebert S. Guidance for exposure design of human studies addressing health risk evaluations of mobile phones. Bioelectromagnetics. 2004;25:524–529
  65. Anderson V, Rowley J. Measurements of skin surface temperature during mobile phone use. Bioelectromagnetics. 2007;28:159–162
  66. Straume A, Oftedal G, Johnsson A. Skin temperature increase caused by a mobile phone: a methodological infrared camera study. Bioelectromagnetics. 2005;26:510–519

 A.A. has nothing to disclose. N.D. has nothing to disclose. K.M. has nothing to disclose. A.V. has nothing to disclose. R.M. has nothing to disclose. E.S. has nothing to disclose. R.S. has nothing to disclose.

 Supported by the Center for Reproductive Medicine, Cleveland Clinic.

PII: S0015-0282(08)03356-6

doi: 10.1016/j.fertnstert.2008.08.022

Fertility and Sterility
Volume 92, Issue 4 , Pages 1318-1325 , October 2009