Electromagnetic Radiation and Oxidative Stress in the Male Germ Line

  • Geoffry N. De Iuliis
  • Bruce V. King
  • R. John Aitken
Part of the Oxidative Stress in Applied Basic Research and Clinical Practice book series (OXISTRESS)


The beneficial impacts of mobile-based communications on society are considerable. Health concerns over the broadcast of radio frequency electromagnetic waves, which carry the information for this medium, are now gaining momentum but are not without its controversies. Studies in the past that aim to determine whether concerns are warranted are sometimes lacking in impact because of poor understanding of radiation science. Nevertheless, the studies completed to date are important in developing the field toward the goal of confirming or disproving claims that radio frequency electromagnetic radiation (RF-EMR) is a serious health issue. We focus on what has been achieved to date, toward determining the effects of RF-EMR on the male reproductive system and information presented which may underpin the potential mechanisms at play. We suggest that oxidative stress may have a key role in the detrimental effects observed in the human spermatozoon and that this cell type may be a unique model to determine the potential mechanism of action given its sensitivities to such stressors.


Electromagnetic radiation Oxidative stress Male germ line Sperm oxidative stress DNA damage 


  1. 1.
    Darnell J, Lodish H, Baltimore D, editors. Nerve cells and the electrical properties of cell membranes. New York: Scientific American Books; 1986.Google Scholar
  2. 2.
    Sheppard AR, Swicord ML, Balzano Q. Quantitative evaluations of mechanisms of radiofrequency interactions with biological molecules and processes. Health Phys. 2008;95(4):365–96.PubMedCrossRefGoogle Scholar
  3. 3.
    Dubey RB, Hanmandlu M, Gupta SK. Risk of brain tumors from wireless phone use. J Comput Assist Tomogr. 2010;34(6):799–807.PubMedCrossRefGoogle Scholar
  4. 4.
    de Vocht F, Burstyn I, Cherrie JW. Time trends (1998-2007) in brain cancer incidence rates in relation to mobile phone use in England. Bioelectromagnetics. 2011;32(5):334–9.PubMedCrossRefGoogle Scholar
  5. 5.
    Joines WT, Zhang Y, Li CX, Jirtle RL. The measured electrical-properties of normal and malignant human tissues from 50 to 900 Mhz. Med Phys. 1994;21(4):547–50.PubMedCrossRefGoogle Scholar
  6. 6.
    Ichikawa F, Chipchase J, Grignani R. Where’s the phone? A study of mobile phone location in public spaces. In: Paper presented at mobile technology, applications and systems, 2005 2nd international conference, Guangzhou, China; 2005.Google Scholar
  7. 7.
    Whittow WG, Panagamuwa CJ, Edwards RM, Vardaxoglou JC. On the effects of straight metallic jewellery on the specific absorption rates resulting from face-illuminating radio communication devices at popular cellular frequencies. Phys Med Biol. 2008;53(5):1167–82.PubMedCrossRefGoogle Scholar
  8. 8.
    Foster KR, Glaser R. Thermal mechanisms of interaction of radiofrequency energy with biological systems with relevance to exposure guidelines. Health Phys. 2007;92(6):609–20.PubMedCrossRefGoogle Scholar
  9. 9.
    Phillips JL, Singh NP, Lai H. Electromagnetic fields and DNA damage. Pathophysiology. 2009;16(2–3):79–88.PubMedCrossRefGoogle Scholar
  10. 10.
    Challis LJ. Mechanisms for interaction between RF fields and biological tissue. Bioelectromagnetics. 2005;Suppl 7:S98–106.Google Scholar
  11. 11.
    Johnson RD, Navratil M, Poe BG, et al. Analysis of mitochondria isolated from single cells. Anal Bioanal Chem. 2007;387(1):107–18.PubMedCrossRefGoogle Scholar
  12. 12.
    Blank M. Do electromagnetic fields interact with electrons in the Na, K-ATPase? Bioelectromagnetics. 2005;26(8):677–83.PubMedCrossRefGoogle Scholar
  13. 13.
    Blank M. Electric stimulation of protein synthesis in muscle. Adv Chem Ser. 1995;250:143–53.CrossRefGoogle Scholar
  14. 14.
    Luben RA. Membrane signal-transduction mechanisms and biological effects of low-energy electromagnetic fields. Adv Chem Ser. 1995;250:437–50.CrossRefGoogle Scholar
  15. 15.
    Kotnik T, Miklavcic D. Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. Biophys J. 2006;90(2):480–91.PubMedCrossRefGoogle Scholar
  16. 16.
    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(2–3):120–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Seger R, Friedman J, Kraus S, Hauptman Y, Schiff Y. Mechanism of short-term ERK activation by electromagnetic fields at mobile phone frequencies. Biochem J. 2007;405:559–68.PubMedCrossRefGoogle Scholar
  18. 18.
    Kotnik T, Pucihar G, Miklavcic D. Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport. J Membr Biol. 2010;236(1):3–13.PubMedCrossRefGoogle Scholar
  19. 19.
    Cotgreave IA. Biological stress responses to radio frequency electromagnetic radiation: are mobile phones really so (heat) shocking? Arch Biochem Biophys. 2005;435(1):227–40.PubMedCrossRefGoogle Scholar
  20. 20.
    Porcelli M, Cacciapuoti G, Fusco S, et al. Non-thermal effects of microwaves on proteins: thermophilic enzymes as model system. FEBS Lett. 1997;402(2–3):102–6.PubMedCrossRefGoogle Scholar
  21. 21.
    de Pomerai DI, Smith B, Dawe A, et al. Microwave radiation can alter protein conformation without bulk heating. FEBS Lett. 2003;543(1–3):93–7.PubMedCrossRefGoogle Scholar
  22. 22.
    Mancinelli F, Caraglia M, Abbruzzese A, d’Ambrosio G, Massa R, Bismuto E. Non-thermal effects of electromagnetic fields at mobile phone frequency on the refolding of an intracellular protein: myoglobin. J Cell Biochem. 2004;93(1):188–96.PubMedCrossRefGoogle Scholar
  23. 23.
    De Iuliis GN, Thomson LK, Mitchell LA, et al. DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2′-deoxyguanosine, a marker of oxidative stress. Biol Reprod. 2009;81(3):517–24.PubMedCrossRefGoogle Scholar
  24. 24.
    Pacey AA. Environmental and lifestyle factors associated with sperm DNA damage. Hum Fertil. 2010;13(4):189–93.CrossRefGoogle Scholar
  25. 25.
    Sakkas D, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010;93(4):1027–36.PubMedCrossRefGoogle Scholar
  26. 26.
    Robaire B, Delbes G, Hales BF. Toxicants and human sperm chromatin integrity. Mol Hum Reprod. 2010;16(1):14–22.PubMedCrossRefGoogle Scholar
  27. 27.
    Aitken RJ, De Iuliis GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2010;16(1):3–13.PubMedCrossRefGoogle Scholar
  28. 28.
    Aitken RJ, De Iuliis GN, McLachlan RI. Biological and clinical significance of DNA damage in the male germ line. Int J Androl. 2009;32(1):46–56.PubMedCrossRefGoogle Scholar
  29. 29.
    Evenson D, Wixon R. Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod Biomed Online. 2006;12(4):466–72.PubMedCrossRefGoogle Scholar
  30. 30.
    Grundler W, Kaiser F, Keilmann F, Walleczek J. Mechanisms of electromagnetic-interaction with cellular-systems. Naturwissenschaften. 1992;79(12):551–9.PubMedCrossRefGoogle Scholar
  31. 31.
    De Iuliis GN, Newey RJ, King BV, Aitken RJ. Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro. PLoS One. 2009;4(7):e6446.PubMedCrossRefGoogle Scholar
  32. 32.
    Naziroglu M, Gumral N. Modulator effects of l-carnitine and selenium on wireless devices (2.45 GHz)-induced oxidative stress and electroencephalography records in brain of rat. Int J Radiat Biol. 2009;85(8):680–9.PubMedCrossRefGoogle Scholar
  33. 33.
    Guney M, Ozguner F, Oral B, Karahan N, Mungan T. 900 MHz Radiofrequency-induced histopathologic changes and oxidative stress in rat endometrium: protection by vitamins E and C. Toxicol Ind Health. 2007;23(7):411–20.PubMedCrossRefGoogle Scholar
  34. 34.
    Ozguner F, Altinbas A, Ozaydin M, et al. Mobile phone-induced myocardial oxidative stress: protection by a novel antioxidant agent caffeic acid phenethyl ester. Toxicol Ind Health. 2005;21(9):223–30.PubMedCrossRefGoogle Scholar
  35. 35.
    Aitken RJ, Sawyer D. The human spermatozoon—not waving but drowning. Adv Exp Med Biol. 2002;518:85–98.CrossRefGoogle Scholar
  36. 36.
    Delamirande E, Gagnon C. Impact of reactive oxygen species on spermatozoa—a balancing act between beneficial and detrimental effects. Hum Reprod. 1995;10:15–21.Google Scholar
  37. 37.
    Aitken J, Fisher H. Reactive oxygen species generation and human spermatozoa—the balance of benefit and risk. Bioessays. 1994;16(4):259–67.PubMedCrossRefGoogle Scholar
  38. 38.
    Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction. 2001;122(4):497–506.PubMedCrossRefGoogle Scholar
  39. 39.
    Aitken RJ, De Iuliis GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2010;16(1):3–13.PubMedCrossRefGoogle Scholar
  40. 40.
    Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol Metab. 2008;93(8):3199–207.PubMedCrossRefGoogle Scholar
  41. 41.
    Agarwal A, Desai NR, Kesari KK. Pathophysiology of cell phone radiation: oxidative stress and carcinogenesis with focus on male reproductive system. Reprod Biol Endocrinol. 2009;7:114.PubMedCrossRefGoogle Scholar
  42. 42.
    Aitken RJ, De Iuliis GN, Finnie JM, Hedges A, McLachlan RI. Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum Reprod. 2010;25(10):2415–26.PubMedCrossRefGoogle Scholar
  43. 43.
    Zini A, Delamirande E, Gagnon C. Reactive oxygen species in semen of infertile patients—levels of superoxide dismutase-like and catalase-like activities in seminal plasma and spermatozoa. Int J Androl. 1993;16(3):183–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Irvine DS, Twigg JP, Gordon EL, Fulton N, Milne PA, Aitken RJ. DNA integrity in human spermatozoa: relationships with semen quality. J Androl. 2000;21(1):33–44.PubMedGoogle Scholar
  45. 45.
    Twigg J, Fulton N, Gomez E, Irvine DS, Aitken RJ. Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: lipid peroxidation, DNA fragmentation and effectiveness of antioxidants. Hum Reprod. 1998;13(6):1429–36.PubMedCrossRefGoogle Scholar
  46. 46.
    Kato Y, Osawa T. Detection of lipid-lysine amide-type adduct as a marker of PUFA oxidation and its applications. Arch Biochem Biophys. 2010;501(2):182–7.PubMedCrossRefGoogle Scholar
  47. 47.
    Makker K, Agarwal A, Sharma R. Oxidative stress & male infertility. Indian J Med Res. 2009;129(4):357–67.PubMedGoogle Scholar
  48. 48.
    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(4):350–5.PubMedCrossRefGoogle Scholar
  49. 49.
    Oral B, Guney M, Ozguner F, et al. Endometrial apoptosis induced by a 900-MHz mobile phone: preventive effects of vitamins E and C. Adv Ther. 2006;23(6):957–73.PubMedCrossRefGoogle Scholar
  50. 50.
    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(1–2):83–8.PubMedCrossRefGoogle Scholar
  51. 51.
    Verschaeve L, Juutilainen J, Lagroye I, Miyakoshi J, Saunders R, de Seze R, Tenforde T, van Rongen E, Veyret B, Xu Z. In vitro and in vivo genotoxicity of radiofrequency fields. Muta Res. 2010;705(3):252–68.PubMedCrossRefGoogle Scholar
  52. 52.
    Chia SE, Tay SK. Occupational risk for male infertility: a case-control study of 218 infertile and 227 fertile men. J Occup Environ Med. 2001;43(11):946–51.PubMedCrossRefGoogle Scholar
  53. 53.
    Fejes I, Zavaczki Z, Szollosi J, et al. Is there a relationship between cell phone use and semen quality? Arch Androl. 2005;51(5):385–93.PubMedCrossRefGoogle Scholar
  54. 54.
    Dasdag S, Ketani MA, Akdag Z, et al. Whole-body microwave exposure emitted by cellular phones and testicular function of rats. Urol Res. 1999;27(3):219–23.PubMedCrossRefGoogle Scholar
  55. 55.
    Hong R, Liu Y, Yu YM, Hu K, Weng EQ. [Effects of extremely low frequency electromagnetic fields on male reproduction in mice]. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi. 2003;21(5):342–5.PubMedGoogle Scholar
  56. 56.
    Lee JS, Ahn SS, Jung KC, Kim YW, Lee SK. Effects of 60 Hz electromagnetic field exposure on testicular germ cell apoptosis in mice. Asian J Androl. 2004;6(1):29–34.PubMedGoogle Scholar
  57. 57.
    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(3): 171–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Erogul O, Oztas E, Yildirim I, et al. Effects of electromagnetic radiation from a cellular phone on human sperm motility: an in vitro study. Arch Med Res. 2006;37(7):840–3.PubMedCrossRefGoogle Scholar
  59. 59.
    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(4):957–64.PubMedCrossRefGoogle Scholar
  60. 60.
    Wdowiak A, Wdowiak L, Wiktor H. Evaluation of the effect of using mobile phones on male fertility. Ann Agric Environ Med. 2007;14(1):169–72.PubMedGoogle Scholar
  61. 61.
    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(1):124–8.PubMedCrossRefGoogle Scholar
  62. 62.
    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. Bioelectromagnectics. 2002;23(2):113–26.CrossRefGoogle Scholar
  63. 63.
    d’Ambrosio G, Massa R, Scarfi MR & Zeni O. Cytogenetic damage in human lymphocytes following GMSK phase modulated microwave exposure. Bioelectromagnetics. 2002;23(1):7–13.CrossRefGoogle Scholar
  64. 64.
    Deepinder F, Makker K, Agarwal A. Cell phones and male infertility: dissecting the relationship. Reprod Biomed Online. 2007;15(3):266–70.PubMedCrossRefGoogle Scholar
  65. 65.
    Mailankot M, Kunnath AP, Jayalekshmi H, Koduru B, Valsalan R. 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 (Sao Paulo). 2009;64(6):561–5.CrossRefGoogle Scholar
  66. 66.
    Imai N, Kawabe M, Hikage T, Nojima T, Takahashi S, Shirai T. Effects on rat testis of 1.95-GHz W-CDMA for IMT-2000 cellular phones. Syst Biol Reprod Med. 2011;57(4):204–9.PubMedGoogle Scholar
  67. 67.
    Lee HJ, Pack JK, Kim TH, et al. The lack of histological changes of CDMA cellular phone-based radio frequency on rat testis. Bioelectromagnetics. 2010;31(7):528–34.PubMedCrossRefGoogle Scholar
  68. 68.
    Agarwal A, Desai NR, Makker K, et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril. 2009;92(4):1318–25.PubMedCrossRefGoogle Scholar
  69. 69.
    Desai NR, Kesari KK, Agarwal A. Pathophysiology of cell phone radiation: oxidative stress and carcinogenesis with focus on male reproductive system. Reprod Biol Endocrinol. 2009;7:114.PubMedCrossRefGoogle Scholar
  70. 70.
    Tomruk A, Guler G, Dincel AS. The influence of 1800 MHz GSM-like signals on hepatic oxidative DNA and lipid damage in nonpregnant, pregnant, and newly born rabbits. Cell Biochem Biophys. 2010;56(1):39–47.PubMedCrossRefGoogle Scholar
  71. 71.
    Sokolovic D, Djindjic B, Nikolic J, et al. Melatonin reduces oxidative stress induced by chronic exposure of microwave radiation from mobile phones in rat brain. J Radiat Res (Tokyo). 2008;49(6):579–86.CrossRefGoogle Scholar
  72. 72.
    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(4): 350–5.PubMedCrossRefGoogle Scholar
  73. 73.
    Seyhan N, Ozgur E, Guler G. Mobile phone radiation-induced free radical damage in the liver is inhibited by the antioxidants n-acetyl cysteine and epigallocatechin-gallate. Int J Radiat Biol. 2010;86(11):935–45.PubMedCrossRefGoogle Scholar
  74. 74.
    Phillips KP, Tanphaichitr N. Human exposure to endocrine disrupters and semen quality. J Toxicol Environ Health B Crit Rev. 2008;11(3–4):188–220.PubMedGoogle Scholar
  75. 75.
    Toppari J, Larsen JC, Christiansen P, et al. Male reproductive health and environmental xenoestrogens. Environ Health Perspect. 1996;104 Suppl 4:741–803.PubMedCrossRefGoogle Scholar
  76. 76.
    Agarwal A, Burns WR, Sabanegh E, Dada R, Rein B. Is male infertility a forerunner to cancer? Int Braz J Urol. 2010;36(5):527–36.PubMedCrossRefGoogle Scholar
  77. 77.
    Sharpe RM, Skakkebaek NE. Testicular dysgenesis syndrome: mechanistic insights and potential new downstream effects. Fertil Steril. 2008;89(2 Suppl):e33–8.PubMedCrossRefGoogle Scholar
  78. 78.
    Repacholi MH. Low-level exposure to radiofrequency electromagnetic fields: health effects and research needs. Bioelectromagnetics. 1998;19(1):1–19.PubMedCrossRefGoogle Scholar
  79. 79.
    Iorio R, Delle Monache S, Delle Monache S, Bennato F, et al. Involvement of mitochondrial activity in mediating ELF-EMF stimulatory effect on human sperm motility. Bioelectromagnetics. 2011;32(1):15–27.PubMedCrossRefGoogle Scholar
  80. 80.
    Mousavy SJ, Riazi GH, Kamarei M, et al. Effects of mobile phone radiofrequency on the structure and function of the normal human hemoglobin. Int J Biol Macromol. 2009;44(3):278–85.PubMedCrossRefGoogle Scholar
  81. 81.
    Gerner C, Haudek V, Schandl U, et al. Increased protein synthesis by cells exposed to a 1,800-MHz radio-frequency mobile phone electromagnetic field, detected by proteome profiling. Int Arch Occup Environ Health. 2010;83(6):691–702.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Geoffry N. De Iuliis
    • 1
  • Bruce V. King
    • 2
  • R. John Aitken
    • 3
  1. 1.Department of Biological SciencesUniversity of Newcastle, Life SciencesCallaghanAustralia
  2. 2.Department of Physics, School of Mathematical and Physical SciencesUniversity of NewcastleCallaghanAustralia
  3. 3.Department of Biological SciencesUniversity of NewcastleCallaghanAustralia

Personalised recommendations