Visn. Nac. Akad. Nauk Ukr. 2016. (2): 73-86

V.F. Chekhun1, І.L. Yakymenko1,2, О.S. Tsybulin3, E.P. Sidorik1, S.D. Kyrylenko4
1Kavetsky Institute of Experimental Pathology, Oncology and Radiobiology of NAS of Ukraine, Kyiv
2National University of Food Technologies, Kyiv
3Bila Tserkva National Agrarian University, Ukraine
4University of Campinas, Brazil


This review aims to analyze experimental data on biological effects of radiofrequency radiation. Recent experimental data indicate that the low-intensity radiofrequency radiation is able to interact with ions and local charges of molecules, potentially affects cell metabolism, leads to activation of free radical processes, accompanied by activation of peroxide processes, changes activity of antioxidant defense enzymes, and causes oxidative damage of DNA. This data allow to classify low-intensity radiofrequency radiation as an oxidative stress-factor for living cell.
Keywords: free radicals, oxidative stress, radiofrequency radiation, reactive oxygen species, DNA damage, apoptosis.


Language of article: ukrainian


  1. Maes W. Stress caused by electromagnetic fields and radiation. (Neubeuern, 2005).
  2. Hardell L., Carlberg M., Hansson M.K., Eriksson M. Case-control study on the use of mobile and cordless phones and the risk for malignant melanoma in the head and neck region. Pathophysiology. 2011. 18(4): 325.
  3. Hardell L., Carlberg M., Soderqvist F., Mild K.H., Morgan L.L. Long-term use of cellular phones and brain tumours: increased risk associated with use for > or =10 years. Occup. Environ. Med. 2007. 64(9): 626.
  4. Sadetzki S., Chetrit A., Jarus-Hakak A., Cardis E., Deutch Y., Duvdevani S., Zultan A., Novikov I., Freedman L.,Wolf M. Cellular phone use and risk of benign and malignant parotid gland tumors a nationwide case-control study. Am. J. Epidemiol. 2008. 167(4): 457.
  5. Sato Y., Akiba S., Kubo O.,Yamaguchi N. A case-case study of mobile phone use and acoustic neuroma risk in Japan. Bioelectromagnetics. 2011. 32(2): 85.
  6. Abdel-Rassoul G., El-Fateh O.A., Salem M.A., Michael A., Farahat F., El-Batanouny M.,Salem E. Neurobehavioral effects among inhabitants around mobile phone base stations. Neurotoxicology. 2007. 28(2): 434.
  7. Buchner K., Eger H. Changes of Clinically Important Neurotransmitters under the Influence of Modulated RF Fields.A Long-term Study under Real-life Conditions. Umwelt -Medizin-Gesellschaft. 2011. 24(1): 44.
  8. Chu M.K., Song H.G., Kim C.,Lee B.C. Clinical features of headache associated with mobile phone use. a cross-sectional study in university students. BMC Neurol. 2011. 11: 115.
  9. Agarwal A., Desai N.R., Makker K., Varghese A., Mouradi R., Sabanegh E., Sharma R. 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.
  10. Guidelines for limiting exposure to time-varying elecrtic, magnetic and electromagnetic fields (up to 300 GHz). Health Phys. 1998. 74(4): .494.
  11. Belyaev I. Dependence of non-thermal biological effects of microwaves on physical and biological variables. implications for reproducibility and safety standards. Eur. J. Oncol. Library. 2010. 5: 187.
  12. Consales C., Merla C., Marino C., Benassi B. Electromagnetic fields, oxidative stress, and neurodegeneration. Int. J. Cell Biol. 2012. 683897.
  13. Desai N.R., Kesari K.K., Agarwal A. Pathophysiology of cell phone radiation: oxidative stress and carcinogenesis with focus on male reproductive system. Reprod. Biol. Endocrinol. 2009. 7: 114.
  14. Yakymenko I., Sidorik E., Tsybulin O. Metabolic changes in living cells under electromagnetic radiation of mobile communication systems. Ukrainian Biochem. J. 2011. 83(2): 5. [in Russian].
  15. Hyland G.J. Physics and biology of mobile telephony. Lancet. 2000. 356(9244): 1833.
  16. Gandhi O.P., Morgan L.L., de Salles A.A., Han Y.Y., Herberman R.B., Davis D.L. Exposure limits. the underestimation of absorbed cell phone radiation, especially in children. Electromagn. Biol. Med. 2012. 31(1): 34.
  17. Panagopoulos D.J., Karabarbounis A., Margaritis L.H. Mechanism for action of electromagnetic fields on cells. Biochem. Biophys. Res. Commun. 2002. 298(1): 95.
  18. Goodman R., Blank M. Insights into electromagnetic interaction mechanisms. J. Cell Physiol. 2002. 192(1): 16.
  19. Blank M., Soo L. Electromagnetic acceleration of electron transfer reactions. J. Cell Biochem. 2001. 81(2): 278.<278::AID-JCB1042>3.0.CO;2-F
  20. Blank M., Soo L. Electromagnetic acceleration of the Belousov-Zhabotinski reaction. Bioelectrochemistry. 2003. 61(1): 93.
  21. Marino A.A., Carrubba S., Frilot C.,Chesson A.L. Evidence that transduction of electromagnetic field is mediated by a force receptor. Neurosci. Lett. 2009. 452(2): 119.
  22. Georgiou C.D. Oxidative stress-induced biological damage by low-level EMFs. Eur. J. Oncol. 2010. 5: 63.
  23. Céspedes O., Ueno S. Effects of radio frequency magnetic fields on iron release from cage proteins. Bioelectromagnetics. 2009. 30(5): 336.
  24. Zmyslony M., Politanski P., Rajkowska E., Szymczak W., Jajte J. Acute exposure to 930 MHz CW electromagnetic radiation in vitro affects reactive oxygen species level in rat lymphocytes treated by iron ions. Bioelectromagnetics. 2004. 25(5): 324.
  25. Bohr H., Bohr J. Microwave-enhanced folding and denaturation of globular proteins. Phys. Rev. E. 2000. 61: 4310.
  26. Budi A., Legge F.S., Treutlein H.,Yarovsky I. Effect of frequency on insulin response to electric field stress. J. Phys. Chem. B. 2007. 111(20): 5748.
  27. Pavicic I., Trosic I. Interaction of GSM modulated RF radiation and macromolecular cytoskeleton structures. In: Biological Effects of Electromagnetic Fields: Proc. 6th Int. Workshop (10–14 Oct. 2010, Bodrum, Turkey).
  28. Hoyto A., Juutilainen J.,Naarala J. Ornithine decarboxylase activity is affected in primary astrocytes but not in secondary cell lines exposed to 872 MHz RF radiation. Int. J. Radiat. Biol. 2007. 83(6): 367.
  29. Pall M.L. Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects. J. Cell. Mol. Med. 2013. 17(8): 958.
  30. Vaks V.L., Domrachev G.A., Rodygin Y.L., Selivanovskii D.A.,Spivak E.I. Dissociation of water by microwave radiation. Radiophys. Quantum Electron. 1994. 37(1): 85.
  31. Halliwell B. Biochemistry of oxidative stress. Biochem. Soc. Trans. 2007. 35: 1147.
  32. Halliwell B. Reactive oxygen species in living systems. source, biochemistry, and role in human disease. Am. J. Med. 1991. 91(3): 14S.
  33. Halliwell B., Gutteridge J.M. Biologically relevant metal ion-dependent hydroxyl radical generation. FEBS Lett. 1992. 307(1): 108.
  34. Halliwell B., Gutteridge J M. The importance of free radicals and catalytic metal ions in human diseases. Mol. Aspects Med. 1985. 8(2): 89.
  35. Halliwell B. Oxidants and human disease: some new concepts. FASEB J. 1987. 1(5): 358.
  36. Gutteridge J.M. Hydroxyl radicals, iron, oxidative stress, and neurodegeneration. Ann. N. Y. Acad. Sci. 1994. 738: 201.
  37. Feig D.I., Reid T.M., Loeb L.A. Reactive oxygen species in tumorigenesis. Cancer Res. 1994. 54: 1890s.
  38. Mates J.M. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology. 2000. 153(1): 83.
  39. 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(3): 559.
  40. Griendling K.K., Sorescu D., Ushio-Fukai M. NAD(P)H oxidase. role in cardiovascular biology and disease. Circ. Res. 2000. 86(5): 494.
  41. Low H., Crane F.L., Morre D.J. Putting together a plasma membrane NADH oxidase. Int. J. Biochem. Cell Biol. 2012. 44(11): 1834.
  42. Inoue M., Sato E.F., Nishikawa M., Park A.M., Kira Y., Imada I., Utsumi K. Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr. Med. Chem. 2003. 10(23): 2495.
  43. De Iuliis G.N., Newey R.J., King B.V., Aitken R.J. Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro. PLoS One. 2009. 4(7): e6446.
  44. Burlaka A., Tsybulin O., Sidorik E., Lukin S., Polishuk V., Tsehmistrenko S., Yakymenko I. Overproduction of free radical species in embryonal cells exposed to low intensity radiofrequency radiation. Exp. Oncol. 2013. 35(3): 219.
  45. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 2002. 80(5): 780.
  46. Guzy R.D., Schumacker P.T. Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp. Physiol. 2006. 91(5): 807.
  47. Wang X., Sharma R.K., Gupta A., George V., Thomas Jr. A.J., Falcone T., Agarwal A. Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study. Fertil. Steril. 2003. 80: 844.
  48. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis. 2007. 12(5): 913.
  49. Caraglia M., Marra M., Mancinelli F., D'Ambrosio G., Massa R., Giordano A., Budillon A., Abbruzzese A., Bismuto E. Electromagnetic fields at mobile phone frequency induce apoptosis and inactivation of the multi-chaperone complex in human epidermoid cancer cells. J. Cell Physiol. 2005. 204(2): 539.
  50. Zhao T.Y., Zou S.P.,Knapp P.E. Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. Neurosci. Lett. 2007. 412(1): 34.
  51. Yakymenko I., Tsybulin O., Sidorik E., Henshel D., Kyrylenko O., Kyrylenko S. Oxidative mechanisms of biological activity of low intensity radiofrequency radiation. Electromag. Biol. Med. 2015. PMID: 26151230.
  52. Avci B., Akar A., Bilgici B.,Tuncel O.K. Oxidative stress induced by 1.8 GHz radio frequency electromagnetic radiation and effects of garlic extract in rats. Int. J. Radiat. Biol. 2012. 88(11): 799.
  53. Bilgici B., Akar A., Avci B.,Tuncel O.K. Effect of 900 MHz radiofrequency radiation on oxidative stress in rat brain and serum. Electromagn. Biol. Med. 2013. 32(1): 20.
  54. 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): 83.
  55. Jelodar G., Akbari A., Nazifi S. The prophylactic effect of vitamin C on oxidative stress indexes in rat eyes following exposure to radiofrequency wave generated by a BTS antenna model. Int. J Radiat. Biol. 2013. 89(2): 128.
  56. Oral B., Guney M., Ozguner F., Karahan N., Mungan T., Comlekci S., Cesur G. Endometrial apoptosis induced by a 900-MHz mobile phone. preventive effects of vitamins E and C. Adv. Ther. 2006. 23(6): 957.
  57. Turker Y., Naziroglu M., Gumral N., Celik O., Saygin M., Comlekci S., Flores-Arce M. Selenium and L-carnitine reduce oxidative stress in the heart of rat induced by 2.45-GHz radiation from wireless devices. Biol. Trace Elem. Res. 2011. 143(3): 1640.
  58. Oksay T., Naziroğlu M., Doğan S., Güzel A., Gümral N., Koşar P.A. Protective effects of melatonin against oxidative injury in rat testis induced by wireless (2.45 GHz) devices. Andrologia. 2014. 46(1): 65.
  59. Guidelines on limits of exposure to static magnetic fields. Health Phys. 2009. 96: 504.
  60. Hong M.N., Kim B.C., Ko Y.G., Lee Y.S., Hong S.C., Kim T., Pack J.K., Choi H.D., Kim N., Lee J.S. Effects of 837 and 1950 MHz radiofrequency radiation exposure alone or combined on oxidative stress in MCF10A cells. Bioelectromagnetics. 2012. 33(7): 604.
  61. Kang K.A., Lee H.C., Lee J.J., Hong M.N., Park M.J., Lee Y.S., Choi H.D., Kim N., Ko Y.G., Lee J.S. Effects of combined radiofrequency radiation exposure on levels of reactive oxygen species in neuronal cells. J. Radiat. Res. 2014. 55(2): 265.
  62. Luukkonen J., Hakulinen P., Maki-Paakkanen J., Juutilainen J., Naarala J. Enhancement of chemically induced reactive oxygen species production and DNA damage in human SH-SY5Y neuroblastoma cells by 872 MHz radiofrequency radiation. Mutat. Res. 2009. 662(1): 54.
  63. Ruediger H.W. Genotoxic effects of radiofrequency electromagnetic fields. Pathophysiology. 2009. 16 89.
  64. Garaj-Vrhovac V., Fucic A., Horvat D. The correlation between the frequency of micronuclei and specific chromosome aberrations in human lymphocytes exposed to microwave radiation in vitro. Mutat. Res. 1992. 281(2): 181.
  65. Tice R.R., Hook G.G., Donner M., McRee D.I., Guy A.W. Genotoxicity of radiofrequency signals. I. Investigation of DNA damage and micronuclei induction in cultured human blood cells. Bioelectromagnetics. 2002. 23(2): 113.
  66. Zotti-Martelli L., Peccatori M., Maggini V., Ballardin M., Barale R. Individual responsiveness to induction of micronuclei in human lymphocytes after exposure in vitro to 1800-MHz microwave radiation. Mutat. Res. 2005. 582(1): 42.
  67. Garson O.M., McRobert T.L., Campbell L.J., Hocking B.A., Gordon I. A chromosomal study of workers with long-term exposure to radio-frequency radiation. Med. J. Aust. 1991. 155(5): 289.
  68. Kerbacher J.J., Meltz M.L., Erwin D.N. Influence of radiofrequency radiation on chromosome aberrations in CHO cells and its interaction with DNA-damaging agents. Radiat. Res. 1990. 123(3): 311.
  69. Maes A., Collier M.,Verschaeve L. Cytogenetic investigations on microwaves emitted by a 455.7 MHz car phone. Folia Biol. 2000. 46(5): 175.
  70. Baohong W., Jiliang H., Lifen J., Deqiang L., Wei Z., Jianlin L., Hongping D. Studying the synergistic damage effects induced by 1.8 GHz radiofrequency field radiation (RFR) with four chemical mutagens on human lymphocyte DNA using comet assay in vitro. Mutat. Res. 2005. 578(1): 149.
  71. Belyaev I.Y., Koch C.B., Terenius O., Roxstrom-Lindquist K., Malmgren L.O., W HS, Salford L.G., Persson B.R. 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(4): 295.
  72. Diem E., Schwarz C., Adlkofer F., Jahn O.,Rudiger H. 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. 2005. 583(2): 178.
  73. Kim J.Y., Hong S.Y., Lee Y.M., Yu S.A., Koh W.S., Hong J.R., Son T., Chang S.K., Lee M. In vitro assessment of clastogenicity of mobile-phone radiation (835 MHz) using the alkaline comet assay and chromosomal aberration test. Environ. Toxicol. 2008. 23(3): 319.
  74. Lai H., Singh N.P. Single- and double-strand DNA breaks in rat brain cells after acute exposure to radiofrequency electromagnetic radiation. Int. J. Radiat. Biol. 1996. 69(4): 513.
  75. Liu C., Duan W., Xu S., Chen C., He M., Zhang L., Yu Z., Zhou Z. Exposure to 1800 MHz radiofrequency electromagnetic radiation induces oxidative DNA base damage in a mouse spermatocyte-derived cell line. Toxicol. Lett. 2013. 218(1): 2.
  76. Guler G., Tomruk A., Ozgur E., Sahin D., Sepici A., Altan N., Seyhan N. The effect of radiofrequency radiation on DNA and lipid damage in female and male infant rabbits. Int. J. Radiat. Biol. 2012. 88(4): 367.
  77. Khalil A.M., Gagaa M.H.,Alshamali A.M. 8-Oxo-7, 8-dihydro-2'-deoxyguanosine as a biomarker of DNA damage by mobile phone radiation. Hum. Exp. Toxicol. 2012. 31(7): 734.
  78. Xu S., Zhou Z., Zhang L., Yu Z., Zhang W., Wang Y., Wang X., Li M., Chen Y., Chen C., He M., Zhang G., Zhong M. Exposure to 1800 MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain Res. 2010. 1311: 189.
  79. Halliwell B. Oxidative stress and cancer. have we moved forward? Biochem. J. 2007. 401(1): 1.
  80. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M.,Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007. 39(1): 44.
  81. Valko M., Rhodes C.J., Moncol J., Izakovic M., Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 2006. 160(1): 1.
  82. Forman H.J., Ursini F., Maiorino M. An overview of mechanisms of redox signaling. J. Mol. Cell. Cardiol. 2014. 73(2): 9.
  83. Sies H. Role of metabolic H2O2 generation: redox signaling and oxidative stress. J. Biol. Chem. 2014. 289(13): 8735.
  84. Oshino N., Jamieson D., Sugano T., Chance B. Optical measurement of the catalase-hydrogen peroxide intermediate (Compound I) in the liver of anaesthetized rats and its implication to hydrogen peroxide production in situ. Biochem. J. 1975. 146(1): 67.
  85. Enyedi B., Niethammer P. H2O2 a chemoattractant? Methods Enzymol. 2013. 528: 237.
  86. Hayden M.S.,Ghosh S. NF-kappaB in immunobiology. Cell Res. 2011. 21(2): 223.
  87. Tsybulin O., Sidorik E., Kyrylenko S., Henshel D., Yakymenko I. GSM 900 MHz microwave radiation affects embryo development of Japanese quails. Electromagn. Biol. Med. 2012. 31(1): 75.
  88. Tsybulin O., Sidorik E., Brieieva O., Buchynska L., Kyrylenko S., Henshel D.,Yakymenko I. GSM 900 MHz cellular phone radiation can either stimulate or depress early embryogenesis in Japanese quails depending on the duration of exposure. Int. J. Radiat. Biol. 2013. 89(9): 756.
  89. Calabrese E.J. Hormesis: why it is important to toxicology and toxicologists. Environ. Toxicol. Chem. 2008. 27(7): 1451.
  90. Johansson O. Electrohypersensitivity: state-of-the-art of a functional impairment. Electromagn. Biol. Med. 2006. 25(4): 245.
  91. Hallberg O., Oberfeld G. Letter to the editor: will we all become electrosensitive? Electromagn. Biol. Med. 2006. 25(3): 189.
  92. Yakymenko I., Sidorik E., Tsybulin O., Chekhun V. Potential risks of microwaves from mobile phones for youth health. Environ. Health. 2011. 56: 48.
  93. Santini R., Santini P., Danze J.M., Ruz P.L.,Seigne M. Study of the health of people living in the vicinity of mobile phone base stations. Influences of distance and sex. Pathol. Biol. 2002. 50(6): 369.
  94. Johansson O., Gangi S., Liang Y., Yoshimura K., Jing C., Liu P.-Y. Cutaneous mast cells are altered in normal healthy volunteers sitting in front of ordinary TVs/PCs – results from open-field provocation experiments. J. Cutan. Pathol. 2001. 28(10): 513.
  95. Nagata M. Inflammatory cells and oxygen radicals. Curr. Drug Targets Inflamm. Allergy. 2005. 4(4): 503.
  96. Okayama Y. Oxidative stress in allergic and inflammatory skin diseases. Curr. Drug Targets Inflamm. Allergy. 2005. 4(4): 517.
  97. Boldogh I., Bacsi A., Choudhury B.K., Dharajiya N., Alam R., Hazra T.K., Mitra S., Goldblum R.M., Sur S. ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation. J. Clin. Invest. 2005. 115(8): 2169.
  98. Yakymenko I., Sidorik E., Kyrylenko S., Chekhun V. Long-term exposure to microwave radiation provokes cancer growth: evidences from radars and mobile communication systems. Exp. Oncol. 2011. 33(2): 62.
  99. Wolf R.,Wolf D. Increased incidence of cancer near a cell-phone transmitted station. In: Trends in cancer prevention. (Nova Sci. Pub. Inc., 2007).
  100. Repacholi M.H., Basten A., Gebski V., Noonan D, Finnie J., Harris A.W. Lymphomas in E mu-Pim1 transgenic mice exposed to pulsed 900 MHZ electromagnetic fields. Radiat. Res. 1997. 147(5): 631.
  101. Hoyto A., Juutilainen J., Naarala J. Ornithine decarboxylase activity of L929 cells after exposure to continuous wave or 50 Hz modulated radiofrequency radiation--a replication study. Bioelectromagnetics. 2007. 28(7): 501.
  102. Clifford A., Morgan D., Yuspa S.H., Soler A.P., Gilmour S. Role of ornithine decarboxylase in epidermal tumorigenesis. Cancer Res. 1995. 55(8): 1680.
  103. Nguyen H.L., Zucker S., Zarrabi K., Kadam P., Schmidt C., Cao J. Oxidative stress and prostate cancer progression are elicited by membrane-type 1 matrix metalloproteinase. Mol. Cancer Res. 2011. 9(10): 1305.
  104. Ralph S.J., Rodríguez-Enríquez S., Neuzil J., Saavedra E., Moreno-Sánchez R. The causes of cancer revisited. “Mitochondrial malignancy” and ROS-induced oncogenic transformation.Why mitochondria are targets for cancer therapy. Mol. Aspects Med. 2010. 31(2): 145.