DOI QR코드

DOI QR Code

Possible Effects of Radiofrequency Electromagnetic Field Exposure on Central Nerve System

  • Kim, Ju Hwan (Department of Pharmacology, College of Medicine, Dankook University) ;
  • Lee, Jin-Koo (Department of Pharmacology, College of Medicine, Dankook University) ;
  • Kim, Hyung-Gun (Department of Pharmacology, College of Medicine, Dankook University) ;
  • Kim, Kyu-Bong (Department of Pharmacy, College of Pharmacy, Dankook University) ;
  • Kim, Hak Rim (Department of Pharmacology, College of Medicine, Dankook University)
  • Received : 2018.08.07
  • Accepted : 2018.11.06
  • Published : 2019.05.01

Abstract

Technological advances of mankind, through the development of electrical and communication technologies, have resulted in the exposure to artificial electromagnetic fields (EMF). Technological growth is expected to continue; as such, the amount of EMF exposure will continue to increase steadily. In particular, the use-time of smart phones, that have become a necessity for modern people, is steadily increasing. Social concerns and interest in the impact on the cranial nervous system are increased when considering the area where the mobile phone is used. However, before discussing possible effects of radiofrequency-electromagnetic field (RF-EMF) on the human body, several factors must be investigated about the influence of EMFs at the level of research using in vitro or animal models. Scientific studies on the mechanism of biological effects are also required. It has been found that RF-EMF can induce changes in central nervous system nerve cells, including neuronal cell apoptosis, changes in the function of the nerve myelin and ion channels; furthermore, RF-EMF act as a stress source in living creatures. The possible biological effects of RF-EMF exposure have not yet been proven, and there are insufficient data on biological hazards to provide a clear answer to possible health risks. Therefore, it is necessary to study the biological response to RF-EMF in consideration of the comprehensive exposure with regard to the use of various devices by individuals. In this review, we summarize the possible biological effects of RF-EMF exposure.

Keywords

References

  1. Abdel-Rassoul, G., El-Fateh, O. A., Salem, M. A., Michael, A., Farahat, F., El-Batanouny, M. and Salem, E. (2007) Neurobehavioral effects among inhabitants around mobile phone base stations. Neurotoxicology 28, 434-440. https://doi.org/10.1016/j.neuro.2006.07.012
  2. Al-Sarraf, H. and Philip, L. (2003) Effect of hypertension on the integrity of blood brain and blood CSF barriers, cerebral blood flow and CSF secretion in the rat. Brain Res. 975, 179-188. https://doi.org/10.1016/S0006-8993(03)02632-5
  3. Aldad, T. S., Gan, G., Gao, X.-B. and Taylor, H. S. (2012) Fetal radiofrequency radiation exposure from 800-1900 Mhz-rated cellular telephones affects neurodevelopment and behavior in mice. Sci. Rep. 2, 312. https://doi.org/10.1038/srep00312
  4. Altun, G., Deniz, O. G., Yurt, K. K., Davis, D. and Kaplan, S. (2018) Effects of mobile phone exposure on metabolomics in the male and female reproductive systems. Environ. Res. 167, 700-707. https://doi.org/10.1016/j.envres.2018.02.031
  5. Ammari, M., Jeljeli, M., Maaroufi, K., Roy, V., Sakly, M. and Abdelmelek, H. (2008) Static magnetic field exposure affects behavior and learning in rats. Electromagn. Biol. Med. 27, 185-196. https://doi.org/10.1080/15368370802072158
  6. Arendash, G. W., Sanchez-Ramos, J., Mori, T., Mamcarz, M., Lin, X., Runfeldt, M., Wang, L., Zhang, G., Sava, V., Tan, J. and Cao, C. (2010) Electromagnetic field treatment protects against and reverses cognitive impairment in Alzheimer's disease mice. J. Alzheimers Dis. 19, 191-210. https://doi.org/10.3233/JAD-2010-1228
  7. Baan, R., Grosse, Y., Lauby-Secretan, B., El Ghissassi, F., Bouvard, V., Benbrahim-Tallaa, L., Guha, N., Islami, F., Galichet, L. and Straif, K. (2011) Carcinogenicity of radiofrequency electromagnetic fields. Lancet Oncol. 12, 624-626. https://doi.org/10.1016/S1470-2045(11)70147-4
  8. Banaceur, S., Banasr, S., Sakly, M. and Abdelmelek, H. (2013) Whole body exposure to 2.4 GHz WIFI signals: effects on cognitive impairment in adult triple transgenic mouse models of Alzheimer's disease (3xTg-AD). Behav. Brain Res. 240, 197-201. https://doi.org/10.1016/j.bbr.2012.11.021
  9. Barr, R., Jones, D. L. and Rodger, C. J. (2000) ELF and VLF radio waves. J. Atmospheric Sol.-Terr. Phys. 62, 1689-1718. https://doi.org/10.1016/S1364-6826(00)00121-8
  10. Barthelemy, A., Mouchard, A., Bouji, M., Blazy, K., Puigsegur, R. and Villegier, A.-S. (2016) Glial markers and emotional memory in rats following acute cerebral radiofrequency exposures. Environ. Sci. Pollut. Res. Int. 23, 25343-25355. https://doi.org/10.1007/s11356-016-7758-y
  11. Belpomme, D., Campagnac, C. and Irigaray, P. (2015) Reliable disease biomarkers characterizing and identifying electrohypersensitivity and multiple chemical sensitivity as two etiopathogenic aspects of a unique pathological disorder. Rev. Environ. Health 30, 251-271. https://doi.org/10.1515/reveh-2015-0027
  12. Benson, V. S., Pirie, K., Schuz, J., Reeves, G. K., Beral, V. and Green, J. (2013) Mobile phone use and risk of brain neoplasms and other cancers: prospective study. Int. J. Epidemiol. 42, 792-802. https://doi.org/10.1093/ije/dyt072
  13. Bhatheja, K. and Field, J. (2006) Schwann cells: origins and role in axonal maintenance and regeneration. Int. J. Biochem. Cell Biol. 38, 1995-1999. https://doi.org/10.1016/j.biocel.2006.05.007
  14. Birks, L., Guxens, M., Papadopoulou, E., Alexander, J., Ballester, F., Estarlich, M., Gallastegi, M., Ha, M., Haugen, M., Huss, A., Kheifets, L., Lim, H., Olsen, J., Santa-Marina, L., Sudan, M., Vermeulen, R., Vrijkotte, T., Cardis, E. and Vrijheid, M. (2017) Maternal cell phone use during pregnancy and child behavioral problems in five birth cohorts. Environ. Int. 104, 122-131. https://doi.org/10.1016/j.envint.2017.03.024
  15. Birks, L. E., Struchen, B., Eeftens, M., Van Wel, L., Huss, A., Gajsek, P., Kheifets, L., Gallastegi, M., Dalmau-Bueno, A., Estarlich, M., Fernandez, M. F., Meder, I. K., Ferrero, A., Jimenez-Zabala, A., Torrent, M., Vrijkotte, T. G. M., Cardis, E., Olsen, J., Valic, B., Vermeulen, R., Vrijheid, M., Roosli, M. and Guxens, M. (2018) Spatial and temporal variability of personal environmental exposure to radio frequency electromagnetic fields in children in Europe. Environ. Int. 117, 204-214. https://doi.org/10.1016/j.envint.2018.04.026
  16. Bouji, M., Lecomte, A., Gamez, C., Blazy, K. and Villegier, A. S. (2016) Neurobiological effects of repeated radiofrequency exposures in male senescent rats. Biogerontology 17, 841-857. https://doi.org/10.1007/s10522-016-9654-8
  17. Braune, S., Wrocklage, C., Raczek, J., Gailus, T. and Lucking, C. H. (1998) Resting blood pressure increase during exposure to a radiofrequency electromagnetic field. Lancet 351, 1857-1858. https://doi.org/10.1016/S0140-6736(98)24025-6
  18. Buckner, C. A., Buckner, A. L., Koren, S. A., Persinger, M. A. and Lafrenie, R. M. (2015) Inhibition of cancer cell growth by exposure to a specific time-varying electromagnetic field involves T-type calcium channels. PLoS ONE 10, e0124136. https://doi.org/10.1371/journal.pone.0124136
  19. Calvente, I., Perez-Lobato, R., Nunez, M.-I., Ramos, R., Guxens, M., Villalba, J., Olea, N. and Fernandez, M. F. (2016) Does exposure to environmental radiofrequency electromagnetic fields cause cognitive and behavioral effects in 10-year-old boys? Bioelectromagnetics 37, 25-36. https://doi.org/10.1002/bem.21951
  20. Cassel, J. C., Cosquer, B., Galani, R. and Kuster, N. (2004) Whole-body exposure to 2.45 GHz electromagnetic fields does not alter radial-maze performance in rats. Behav. Brain Res. 155, 37-43. https://doi.org/10.1016/j.bbr.2004.03.031
  21. Cobb, B. L., Jauchem, J. R. and Adair, E. R. (2004) Radial arm maze performance of rats following repeated low level microwave radiation exposure. Bioelectromagnetics 25, 49-57. https://doi.org/10.1002/bem.10148
  22. Cosquer, B., Vasconcelos, A. P., Frohlich, J. and Cassel, J. C. (2005) Blood-brain barrier and electromagnetic fields: effects of scopolamine methylbromide on working memory after whole-body exposure to 2.45 GHz microwaves in rats. Behav. Brain Res. 161, 229-237. https://doi.org/10.1016/j.bbr.2005.02.025
  23. Cucurachi, S., Tamis, W. L. M., Vijver, M. G., Peijnenburg, W. J. G. M., Bolte, J. F. B. and De Snoo, G. R. (2013) A review of the ecological effects of radiofrequency electromagnetic fields (RF-EMF). Environ. Int. 51, 116-140. https://doi.org/10.1016/j.envint.2012.10.009
  24. Cui, Y., Liu, X., Yang, T., Mei, Y.-A. and Hu, C. (2014) Exposure to extremely low-frequency electromagnetic fields inhibits T-type calcium channels via AA/LTE4 signaling pathway. Cell Calcium. 55, 48-58. https://doi.org/10.1016/j.ceca.2013.11.002
  25. D'andrea, J. A., Chou, C. K., Johnston, S. A. and Adair, E. R. (2003) Microwave effects on the nervous system. Bioelectromagnetics Suppl 6, S107-S147.
  26. Danker-Hopfe, H., Dorn, H., Bolz, T., Peter, A., Hansen, M.-L., Eggert, T. and Sauter, C. (2016) Effects of mobile phone exposure (GSM 900 and WCDMA/UMTS) on polysomnography based sleep quality: an intra- and inter-individual perspective. Environ. Res. 145, 50-60. https://doi.org/10.1016/j.envres.2015.11.011
  27. Demsia, G., Vlastos, D. and Matthopoulos, D. P. (2004) Effect of 910-MHz electromagnetic field on rat bone marrow. ScientificWorldJournal 4 Suppl 2, 48-54.
  28. Dubreuil, D., Jay, T. and Edeline, J. M. (2002) Does head-only exposure to GSM-900 electromagnetic fields affect the performance of rats in spatial learning tasks? Behav. Brain Res. 129, 203-210. https://doi.org/10.1016/S0166-4328(01)00344-8
  29. Dubreuil, D., Jay, T. and Edeline, J. M. (2003) Head-only exposure to GSM 900-MHz electromagnetic fields does not alter rat's memory in spatial and non-spatial tasks. Behav. Brain Res. 145, 51-61. https://doi.org/10.1016/S0166-4328(03)00100-1
  30. Elder, J. A. (2003) Ocular effects of radiofrequency energy. Bioelectromagnetics Suppl 6, S148-S161.
  31. Elliott, P., Toledano, M. B., Bennett, J., Beale, L., De Hoogh, K., Best, N. and Briggs, D. J. (2010) Mobile phone base stations and early childhood cancers: case-control study. BMJ 340, c3077. https://doi.org/10.1136/bmj.c3077
  32. Falzone, N., Huyser, C., Becker, P., Leszczynski, D. and Franken, D. R. (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, 20-26. https://doi.org/10.1111/j.1365-2605.2010.01054.x
  33. Feng, Y., He, D., Yao, Z. and Klionsky, D. J. (2014) The machinery of macroautophagy. Cell Res. 24, 24-41. https://doi.org/10.1038/cr.2013.168
  34. Franke, H., Ringelstein, E. B. and Stogbauer, F. (2005) Electromagnetic fields (GSM 1800) do not alter blood-brain barrier permeability to sucrose in models in vitro with high barrier tightness. Bioelectromagnetics 26, 529-535. https://doi.org/10.1002/bem.20123
  35. Frey, A. H. (1998) Headaches from cellular telephones: are they real and what are the implications? Environ. Health Perspect. 106, 101-103. https://doi.org/10.1289/ehp.98106101
  36. Fritze, K., Sommer, C., Schmitz, B., Mies, G., Hossmann, K. A., Kiessling, M. and Wiessner, C. (1997) Effect of global system for mobile communication (GSM) microwave exposure on blood-brain barrier permeability in rat. Acta Neuropathol. 94, 465-470. https://doi.org/10.1007/s004010050734
  37. Fujimoto, C., Iwasaki, S., Urata, S., Morishita, H., Sakamaki, Y., Fujioka, M., Kondo, K., Mizushima, N. and Yamasoba, T. (2017) Autophagy is essential for hearing in mice. Cell Death Dis. 8, e2780. https://doi.org/10.1038/cddis.2017.194
  38. Gruber, M. J., Palmquist, E. and Nordin, S. (2018) Characteristics of perceived electromagnetic hypersensitivity in the general population. Scand. J. Psychol. 59, 422-427. https://doi.org/10.1111/sjop.12449
  39. Hardell, L., Carlberg, M. and Hansson Mild, K. (2005) Use of cellular telephones and brain tumour risk in urban and rural areas. Occup. Environ. Med. 62, 390-394. https://doi.org/10.1136/oem.2004.017434
  40. Hardell, L., Carlberg, M., Soderqvist, F., Mild, K. H. and Morgan, L. L. (2007) Long-term use of cellular phones and brain tumours: increased risk associated with use for > or =10 years. Occup. Environ. Med. 64, 626-632. https://doi.org/10.1136/oem.2006.029751
  41. Hinrikus, H., Bachmann, M. and Lass, J. (2018) Understanding physical mechanism of low-level microwave radiation effect. Int. J. Radiat. Biol. 94, 877-882. https://doi.org/10.1080/09553002.2018.1478158
  42. Hoeijmakers, J. H. (2009) DNA damage, aging, and cancer. N. Engl. J. Med. 361,1475-1485. https://doi.org/10.1056/NEJMra0804615
  43. Hollenbach, D. F. and Herndon, J. M. (2001) Deep-earth reactor: nuclear fission, helium, and the geomagnetic field. Proc. Natl. Acad. Sci. U. S. A. 98, 11085-11090. https://doi.org/10.1073/pnas.201393998
  44. Hossmann, K. A. and Hermann, D. M. (2003) Effects of electromagnetic radiation of mobile phones on the central nervous system. Bioelectromagnetics 24, 49-62. https://doi.org/10.1002/bem.10068
  45. Hutter, H. P., Moshammer, H., Wallner, P. and Kundi, M. (2006) Subjective symptoms, sleeping problems, and cognitive performance in subjects living near mobile phone base stations. Occup. Environ. Med. 63, 307-313. https://doi.org/10.1136/oem.2005.020784
  46. ICNIRP (1998) Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz). International Commission on Non-Ionizing Radiation Protection. Health Phys. 74, 494-522.
  47. Ikinci, A., Mercantepe, T., Unal, D., Erol, H. S., Sahin, A., Aslan, A., Baş, O., Erdem, H., Sonmez, O. F., Kaya, H. and Odaci, E. (2016) Morphological and antioxidant impairments in the spinal cord of male offspring rats following exposure to a continuous 900MHz electromagnetic field during early and mid-adolescence. J. Chem. Neuroanat. 75, 99-104. https://doi.org/10.1016/j.jchemneu.2015.11.006
  48. Jeong, Y. J., Kang, G.-Y., Kwon, J. H., Choi, H.-D., Pack, J.-K., Kim, N., Lee, Y.-S. and Lee, H.-J. (2015) 1950 MHz electromagnetic fields ameliorate a${\beta}$ pathology in Alzheimer's disease mice. Curr. Alzheimer Res. 12, 481-492. https://doi.org/10.2174/156720501205150526114448
  49. Jiang, D.-P., Li, J.-H,. Zhang, J., Xu, S.-L., Kuang, F., Lang, H.-Y., Wang, Y.-F., An, G.-Z., Li, J. and Guo, G.-Z. (2016) Long-term electromagnetic pulse exposure induces Abeta deposition and cognitive dysfunction through oxidative stress and overexpression of APP and BACE1. Brain Res. 1642, 10-19. https://doi.org/10.1016/j.brainres.2016.02.053
  50. Jirik, V., Pekarek, L., Janout, V. and Tomaskova, H. (2012) Association between childhood leukaemia and exposure to power-frequency magnetic fields in Middle Europe. Biomed. Environ. Sci. 25, 597-601. https://doi.org/10.3967/0895-3988.2012.05.015
  51. Johansson, O. and Redmayne, M. (2016) Exacerbation of demyelinating syndrome after exposure to wireless modem with public hotspot. Electromagn. Biol. Med. 35, 393-397. https://doi.org/10.3109/15368378.2015.1107839
  52. Kazemi, E., Mortazavi, S. M. J., Ali-Ghanbari, A., Sharifzadeh, S., Ranjbaran, R., Mostafavi-Pour, Z., Zal, F. and Haghani, M. (2015) Effect of 900 MHz electromagnetic radiation on the induction of ROS in human peripheral blood mononuclear cells. J. Biomed. Phys. Eng. 5, 105-114.
  53. Kim, J.-Y., Hong, S.-Y., Lee, Y.-M., Yu, S.-A., Koh, W. S., Hong, J.-R., Son, T., Chang, S.-K. and Lee, M. (2008) In vitro assessment of clastogenicity of mobile-phone radiation (835 MHz) using the alkaline comet assay and chromosomal aberration test. Environ. Toxicol. 23, 319-327. https://doi.org/10.1002/tox.20347
  54. Kim, J. H., Huh, Y. H. and Kim, H. R. (2016) Induction of autophagy in the striatum and hypothalamus of mice after 835 MHz radiofrequency exposure. PLoS ONE 11, e0153308. https://doi.org/10.1371/journal.pone.0153308
  55. Kim, J. H., Kim, H.-J., Yu, D.-H., Kweon, H.-S., Huh, Y. H. and Kim, H. R. (2017a) Changes in numbers and size of synaptic vesicles of cortical neurons induced by exposure to 835 MHz radiofrequencyelectromagnetic field. PLoS ONE 12, e0186416. https://doi.org/10.1371/journal.pone.0186416
  56. Kim, J. H., Sohn, U. D., Kim, H.-G. and Kim, H. R. (2018a) Exposure to 835 MHz RF-EMF decreases the expression of calcium channels, inhibits apoptosis, but induces autophagy in the mouse hippocampus. Korean J. Physiol. Pharmacol. 22, 277-289. https://doi.org/10.4196/kjpp.2018.22.3.277
  57. Kim, J. H., Yu, D. H., Huh, Y. H., Lee, E. H., Kim, H. G. and Kim, H. R. (2017b) Long-term exposure to 835 MHz RF-EMF induces hyperactivity, autophagy and demyelination in the cortical neurons of mice. Sci. Rep. 7, 41129. https://doi.org/10.1038/srep41129
  58. Kim, J. H., Yu, D. H., Kim, H. J., Huh, Y. H., Cho, S. W., Lee, J. K., Kim, H. G. and Kim, H. R. (2018b) Exposure to 835 MHz radiofrequency electromagnetic field induces autophagy in hippocampus but not in brain stem of mice. Toxicol. Ind. Health 34, 23-35. https://doi.org/10.1177/0748233717740066
  59. Kleinerman, R. A., Linet, M. S., Hatch, E. E., Wacholder, S., Tarone, R. E., Severson, R. K., Kaune, W. T., Friedman, D. R., Haines, C. M., Muirhead, C. R., Boice, J. D. J. and Robison, L. L. (1997) Magnetic field exposure assessment in a case-control study of childhood leukemia. Epidemiology 8, 575-583. https://doi.org/10.1097/00001648-199709000-00017
  60. Kleinlogel, H., Dierks, T., Koenig, T., Lehmann, H., Minder, A. and Berz, R. (2008) Effects of weak mobile phone - electromagnetic fields (GSM, UMTS) on event related potentials and cognitive functions. Bioelectromagnetics 29, 488-497. https://doi.org/10.1002/bem.20418
  61. Kolodynski, A. A. and Kolodynska, V. V. (1996) Motor and psychological functions of school children living in the area of the Skrunda Radio Location Station in Latvia. Sci. Total Environ. 180, 87-93. https://doi.org/10.1016/0048-9697(95)04924-X
  62. Kumlin, T., Iivonen, H., Miettinen, P., Juvonen, A., Van Groen, T., Puranen, L., Pitkaaho, R., Juutilainen, J. and Tanila, H. (2007) Mobile phone radiation and the developing brain: behavioral and morphological effects in juvenile rats. Radiat. Res. 168, 471-479. https://doi.org/10.1667/RR1002.1
  63. Kuribayashi, M., Wang, J., Fujiwara, O., Doi, Y., Nabae, K., Tamano, S., Ogiso, T., Asamoto, M. and Shirai, T. (2005) Lack of effects of 1439 MHz electromagnetic near field exposure on the blood-brain barrier in immature and young rats. Bioelectromagnetics 26, 578-588. https://doi.org/10.1002/bem.20138
  64. Kuybulu, A. E., Oktem, F., Eiris, I. M., Sutcu, R., Ormeci, A. R., Eomlekci, S. and Uz, E. (2016) Effects of long-term pre- and post-natal exposure to 2.45 GHz wireless devices on developing male rat kidney. Ren. Fail. 38, 571-580. https://doi.org/10.3109/0886022X.2016.1148937
  65. Lagiou, P., Tamimi, R., Lagiou, A., Mucci, L. and Trichopoulos, D. (2002) Is epidemiology implicating extremely low frequency electric and magnetic fields in childhood leukemia? Environ. Health Prev. Med. 7, 33-39. https://doi.org/10.1007/BF02897328
  66. Lai, H., Carino, M. A., Horita, A. and Guy, A. W. (1992) Single vs. repeated microwave exposure: effects on benzodiazepine receptors in the brain of the rat. Bioelectromagnetics 13, 57-66. https://doi.org/10.1002/bem.2250130107
  67. Lai, H., Horita, A. and Guy, A. W. (1994) Microwave irradiation affects radial-arm maze performance in the rat. Bioelectromagnetics 15, 95-104. https://doi.org/10.1002/bem.2250150202
  68. Lai, H. and Singh, N. P. (2004) Magnetic-field-induced DNA strand breaks in brain cells of the rat. Environ. Health Perspect. 112, 687-694. https://doi.org/10.1289/ehp.6355
  69. Langer, C. E., De Llobet, P., Dalmau, A., Wiart, J., Goedhart, G., Hours, M., Benke, G. P., Bouka, E., Bruchim, R., Choi, K.-H., Eng, A., Ha, M., Karalexi, M., Kiyohara, K., Kojimahara, N., Krewski, D., Kromhout, H., Lacour, B. T., Mannetje, A., Maule, M., Migliore, E., Mohipp, C., Momoli, F., Petridou, E., Radon, K., Remen, T., Sadetzki, S., Sim, M. R., Weinmann, T., Vermeulen, R., Cardis, E. and Vrijheid, M. (2017) Patterns of cellular phone use among young people in 12 countries: Implications for RF exposure. Environ. Int. 107, 65-74. https://doi.org/10.1016/j.envint.2017.06.002
  70. Lee, S., Johnson, D., Dunbar, K., Dong, H., Ge, X., Kim, Y. C., Wing, C., Jayathilaka, N., Emmanuel, N., Zhou, C. Q., Gerber, H. L., Tseng, C. C. and Wang, S. M. (2005) 2.45 GHz radiofrequency fields alter gene expression in cultured human cells. FEBS Lett. 579, 4829-4836. https://doi.org/10.1016/j.febslet.2005.07.063
  71. Leitgeb, N. (2011) Comparative health risk assessment of electromagnetic fields. Wien. Med. Wochenschr. 161, 251-262. https://doi.org/10.1007/s10354-011-0884-8
  72. Ma, Q., Chen, C., Deng, P., Zhu, G., Lin, M., Zhang, L., Xu, S., He, M., Lu, Y., Duan, W., Pi, H., Cao, Z., Pei, L., Li, M., Liu, C., Zhang, Y., Zhong, M., Zhou, Z. and Yu, Z. (2016) Extremely low-frequency electromagnetic fields promote in vitro neuronal differentiation and neurite outgrowth of embryonic neural stem cells via up-regulating TRPC1. PLoS ONE 11, e0150923. https://doi.org/10.1371/journal.pone.0150923
  73. Magras, I. N. and Xenos, T. D. (1997) RF radiation-induced changes in the prenatal development of mice. Bioelectromagnetics 18, 455-461. https://doi.org/10.1002/(SICI)1521-186X(1997)18:6<455::AID-BEM8>3.0.CO;2-1
  74. Mann, K., Wagner, P., Brunn, G., Hassan, F., Hiemke, C. and Roschke, J. (1998) Effects of pulsed high-frequency electromagnetic fields on the neuroendocrine system. Neuroendocrinology 67, 139-144. https://doi.org/10.1159/000054308
  75. Marchesi, N., Osera, C., Fassina, L., Amadio, M., Angeletti, F., Morini, M., Magenes, G., Venturini, L., Biggiogera, M., Ricevuti, G., Govoni, S., Caorsi, S., Pascale, A. and Comincini, S. (2014) Autophagy is modulated in human neuroblastoma cells through direct exposition to low frequency electromagnetic fields. J. Cell Physiol. 229, 1776-1786. https://doi.org/10.1002/jcp.24631
  76. Mashevich, M., Folkman, D., Kesar, A., Barbul, A., Korenstein, R., Jerby, E. and Avivi, L. (2003) Exposure of human peripheral blood lymphocytes to electromagnetic fields associated with cellular phones leads to chromosomal instability. Bioelectromagnetics 24, 82-90. https://doi.org/10.1002/bem.10086
  77. Medina-Fernandez, F. J., Escribano, B. M., Aguera, E., Aguilar-Luque, M., Feijoo, M., Luque, E., Garcia-Maceira, F. I., Pascual-Leone, A., Drucker-Colin, R. and Tunez, I. (2017) Effects of transcranial magnetic stimulation on oxidative stress in experimental autoimmune encephalomyelitis. Free Radic. Res. 51, 460-469. https://doi.org/10.1080/10715762.2017.1324955
  78. Micheau, J. and Van Marrewijk, B. (1999) Stimulation of 5-HT1A receptors by systemic or medial septum injection induces anxiogenic-like effects and facilitates acquisition of a spatial discrimination task in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 23, 1113-1133. https://doi.org/10.1016/S0278-5846(99)00057-3
  79. Millan, M. J. (2003) The neurobiology and control of anxious states. Prog. Neurobiol. 70, 83-244. https://doi.org/10.1016/S0301-0082(03)00087-X
  80. Morgan, L. L., Miller, A. B., Sasco, A. and Davis, D. L. (2015) Mobile phone radiation causes brain tumors and should be classified as a probable human carcinogen (2A) (review). Int. J. Oncol. 46, 1865-1871. https://doi.org/10.3892/ijo.2015.2908
  81. Morris, R. G., Garrud, P., Rawlins, J. N. and O'keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683. https://doi.org/10.1038/297681a0
  82. Mortazavi, S. A., Tavakkoli-Golpayegani, A., Haghani, M. and Mortazavi, S. M. (2014) Looking at the other side of the coin: the search for possible biopositive cognitive effects of the exposure to 900 MHz GSM mobile phone radiofrequency radiation. J. Environ. Health Sci. Eng. 12, 75. https://doi.org/10.1186/2052-336X-12-75
  83. Moser, E. I., Krobert, K. A., Moser, M. B. and Morris, R. G. (1998) Impaired spatial learning after saturation of long-term potentiation. Science 281, 2038-2042. https://doi.org/10.1126/science.281.5385.2038
  84. Moulder, J. E., Foster, K. R., Erdreich, L. S. and Mcnamee, J. P. (2005) Mobile phones, mobile phone base stations and cancer: a review. Int. J. Radiat. Biol. 81, 189-203. https://doi.org/10.1080/09553000500091097
  85. Myung, S. K., Ju, W., Mcdonnell, D. D., Lee, Y. J., Kazinets, G., Cheng, C. T. and Moskowitz, J. M. (2009) Mobile phone use and risk of tumors: a meta-analysis. J. Clin. Oncol. 27, 5565-5572. https://doi.org/10.1200/JCO.2008.21.6366
  86. Nanou, E. and Catterall, W. A. (2018) Calcium channels, synaptic plasticity, and neuropsychiatric disease. Neuron 98, 466-481. https://doi.org/10.1016/j.neuron.2018.03.017
  87. Neher, E. and Sakaba, T. (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861-872. https://doi.org/10.1016/j.neuron.2008.08.019
  88. Nittby, H., Brun, A., Eberhardt, J., Malmgren, L., Persson, B. R. and Salford, L. G. (2009) Increased blood-brain barrier permeability in mammalian brain 7 days after exposure to the radiation from a GSM-900 mobile phone. Pathophysiology 16, 103-112. https://doi.org/10.1016/j.pathophys.2009.01.001
  89. Nixon, R. A. (2013) The role of autophagy in neurodegenerative disease. Nat. Med. 19, 983-997. https://doi.org/10.1038/nm.3232
  90. Ohtani, S., Ushiyama, A., Maeda, M., Ogasawara, Y., Wang, J., Kunugita, N. and Ishii, K. (2015) The effects of radio-frequency electromagnetic fields on T cell function during development. J. Radiat. Res. 56, 467-474. https://doi.org/10.1093/jrr/rru126
  91. Oscar, K. J. and Hawkins, T. D. (1977) Microwave alteration of the blood-brain barrier system of rats. Brain Res. 126, 281-293. https://doi.org/10.1016/0006-8993(77)90726-0
  92. Pall, M. L. (2013) Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects. J. Cell. Mol. Med. 17, 958-965. https://doi.org/10.1111/jcmm.12088
  93. Pall, M. L. (2015) Scientific evidence contradicts findings and assumptions of Canadian Safety Panel 6: microwaves act through voltage-gated calcium channel activation to induce biological impacts at non-thermal levels, supporting a paradigm shift for microwave/lower frequency electromagnetic field action. Rev. Environ. Health 30, 99-116.
  94. Pchitskaya, E., Popugaeva, E. and Bezprozvanny, I. (2018) Calcium signaling and molecular mechanisms underlying neurodegenerative diseases. Cell Calcium 70, 87-94. https://doi.org/10.1016/j.ceca.2017.06.008
  95. Phillips, J. L., Singh, N. P. and Lai, H. (2009) Electromagnetic fields and DNA damage. Pathophysiology 16, 79-88. https://doi.org/10.1016/j.pathophys.2008.11.005
  96. Preece, A. W., Iwi, G., Davies-Smith, A., Wesnes, K., Butler, S., Lim, E. and Varey, A. (1999) Effect of a 915-MHz simulated mobile phone signal on cognitive function in man. Int. J. Radiat. Biol. 75, 447-456. https://doi.org/10.1080/095530099140375
  97. Ray, S. and Behari, J. (1990) Physiological changes in rats after exposure to low levels of microwaves. Radiat. Res. 123, 199-202. https://doi.org/10.2307/3577545
  98. Redmayne, M. and Johansson, O. (2014) Could myelin damage from radiofrequency electromagnetic field exposure help explain the functional impairment electrohypersensitivity? A review of the evidence. J. Toxicol. Environ. Health B Crit. Rev. 17, 247-258. https://doi.org/10.1080/10937404.2014.923356
  99. Repacholi, M. H., Lerchl, A., Roosli, M., Sienkiewicz, Z., Auvinen, A., Breckenkamp, J., D’inzeo, G., Elliott, P., Frei, P., Heinrich, S., Lagroye, I., Lahkola, A., Mccormick, D. L., Thomas, S. and Vecchia, P. (2012) Systematic review of wireless phone use and brain cancer and other head tumors. Bioelectromagnetics 33, 187-206. https://doi.org/10.1002/bem.20716
  100. Ruediger, H. W. (2009) Genotoxic effects of radiofrequency electromagnetic fields. Pathophysiology 16, 89-102. https://doi.org/10.1016/j.pathophys.2008.11.004
  101. Salford, L., Nittby, H., Brun, A., Grafstrom, G., Malmgren, L., Sommarin, M., Eberhardt, J., Widegren, B. and Persson, B. (2008) The mammalian brain in the electromagnetic fields designed by man with special reference to blood-brain barrier function, neuronal damage and possible physical mechanisms. Prog. Theor. Phys. Supp. 173, 283-309. https://doi.org/10.1143/PTPS.173.283
  102. Salford, L. G., Brun, A., Sturesson, K., Eberhardt, J. L. and Persson, B. R. (1994) Permeability of the blood-brain barrier induced by 915 MHz electromagnetic radiation, continuous wave and modulated at 8, 16, 50, and 200 Hz. Microsc. Res. Tech. 27, 535-542. https://doi.org/10.1002/jemt.1070270608
  103. Salford, L. G., Brun, A. E., Eberhardt, J. L., Malmgren, L. and Persson, B. R. (2003) Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ. Health Perspect. 111, 881-883; discussion A408. https://doi.org/10.1289/ehp.6039
  104. Santini, R., Santini, P., Danze, J. M., Le Ruz, P. and Seigne, M. (2002) Study of the health of people living in the vicinity of mobile phone base stations: I. Influences of distance and sex. Pathol. Biol. 50, 369-373. https://doi.org/10.1016/S0369-8114(02)00311-5
  105. Schmid, M. R., Loughran, S. P., Regel, S. J., Murbach, M., Bratic Grunauer, A., Rusterholz, T., Bersagliere, A., Kuster, N. and Achermann, P. (2012) Sleep EEG alterations: effects of different pulse-modulated radio frequency electromagnetic fields. J. Sleep Res. 21, 50-58. https://doi.org/10.1111/j.1365-2869.2011.00918.x
  106. Sherafat, M. A., Heibatollahi, M., Mongabadi, S., Moradi, F., Javan, M. and Ahmadiani, A. (2012) Electromagnetic field stimulation potentiates endogenous myelin repair by recruiting subventricular neural stem cells in an experimental model of white matter demyelination. J. Mol. Neurosci. 48, 144-153. https://doi.org/10.1007/s12031-012-9791-8
  107. Son, Y., Jeong, Y. J., Kwon, J. H., Choi, H. D., Pack, J. K., Kim, N., Lee, Y. S. and Lee, H. J. (2016) 1950 MHz radiofrequency electromagnetic fields do not aggravate memory deficits in 5xFAD mice. Bioelectromagnetics 37, 391-399. https://doi.org/10.1002/bem.21992
  108. Son, Y., Kim, J. S., Jeong, Y. J., Jeong, Y. K., Kwon, J. H., Choi, H.-D., Pack, J.-K., Kim, N., Lee, Y.-S. and Lee, H.-J. (2018) Long-term RF exposure on behavior and cerebral glucose metabolism in 5xFAD mice. Neurosci. Lett. 666, 64-69. https://doi.org/10.1016/j.neulet.2017.12.042
  109. Stam, R. (2010) Electromagnetic fields and the blood-brain barrier. Brain Res. Rev. 65, 80-97. https://doi.org/10.1016/j.brainresrev.2010.06.001
  110. Stewart, A., Rao, J. N., Middleton, J. D., Pearmain, P. and Evans, T. (2012) Mobile telecommunications and health: report of an investigation into an alleged cancer cluster in Sandwell, West Midlands. Perspect. Public Health 132, 299-304. https://doi.org/10.1177/1757913911427375
  111. Sun, Z.-C., Ge, J.-L., Guo, B., Guo, J., Hao, M., Wu, Y.-C., Lin, Y.-A., La, T., Yao, P.-T., Mei, Y.-A., Feng, Y. and Xue, L. (2016) Extremely low frequency electromagnetic fields facilitate vesicle endocytosis by increasing presynaptic calcium channel expression at a central synapse. Sci. Rep. 6, 21774. https://doi.org/10.1038/srep21774
  112. Sutton, C. H. and Carroll, F. B. (1979) Effects of microwave-induced hyperthermia on the blood-brain barrier of the rat. Radio Sci. 14, 329-334. https://doi.org/10.1029/RS014i06Sp00329
  113. Swerdlow, A. J., Feychting, M., Green, A. C., Leeka Kheifets, L. K. and Savitz, D. A. (2011) Mobile phones, brain tumors, and the interphone study: where are we now? Environ. Health Perspect. 119, 1534-1538. https://doi.org/10.1289/ehp.1103693
  114. Tattersall, J. E. H., Scott, I. R., Wood, S. J., Nettell, J. J., Bevir, M. K., Wang, Z., Somasiri, N. P. and Chen, X. (2001) Effects of low intensity radiofrequency electromagnetic fields on electrical activity in rat hippocampal slices. Brain Res. 904, 43-53. https://doi.org/10.1016/S0006-8993(01)02434-9
  115. Turedi, S., Kerimoglu, G., Mercantepe, T. and Odaci, E. (2017) Biochemical and pathological changes in the male rat kidney and bladder following exposure to continuous 900-MHz electromagnetic field on postnatal days 22-59. Int. J. Radiat. Biol. 93, 990-999. https://doi.org/10.1080/09553002.2017.1350768
  116. Volkow, N. D., Tomasi, D., Wang, G. J., Vaska, P., Fowler, J. S., Telang, F., Alexoff, D., Logan, J. and Wong, C. (2011) Effects of cell phone radiofrequency signal exposure on brain glucose metabolism. JAMA 305, 808-813. https://doi.org/10.1001/jama.2011.186
  117. Wagner, P., Roschke, J., Mann, K., Hiller, W. and Frank, C. (1998) Human sleep under the influence of pulsed radiofrequency electromagnetic fields: a polysomnographic study using standardized conditions. Bioelectromagnetics 19, 199-202. https://doi.org/10.1002/(SICI)1521-186X(1998)19:3<199::AID-BEM8>3.0.CO;2-X
  118. Wainwright, P. (2000) Thermal effects of radiation from cellular telephones. Phys. Med. Biol. 45, 2363-2372. https://doi.org/10.1088/0031-9155/45/8/321
  119. Wang, B. and Lai, H. (2000) Acute exposure to pulsed 2450-MHz microwaves affects water-maze performance of rats. Bioelectromagnetics 21, 52-56. https://doi.org/10.1002/(SICI)1521-186X(200001)21:1<52::AID-BEM8>3.0.CO;2-6
  120. Wyde, M. E., Horn, T. L., Capstick, M. H., Ladbury, J. M., Koepke, G., Wilson, P. F., Kissling, G. E., Stout, M. D., Kuster, N., Melnick, R. L., Gauger, J., Bucher, J. R. and Mccormick, D. L. (2018) Effect of cell phone radiofrequency radiation on body temperature in rodents: Pilot studies of the National Toxicology Program's reverberation chamber exposure system. Bioelectromagnetics 39, 190-199. https://doi.org/10.1002/bem.22116
  121. Xu, S., Ning, W., Xu, Z., Zhou, S., Chiang, H. and Luo, J. (2006) Chronic exposure to GSM 1800-MHz microwaves reduces excitatory synaptic activity in cultured hippocampal neurons. Neurosci. Lett. 398, 253-257. https://doi.org/10.1016/j.neulet.2006.01.004
  122. Xu, S., Zhou, Z., Zhang, L., Yu, Z., Zhang, W., Wang, Y., Wang, X., Li, M., Chen, Y., Chen, C., He, M., Zhang, G. and Zhong, M. (2010) Exposure to 1800 MHz radiofrequency radiation induces oxidative damage to mitochondrial DNA in primary cultured neurons. Brain Res. 1311, 189-196. https://doi.org/10.1016/j.brainres.2009.10.062
  123. Yamaguchi, H., Tsurita, G., Ueno, S., Watanabe, S., Wake, K., Taki, M. and Nagawa, H. (2003) 1439 MHz pulsed TDMA fields affect performance of rats in a T-maze task only when body temperature is elevated. Bioelectromagnetics 24, 223-230. https://doi.org/10.1002/bem.10099
  124. Zhao, T. Y., Zou, S. P. and Knapp, P. E. (2007) Exposure to cell phone radiation up-regulates apoptosis genes in primary cultures of neurons and astrocytes. Neurosci. Lett. 412, 34-38. https://doi.org/10.1016/j.neulet.2006.09.092

Cited by

  1. Effect of Radiofrequency Electromagnetic Radiation on Photobacterium phosphoreum Luminescence vol.81, pp.6, 2019, https://doi.org/10.15407/microbiolj81.06.058
  2. Environmental risk factors of primary brain tumors: A review vol.175, pp.10, 2019, https://doi.org/10.1016/j.neurol.2019.08.004
  3. Design and Implementation of a Monitoring System using Optical Camera Communication for a Smart Factory vol.9, pp.23, 2019, https://doi.org/10.3390/app9235103
  4. Histological and Haematological Alterations in Female Mice after Exposure to Electromagnetic Fields vol.23, pp.3, 2020, https://doi.org/10.3923/pjbs.2020.398.405
  5. Dynamic changes in cytoskeleton proteins of olfactory ensheathing cells induced by radiofrequency electromagnetic fields vol.223, pp.5, 2020, https://doi.org/10.1242/jeb.217190
  6. Design and Implementation of the MIMO–COOK Scheme Using an Image Sensor for Long-Range Communication vol.20, pp.8, 2019, https://doi.org/10.3390/s20082258
  7. Designs for Sensing Radiation: Deployment of a Tangible Interface and a Visual Projection Interface for User Interaction vol.33, pp.2, 2019, https://doi.org/10.15187/adr.2020.05.33.2.57
  8. Does the short-term exposure to radiofrequency electromagnetic field originating from mobile phone affect auditory functions as measured by Acoustic Admittance and Evoked Otoacoustic Emission tests? vol.39, pp.4, 2020, https://doi.org/10.1080/15368378.2020.1826960
  9. Modelling the Influence of Electromagnetic Field on the User of a Wearable IoT Device Used in a WSN for Monitoring and Reducing Hazards in the Work Environment vol.20, pp.24, 2019, https://doi.org/10.3390/s20247131
  10. Changes of selected biochemical parameters of the honeybee under the influence of an electric field at 50 Hz and variable intensities vol.51, pp.6, 2019, https://doi.org/10.1007/s13592-020-00774-1
  11. Long-term exposure to electromagnetic radiation from mobile phones can cause considerable changes in the balance of Bax/Bcl2 mRNA expression in the hippocampus of mice vol.40, pp.1, 2019, https://doi.org/10.1080/15368378.2020.1830793
  12. Possible effects of different doses of 2.1 GHz electromagnetic radiation on learning, and hippocampal levels of cholinergic biomarkers in Wistar rats vol.40, pp.1, 2019, https://doi.org/10.1080/15368378.2020.1851251
  13. 1,800 MHz Radiofrequency Electromagnetic Irradiation Impairs Neurite Outgrowth With a Decrease in Rap1-GTP in Primary Mouse Hippocampal Neurons and Neuro2a Cells vol.9, 2019, https://doi.org/10.3389/fpubh.2021.771508
  14. The Biocompatibility of Wireless Power Charging System on Human Neural Cells vol.11, pp.8, 2021, https://doi.org/10.3390/app11083611
  15. 30 Hz, Could It Be Part of a Window Frequency for Cellular Response? vol.22, pp.7, 2021, https://doi.org/10.3390/ijms22073642
  16. Electromagnetic pollution alert: Microwave radiation and absorption in human organs and tissues vol.40, pp.2, 2021, https://doi.org/10.1080/15368378.2021.1874976
  17. Exposure to RF-EMF Alters Postsynaptic Structure and Hinders Neurite Outgrowth in Developing Hippocampal Neurons of Early Postnatal Mice vol.22, pp.10, 2019, https://doi.org/10.3390/ijms22105340
  18. Design and Implementation of 2D MIMO-Based Optical Camera Communication Using a Light-Emitting Diode Array for Long-Range Monitoring System vol.21, pp.9, 2019, https://doi.org/10.3390/s21093023
  19. Microwave Absorption Performance of Single-Layer and Multi-Layer Structures Prepared by CNTs/Fe3O4 Nonwoven Materials vol.11, pp.8, 2019, https://doi.org/10.3390/cryst11081000
  20. Could Electromagnetic Field Exposure Contribute to “Zoom Fatigue”? vol.27, pp.4, 2021, https://doi.org/10.1089/act.2021.29339.dha
  21. Tracking Devices for Pets: Health Risk Assessment for Exposure to Radiofrequency Electromagnetic Fields vol.11, pp.9, 2019, https://doi.org/10.3390/ani11092721
  22. Prenatal chronic exposure to electromagnetic fields modulated adenosine deaminase activity in serum and brain of Wistar rats’ offspring vol.55, pp.4, 2019, https://doi.org/10.1080/08327823.2021.1993045
  23. IMPACTS OF STATIC ELECTRIC FIELD PRODUCED BY ULTRA-HIGH-VOLTAGE DIRECT-CURRENT TRANSMISSION LINES ON HIPPOCAMPAL PROTEIN EXPRESSION AND MORPHOLOGICAL STRUCTURE IN MICE vol.21, pp.10, 2021, https://doi.org/10.1142/s0219519421400716