Skip to main content

Genetic damage in humans exposed to extremely low-frequency electromagnetic fields

Abstract

The classification of extremely low-frequency magnetic fields by the International Agency for Research on Cancer in the group of ‘possible human carcinogens’ (group 2B) is essentially based on epidemiologic evidence showing an association between MF exposures and childhood leukaemia. Despite many in vitro and in vivo investigations, there is no established causal relationship yet. However, human cytogenetic biomonitoring studies that were conducted in the past show predominantly positive results, i.e. increased cytogenetic damage in peripheral blood lymphocytes or buccal cells of ELF-MF-exposed subjects. This is important given the established link between observed cytogenetic damage in cells of people and an increased cancer risk. We here conducted an evaluation of the published investigations and found that many of the studies clearly have shortcomings, which often prevent any firm conclusion. As a matter of fact, there are reasons to believe that effects are not that impressive. However, the totality of the studies cannot simply be disregarded warranting further caution and the application, to a certain extent, of the precautionary principle.

This is a preview of subscription content, access via your institution.

References

  1. Albert GC, McNamee JP, Marro L, Bellier PV, Prato FS, Thomas AW (2009) Assessment of genetic damage in peripheral blood of human volunteers exposed (whole-body) to a 200 muT, 60 Hz magnetic field. Int J Radiat Biol 85:144–152

    CAS  Article  PubMed  Google Scholar 

  2. Andreassi MG, Barale R, Iozzo P, Picano E (2011) The association of micronucleus frequency with obesity, diabetes and cardiovascular disease. Mutagenesis 26:77–83

    CAS  Article  PubMed  Google Scholar 

  3. Balamuralikrishnan B, Balachandar V, Kumar SS, Stalin N, Varsha P, Devi SM, Arun M, Manikantan P, Venkatesan C, Sasikala K, Dharwadjar SN (2012) Evaluation of chromosomal alterations in electric workers occupationally exposed to low frequency of electromagnetic fields (EMFs) in Coimbatore population, India. Asian Pac J Cancer Prev 13:2961–2966

    Article  PubMed  Google Scholar 

  4. Bauchinger M, Hauf R, Schmid E, Dresp J (1981) Analysis of structural chromosome changes and SCE after occupational long-term exposure to electric and magnetic fields from 380 kV-systems. Radiat Environ Biophys 19:235–238

    CAS  Article  PubMed  Google Scholar 

  5. Bergqvist U, Brix J, de Gruijl F, de Seze R,Hietanen M, Jeffereys JGR, Lagroye I, Lotz GW, Owen RD, Repacholi MH, Saunders R, Tenforde TS, Verschaeve L, Veyret B (2003) Review of experimental investigations of EMF biological effects (0-100 kHz)—ICNIRP Standing committee II. In: Matthes R, McKinley A, Bernhardt J, Vecchia P, Veyret B (eds) Exposure to static and low frequency electromagnetic fields, biological effects and health consequences. ICNIRP13/2003, ISBN 3-934994-03-2

  6. Bonassi S, Abbondandolo A, Camurri L, Dal PL, De FM, Degrassi F, Forni A, Lamberti L, Lando C, Padovani P (1995) Are chromosome aberrations in circulating lymphocytes predictive of future cancer onset in humans? Preliminary results of an Italian cohort study. Cancer Genet Cytogenet 79:133–135

    CAS  Article  PubMed  Google Scholar 

  7. Bonassi S, Hagmar L, Stromberg U, Montagud AH, Tinnerberg H, Forni A, Heikkila P, Wanders S, Wilhardt P, Hansteen IL, Knudsen LE, Norppa H (2000) Chromosomal aberrations in lymphocytes predict human cancer independently of exposure to carcinogens. European Study Group on Cytogenetic Biomarkers and Health. Cancer Res 60:1619–1625

    CAS  PubMed  Google Scholar 

  8. Bonassi S, Fenech M, Lando C, Lin YP, Ceppi M, Chang WP, Holland N, Kirsch-Volders M, Zeiger E, Ban S, Barale R, Bigatti MP, Bolognesi C, Jia C, Di Giorgio M, Ferguson LR, Fucic A, Lima OG, Hrelia P, Krishnaja AP, Lee TK, Migliore L, Mikhalevich L, Mirkova E, Mosesso P, Müller WU, Odagiri Y, Scarffi MR, Szabova E, Vorobtsova I, Vral A, Zijno A (2001) HUman MicroNucleus project: international database comparison for results with the cytokinesis-block micronucleus assay in human lymphocytes: I. Effect of laboratory protocol, scoring criteria, and host factors on the frequency of micronuclei. Environ Mol Mutagen 37:31–45

    CAS  Article  PubMed  Google Scholar 

  9. Bonassi S, Znaor A, Ceppi M, Lando C, Chang WP, Holland N, Kirsch-Volders M, Zeiger E, Ban S, Barale R, Bigatti MP, Bolognesi C, Cebulska-Wasilewska A, Fabianova E, Fucic A, Hagmar L, Joksic G, Martelli A, Migliore L, Mirkova E, Scarfi MR, Zijno A, Norppa H, Fenech M (2007) An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis 28:625–631

    CAS  Article  PubMed  Google Scholar 

  10. Bonassi S, Norppa H, Ceppi M, Stromberg U, Vermeulen R, Znaor A, Cebulska-Wasilewska A, Fabianova E, Fucic A, Gundy S, Hansteen IL, Knudsen LE, Lazutka J, Rossner P, Sram RJ, Boffetta P (2008) Chromosomal aberration frequency in lymphocytes predicts the risk of cancer: results from a pooled cohort study of 22 358 subjects in 11 countries. Carcinogenesis 29:1178–1183

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Bonassi S, El-Zein R, Bolognesi C, Fenech M (2011) Micronuclei frequency in peripheral blood lymphocytes and cancer risk: evidence from human studies. Mutagenesis 26:93–100

    CAS  Article  PubMed  Google Scholar 

  12. Carbonari K, Gonçalves L, Roth D, Moreira P, Fernández R, Martino-Roth MdG (2005) Increased micronucleated cell frequency related to exposure to radiation emitted by computer cathode ray tube video display monitors. Genet Mol Biol 28:469–474

    Article  Google Scholar 

  13. Carrano AV (1988) Considerations for population monitoring using cytogenetic techniques. ICPEMC—International Commission For Protection Against Environmental Mutagens and Carcinogens. Publication N. 14. Mutat Res 204:379–406

    CAS  Article  PubMed  Google Scholar 

  14. Celikler S, Aydemir N, Vatan O, Kurtuldu S, Bilaloglu R (2009) A biomonitoring study of genotoxic risk to workers of transformers and distribution line stations. Int J Environ Hyg Health Res 19:421–430

    Article  Google Scholar 

  15. Dominici L, Villarini M, Fatigoni C, Monarca S, Moretti M (2011) Genotoxic hazard evaluation in welders occupationally exposed to extremely low-frequency magnetic fields (ELF-MF). Int J Hyg Environ Health 215:68–75

    CAS  Article  PubMed  Google Scholar 

  16. EHC (2007) Environmental health criteria 238: extremely low frequency fields. World Health Organization, Geneva. ISBN 978-92-4-157238-5

    Google Scholar 

  17. Erdal ME, Erdal N, Oğuzkan S (1999) Chromosomal aberrations in peripheral lymphocytes of a high-voltage power lineman exposed to electromagnetic fields. Turk J Med Sci 29:335–336

    Google Scholar 

  18. Evans HJ (1977) Molecular mechanisms in the induction of chromosome aberrations. In: Scott D, Bridges BA, Sobels FH (eds) Progress in genetic toxicology. Elsevier/North Holland Biomedical Press, Amsterdam, pp 57–74. ISBN 0-444-80014-X

    Google Scholar 

  19. Gadhia P, Chakraborty S, Pithawala M (2010) Cytogenetic studies on railway engine drivers exposed to extremely low frequency electromagnetic fields (ELF-EMF). Int J Hum Genet 10:263–269

    Google Scholar 

  20. Gobba F, Rocatto L, Sinigaglia B, Temperani P (2003) Sister chromatid exchanges (SCE) and high frequency cells in workers occupationally exposed to extremely low frequency magnetic fields. Med Lav 94:450–458 (in Italian)

    CAS  PubMed  Google Scholar 

  21. Goud KI, Hasan Q, Balakrishna N, Rao KP, Ahuja YR (2004) Genotoxicity evaluation of individuals working with photocopying machines. Mutat Res 563:151–158

    CAS  Article  PubMed  Google Scholar 

  22. Hagmar L, Bonassi S, Stromberg U, Brøgge A, Knudsen LE, Norppa H, Reuterwall C (1998) Chromosomal aberrations in lymphocytes predict human cancer: a report from the European Study Group on Cytogenetic Biomarkers and Health (ESCH). Cancer Res 58:4117–4121

    CAS  PubMed  Google Scholar 

  23. Hagmar L, Stromberg U, Bonassi S, Hansteen IL, Knudsen LE, Lindholm C, Norppa H (2004) Impact of types of lymphocyte chromosomal aberrations on human cancer risk: results from Nordic and Italian cohorts. Cancer Res 64:2258–2263

    CAS  Article  PubMed  Google Scholar 

  24. Higino Estécio MR, Silva AE (2002) Chromosome abnormalities caused by computer video display monitors’ radiation. Rev Saúde Pública 36:330–336 (in Portuguese)

    Article  Google Scholar 

  25. IARC (2002) IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 80, non-ionizing radiation, part 1: static and extremely low-frequency (ELF) electric and magnetic fields. IARC Press, Lyon. ISBN 92-832-1280-0

    Google Scholar 

  26. IARC (2013) IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 102, non- ionizing radiation, part 2: radiofrequency electromagnetic fields. IARC Press, Lyon. ISBN 978-92-832-1325-3

    Google Scholar 

  27. Khalil AM, Quassem W, Amoura F (1993) Cytogenetic changes in human lymphocytes from workers occupationally exposed to high-voltage electromagnetic fields. Electro Magnetobiol 12:17–26

    Article  Google Scholar 

  28. Leitgeb N (2015a) Synoptic analysis of epidemiologic evidence of glioma risk from mobile phones. J Electromagn Anal 7:233–243

    Google Scholar 

  29. Leitgeb N (2015b) Synoptic analysis clarifies childhood leukemia risk from ELF magnetic field exposure. J Electromagn Anal 7:245–258

    Google Scholar 

  30. Maes A (1998) Genetic effects of non-ionizing radiations, especially microwaves and extremely low frequency fields. PhD thesis, Free University of Brussels (VUB), Brussels (in Dutch)

  31. Maes A, Anthonissen R, Wambacq S, Simons K, Verschaeve L (2016) The cytome assay as a tool to investigate the possible association between exposure to extreme low frequency magnetic fields and an increased risk for Alzheimer’s disease. J Alzheimer’s Dis 50:741–749

    CAS  Article  Google Scholar 

  32. Markkanen A (2009) Effects of electromagnetic fields on cellular responses to agents causing oxidative stress and DNA damage. Kuopio University Publications C. Natural and Environmental Sciences vol 253, 59 p. ISBN 978-951-27-1191-8

  33. Mateuca R, Lombaert N, Aka PV, Decordier I, Kirsch-Volders M (2006) Chromosomal changes: induction, detection methods and applicability in human biomonitoring. Biochimie 88:1515–1531

    CAS  Article  PubMed  Google Scholar 

  34. Migliore L, Coppedè F, Fenech M, Thomas P (2011) Association of micronucleus frequency with neurodegenerative diseases. Mutagenesis 26:85–92

    CAS  Article  PubMed  Google Scholar 

  35. Murgia E, Ballardin M, Bonassi S, Rossi AM, Barale R (2008) Validation of micronuclei frequency in peripheral blood lymphocytes as early cancer risk biomarker in a nested case-control study. Mutat Res 639:27–34

    CAS  Article  PubMed  Google Scholar 

  36. Nordenson I, Hansson Mild K, Nordström S, Sweins A, Birke E (1984) Clastogenic effects in human lymphocytes of power frequency electric fields: in vivo and in vitro studies. Radiat Environ Biophys 23:191–201

    CAS  Article  PubMed  Google Scholar 

  37. Nordenson I, Hansson Mild K, Ostman U, Ljungberg H (1988) Chromosomal effects in lymphocytes of 400 kV-substation workers. Radiat Environ Biophys 27:39–47

    CAS  Article  PubMed  Google Scholar 

  38. Nordenson I, Hansson Mild K, Järventaus H, Hirvonen A, Sandström M, Wilén J, Blix N, Norppa H (2001) Chromosome aberrations in peripheral lymphocytes of train engine drivers. Bioelectromagnetics 22:306–315

    CAS  Article  PubMed  Google Scholar 

  39. Othman EO, Aly MS, El Nahas SM (2001) Aneuploidy in workers occupationally exposed to electromagnetic fields detected by FISH. Cytologia 66:117–125

    Article  Google Scholar 

  40. Rastkhah E, Zakeri F, Ghoranneviss M, Rajabpour MR, Farshidpour MR, Mianji F, Bayat M (2016) The cytokinesis-blocked micronucleus assay: dose–response calibration curve, background frequency in the population and dose estimation. Radiat Environ Biophys 55:41–51

    CAS  Article  PubMed  Google Scholar 

  41. Scaringi M, Temperani P, Rossi P, Bravo G, Gobba F (2007) Evaluation of the genotoxicity of the extremely low frequency-magnetic fields (ELF-MF) in workers exposed for professional reasons. Giorn It Med Lavoro Ergon 29:420–421 (in Italian)

    CAS  Google Scholar 

  42. SCENIHR (2015) Opinion on Potential health effects of exposure to electromagnetic fields (EMF) European Commission, DG Health and Food Safety. http://ec.europa.eu/health/scientific_committees/emerging/docs/scenihr_o_041.pdf

  43. Schmiedel S, Blettner M (2010) The association between extremely low-frequency electromagnetic fields and childhood leukaemia in epidemiology: enough is enough? Br J Cancer 103:931–932

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Skyberg K, Hansteen I-L, Vistnes AM (1993) Chromosome aberrations in lymphocytes of high-voltage cable splicers exposed to electromagnetic fields. Scand J Work Environ Health 19:29–34

    CAS  Article  PubMed  Google Scholar 

  45. Skyberg K, Hansteen I-L, Vistnes AM (2001) Chromosomal aberrations in lymphocytes of employees in transformer and generator production exposed to electromagnetic fields and mineral oil. Bioelectromagnetics 22:150–160

    CAS  Article  PubMed  Google Scholar 

  46. Tiwari R, Lakshmi NK, Bhargava SC, Ahuja YR (2015) Epinephrine, DNA integrity and oxidative stress in workers exposed to extremely low-frequency electromagnetic fields (ELF-EMFs) at 132 kV substations. Electromagn Biol Med 34:56–62

    CAS  Article  PubMed  Google Scholar 

  47. Udroiu I, Cristaldi M, Icradi LA (2006) Clastogenicity and aneuploidy in newborn and adult mice exposed to 50 Hz magnetic fields. Int J Radiat Biol 82:561–567

    CAS  Article  PubMed  Google Scholar 

  48. Udroiu I, Giuliani L, Icradi LA (2010) Genotoxic properties of extremely low frequency electromagnetic fields. Eur J Oncol Libr 5:123–134

    Google Scholar 

  49. Valjus J, Norppa H, Järventaus H, Sorsa M, Nykyri E, Salomaa S, Järvinen P, Kjader J (1993) Analysis of chromosomal aberrations, sister chromatid exchanges and micronuclei among power linesmen with long-term exposure to 50-Hz electromagnetic fields. Radiat Environ Biophys 32:325–336

    CAS  Article  PubMed  Google Scholar 

  50. Verschaeve L (2009) Genetic damage in subjects exposed to radiofrequency radiation. Mut Res 681:259–270

    CAS  Article  Google Scholar 

  51. Verschaeve L (2015) Genetic toxicology: tests and applications. University Press, Antwerp. ISBN 978-90-5718-283-9

    Google Scholar 

  52. Verschaeve L, Juutilainen J, Lagroye I, Miyakoshi J, van Rongen E, Saunders R, de Seze R, Tenforde T, Veyret B, Xu Z (2010) In vitro and in vivo genotoxicity of radiofrequency fields. Mut Res 705:252–268

    CAS  Article  Google Scholar 

  53. Vijayalaxmi, Obe G (2005) Controversial cytogenetic observations in mammalian somatic cells exposed to extremely low frequency electromagnetic radiation: a review and future research recommendations. Bioelectromagnetics 26:412–430

    CAS  Article  PubMed  Google Scholar 

  54. Villarini M, Dominici L, Fatigoni C, Levorato S, Vannini S, Monarca S, Moretti M (2015) Primary DNA damage in welders occupationally exposed to extremely-low-frequency magnetic fields (ELF-MF). Ann Ig 27:511–519

    PubMed  Google Scholar 

  55. Whorton EB Jr (1985) Some experimental design and analysis considerations for cytogenetics studies. Environ Mutagen 7(Suppl 4):9–15

    Article  PubMed  Google Scholar 

  56. Whorton EB Jr, Bee DE, Kilian DJ (1979) Variations in the proportion of abnormal cells and required sample sizes for human cytogenetic studies. Mutat Res 64:79–86

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This literature review was conducted as part of our activities within the Belgian BioElectroMagnetics Group (BBEMG).

Author information

Affiliations

Authors

Corresponding author

Correspondence to L. Verschaeve.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Maes, A., Verschaeve, L. Genetic damage in humans exposed to extremely low-frequency electromagnetic fields. Arch Toxicol 90, 2337–2348 (2016). https://doi.org/10.1007/s00204-016-1769-9

Download citation

Keywords

  • Magnetic fields
  • ELF
  • Cytogenetic damage
  • Lymphocytes
  • Buccal cells
  • Workers