Archives of Toxicology

, Volume 90, Issue 10, pp 2337–2348 | Cite as

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

  • A. Maes
  • L. Verschaeve
Review Article


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.


Magnetic fields ELF Cytogenetic damage Lymphocytes Buccal cells Workers 



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


  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 85:144–152CrossRefPubMedGoogle Scholar
  2. Andreassi MG, Barale R, Iozzo P, Picano E (2011) The association of micronucleus frequency with obesity, diabetes and cardiovascular disease. Mutagenesis 26:77–83CrossRefPubMedGoogle 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 13:2961–2966CrossRefPubMedGoogle 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 19:235–238CrossRefPubMedGoogle 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 3-934994-03-2Google Scholar
  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 79:133–135CrossRefPubMedGoogle 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 60:1619–1625PubMedGoogle 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 37:31–45CrossRefPubMedGoogle 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 28:625–631CrossRefPubMedGoogle 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 29:1178–1183CrossRefPubMedPubMedCentralGoogle 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 26:93–100CrossRefPubMedGoogle 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 28:469–474CrossRefGoogle 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 204:379–406CrossRefPubMedGoogle 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 19:421–430CrossRefGoogle 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 215:68–75CrossRefPubMedGoogle Scholar
  16. EHC (2007) Environmental health criteria 238: extremely low frequency fields. World Health Organization, Geneva. ISBN 978-92-4-157238-5Google 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 29:335–336Google 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-XGoogle 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 10:263–269Google 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) PubMedGoogle Scholar
  21. Goud KI, Hasan Q, Balakrishna N, Rao KP, Ahuja YR (2004) Genotoxicity evaluation of individuals working with photocopying machines. Mutat Res 563:151–158CrossRefPubMedGoogle 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 58:4117–4121PubMedGoogle 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 64:2258–2263CrossRefPubMedGoogle 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) CrossRefGoogle 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 92-832-1280-0Google 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 978-92-832-1325-3Google 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 12:17–26CrossRefGoogle Scholar
  28. Leitgeb N (2015a) Synoptic analysis of epidemiologic evidence of glioma risk from mobile phones. J Electromagn Anal 7:233–243Google Scholar
  29. Leitgeb N (2015b) Synoptic analysis clarifies childhood leukemia risk from ELF magnetic field exposure. J Electromagn Anal 7:245–258Google 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)Google Scholar
  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 50:741–749CrossRefGoogle 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 978-951-27-1191-8Google Scholar
  33. Mateuca R, Lombaert N, Aka PV, Decordier I, Kirsch-Volders M (2006) Chromosomal changes: induction, detection methods and applicability in human biomonitoring. Biochimie 88:1515–1531CrossRefPubMedGoogle Scholar
  34. Migliore L, Coppedè F, Fenech M, Thomas P (2011) Association of micronucleus frequency with neurodegenerative diseases. Mutagenesis 26:85–92CrossRefPubMedGoogle 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 639:27–34CrossRefPubMedGoogle 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 23:191–201CrossRefPubMedGoogle Scholar
  37. Nordenson I, Hansson Mild K, Ostman U, Ljungberg H (1988) Chromosomal effects in lymphocytes of 400 kV-substation workers. Radiat Environ Biophys 27:39–47CrossRefPubMedGoogle 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 22:306–315CrossRefPubMedGoogle Scholar
  39. Othman EO, Aly MS, El Nahas SM (2001) Aneuploidy in workers occupationally exposed to electromagnetic fields detected by FISH. Cytologia 66:117–125CrossRefGoogle 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 55:41–51CrossRefPubMedGoogle 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) Google Scholar
  42. SCENIHR (2015) Opinion on Potential health effects of exposure to electromagnetic fields (EMF) European Commission, DG Health and Food Safety.
  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 103:931–932CrossRefPubMedPubMedCentralGoogle 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 19:29–34CrossRefPubMedGoogle 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 22:150–160CrossRefPubMedGoogle 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 34:56–62CrossRefPubMedGoogle 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 82:561–567CrossRefPubMedGoogle Scholar
  48. Udroiu I, Giuliani L, Icradi LA (2010) Genotoxic properties of extremely low frequency electromagnetic fields. Eur J Oncol Libr 5:123–134Google 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 32:325–336CrossRefPubMedGoogle Scholar
  50. Verschaeve L (2009) Genetic damage in subjects exposed to radiofrequency radiation. Mut Res 681:259–270CrossRefGoogle Scholar
  51. Verschaeve L (2015) Genetic toxicology: tests and applications. University Press, Antwerp. ISBN 978-90-5718-283-9Google 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 705:252–268CrossRefGoogle 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 26:412–430CrossRefPubMedGoogle 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 27:511–519PubMedGoogle Scholar
  55. Whorton EB Jr (1985) Some experimental design and analysis considerations for cytogenetics studies. Environ Mutagen 7(Suppl 4):9–15CrossRefPubMedGoogle 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 64:79–86CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Scientific Institute of Public HealthO.D. Food, Medicines and Consumers SafetyBrusselsBelgium
  2. 2.Department of Biomedical SciencesUniversity of AntwerpAntwerpBelgium

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