Mini review
Genetic, carcinogenic and teratogenic effects of radiofrequency fields1

https://doi.org/10.1016/S1383-5742(97)00037-9Get rights and content

Abstract

This paper reviews the literature data on the genetic toxicology of radiofrequency (RF) radiation. Whereas in the past most studies were devoted to microwave ovens and radar equipment, it is now mobile telecommunication that attracts most attention. Therefore we focus on mobile telephone frequencies where possible. According to a great majority of the papers, radiofrequency fields, and mobile telephone frequencies in particular, are not genotoxic: they do not induce genetic effects in vitro and in vivo, at least under non-thermal exposure conditions, and do not seem to be teratogenic or to induce cancer. Yet, some investigations gave rather alarming results that should be confirmed and completed by further experiments. Among them the investigation of synergistic effects and of possible mechanisms of action should be emphasised.

Introduction

Radiofrequency fields, and especially microwaves (300 MHz–300 GHz) are a very important part of the electromagnetic spectrum with respect to their applications and possible health consequences. These non ionising radiations have relatively short wavelengths and high frequencies compared to, e.g., extreme low frequency fields, and therefore also a greater amount of energy which is sufficient to cause heating in conductive materials (Fig. 1). Close to the transmitter, these high-frequency fields may thus be harmful to human beings by producing thermal effects that may sometimes, when thermoregulation processes are insufficient, produce irreversible damage (e.g. cataract; 1, 2). This kind of effect is well known from animal experiments and for that reason does not constitute a particular health problem, as measures can be taken to prevent excessive exposure. But also low-level exposures leading to non-thermal effects are, at least according to certain investigators, possible. Non-thermal effects have been reported in cell cultures and animals, in response to exposure to low-level fields. They are not well established and therefore highly controversial.

While in the past decade people were especially concerned about the safety of microwave ovens (2450 MHz) and even before radar equipment, it is wireless communications (e.g. mobile telephones) that is particularly considered at present. It is now indeed generally accepted that modern microwave ovens are harmless (leakage of microwaves from ovens is insignificant) at least when properly used, whereas a number of investigations on radar operators has identified some “thermal” effects that lead to safety precautions minimising the hazards. But little is known about the health hazards of cellular telephones that are rapidly gaining popularity. There are several systems in use which allow many users to communicate via the system simultaneously. The dominant access technique in Europe is the so-called TDMA technique (Time Division Multiple Access) which is used in GSM (Global System for Mobile communication), DECT (Digital European Cordless Telecommunications), DCS 1800 (Digital personal Communication System) and in TETRA (Trans European Trunked RAdio) systems. The carrier frequency bands allocated for these services are set mainly in the spectrum regions of 800–900 MHz and 1.8–2.2 GHz. With regard to these (and other mobile phone) systems, one has to distinguish the possible effects emanating from transmission antennas and mobile base station antennas from the mobile phone handset itself. People may be exposed to all these sources, but it is the handset that is most often suspected of having deleterious effects. There is a concern that, as the antenna of the handset is brought close to the head when calls are made or received, there may be a thermal insult at the molecular or cellular level. According to some scientists part of the microwave-energy is absorbed by the head and may eventually produce so-called `hot-spots' in the brain (e.g. 3, 4). Also, non-thermal effects are often anticipated. Most often headache, eye injury and cancer are mentioned as potential biological effects [5]. However, the only established possible dangerous effect of mobile phones is the interference in some circumstances with pacemakers and other apparatus prompting a warning to users from health authorities (e.g. [6]). With regard to headache, cancer or other serious illnesses, little is known for sure. Therefore there is an urgent need for the updating of our knowledge. Indeed, not only the general public, but also some of the scientists involved in research on microwave or radiofrequency bioeffects are sufficiently worried about the possible adverse health effects of present-day mobile telephones to recommend restricted use of mobile phone handsets. A few even advise not to use them at all. Although most scientists claim that no research to date suggests serious cause for concern, they all agree that the explosive growth in use of mobile telephones (In 1995 there were over 85 million mobile telephone subscribers world-wide) justifies further research.

In this paper we review the investigations that have been performed on the genotoxic effects of radiofrequency fields, including investigations on cancer and teratogenic effects.

Section snippets

Quantities and units

Non ionising radiations are those electromagnetic radiations with a wavelength equal or higher than 10−7 m. The different non-ionising radiations are given in Fig. 1 where it can be seen that wavelength, frequency and photon energy are inter-related. Non-ionising radiations have photon energies lower than approximately 12 eV, which is considered the boundary with ionising radiations. This energy is too low to induce ionisations of molecules and too low to break even the weakest chemical bond.

Epidemiological investigations

Epidemiological studies, unlike most laboratory studies, tend to take several years and can only give information on exposures that have already occurred in people. Therefore, as mobile telephone bio-effects are only a very recent concern, there are until now no published epidemiological investigations on cause-specific morbidity or mortality in relation to mobile telephone use. Up to now only limited preliminary notes were published on, e.g., the methodology of epidemiological research with

Genetic toxicology: in vitro laboratory investigations

Possible effects on DNA or chromosome structure in somatic cells are considered to be very important as these changes could be associated with cell death or, possibly, with the development of cancer. Furthermore, such effects in male or female germ cells are important, as surviving mutations might be passed on to the next generation. Many investigations of RF-induced genetic effects in somatic- as well as in germ cells, therefore, have already been conducted in many different cell and animal

Genetic toxicology: in vivo laboratory investigations

Several studies were conducted over the past 20 years using Drosophila melanogaster as the test organism. As for the experiments with micro-organisms, they all yielded negative results. Therefore we will also refer to the earlier mentioned review papers. As seen in Table 2 and Table 3, experiments in mammals gave more conflicting results. This was true as well for investigations on germ cells as for investigations on somatic cells.

Cancer-related in vitro investigations

As stated above, the evidence for a clastogenic or genetic effect of microwaves is rather contradictory, although overall it may be concluded that RF-fields/microwaves are not genotoxic under non-thermal conditions. Therefore it may also be concluded that RF-fields or microwaves are not tumour initiators and that, if they are somehow related to carcinogenicity, this should be by some other mechanism (e.g. by influencing tumour promotion or by increasing the uptake of carcinogens in cells).

Cancer-related in vivo investigations

A relatively large number of in vivo investigations, mainly on 2450-MHz waves but also on other frequencies, have already been performed (Table 6 and [50]). Results of many cancer investigations (especially when ongoing and so far unpublished investigations are included) do not support the suggestion that even an extensive daily exposure to EMF causes tumour growth or tumour promotion (e.g. 51, 52, 53). Overall, the evidence for a co-carcinogenic effect or a RF-induced influence on tumour

Other cancer-related studies

The above-mentioned investigations may be considered more or less directly related to cancer. Other investigations on other physiological processes may of course also be related to cancer. This is especially true for effects on the immune system. It is indeed well known that the immune system plays an important role in controlling the proliferation of cancer cells. Therefore, numerous studies have also been performed at various power levels and frequencies. However, these investigations are

Conclusion

Today, it is still not very clear whether proper use of radiofrequency fields and microwave-emitting devices may be harmful to human beings. Many investigations have been performed in the past and many different end-points have been studied. Investigations on genetic- or cancer-related effects are among them. It was almost invariably found that biological effects of acute exposure to these fields were consistent with responses to induced heating, resulting in frank rises in cellular, tissue or

References (125)

  • S.N. Goud et al.

    Genetic effects of microwave radiation in mice

    Mutation Res.

    (1982)
  • R.D. Saunders et al.

    Dominant lethal studies in male mice after exposure to 2.45 GHz microwave radiation

    Mutation Res.

    (1983)
  • S.F. Cleary et al.

    Cataract incidence in radar workers

    Arch. Environ. Health

    (1965)
  • L. Martens et al.

    Calculation of the electromagnetic fields induced in the head of an operator of a cordless telephone

    Radio Sci.

    (1995)
  • A.W. Guy

    The starting point: wireless technology research, L.L.C.'s dosimetry risk evaluation research

    Hum. Ecol. Risk Assess.

    (1997)
  • U. Bergqvist, Review of epidemiological studies, in: N. Kuster, Q. Balzano, J.C. Lin (Eds.), Mobile Communication...
  • H.I. Bassen, RF interference of medical devices, in: N. Kuster, Q. Balzano, J.C. Lin (Eds.), Mobile Communication...
  • N. Kuster, Q. Balzano, Experimental and numerical dosimetry., in: N. Kuster, Q. Balzano, J.C. Lin (Eds.), Mobile...
  • D.P. Funch et al.

    Utility of telephone company records for epidemiologic studies of cellular phones

    Epidemiology

    (1996)
  • K.J. Rothman et al.

    Assessment of cellular telephone and other radio frequency exposure for epidemiologic research

    Epidemiology

    (1996)
  • K.J. Rothman et al.

    Overall mortality of cellular telephone customers

    Epidemiology

    (1996)
  • L. Verschaeve

    Can nonionising radiation induce cancer?

    Cancer J.

    (1995)
  • A.M. Lilienfield, J. Tonascia, S. Tonascia, et al., Evaluation of health status of foreign service and other employees...
  • S. Milham

    Increased mortality in amateur radio operators due to lymphatic and hematopoietic malignancies

    Am. J. Epidemiol.

    (1988)
  • B. Armstrong et al.

    Association between exposure to pulsed electromagnetic fields and cancer in electric utility workers in Quebec, Canada, and France

    Am. J. Epidemiol.

    (1994)
  • C.D. Robinette et al.

    Effect upon health of occupational exposure to microwave radiation (radar)

    Am. J. Epidemiol.

    (1980)
  • S. Szmigielski, Cancer morbidity in subjects occupationally exposed to high-frequency (radiofrequency and microwave)...
  • R.D. Saunders, C.I. Kowalczuk, Z.J. Sienkiewicz, Biological Effects of Exposure to Non-ionising Electromagnetic Fields...
  • WHO, Electromagnetic fields (300 Hz to 300 GHz), Environmental Health Criteria 137, WHO, Geneva, 1993, pp....
  • G. d'Ambrosio et al.

    Genotoxic effects of amplitude-modulated microwaves on human lymphocytes exposed in vitro under controlled conditions

    Electro-Magnetobiol.

    (1995)
  • M.T. Alam et al.

    Cytological effects of microwave radiation in Chinese hamster cells in vitro

    Can. J. Genet. Cytol.

    (1978)
  • A. Maes et al.

    In vitro cytogenetic effects of 2450 MHz waves on human peripheral blood lymphocytes

    Bioelectromagnetics

    (1993)
  • D.J. Brusick, An Assessment of the Genotoxic Activity of Radiofrequency Radiation, State of the Science Colloquium,...
  • A. Maes et al.

    954 MHz microwaves enhance the mutagenic properties of mitomycin C

    Environ. Mol. Mutagen.

    (1996)
  • A. Maes, M. Collier, U. Van Gorp, S. Vandoninck, L. Verschaeve, Cytogenetic effects of 935.2-MHz (GSM) microwaves alone...
  • M. Gillois, C. Auge, C. Chevalet, Effet des ondes électromagnétiques non-ionisants sur la viabilité et l'hérédité des...
  • J. Holt et al.

    Four years of microwaves in cancer therapy

    J. Belge Radiol.

    (1976)
  • S.A. Gunn et al.

    The effect of microwave radiation on morphology and function of rat testis

    Lab. Invest.

    (1961)
  • R.D. Saunders et al.

    Effects of 2.45 GHz microwave radiation and heat on mouse spermatogenic epithelium

    Int. J. Radiat. Biol.

    (1981)
  • C.V. Beechey et al.

    Cytogenetic effects of microwave irradiation on male germ cells of the mouse

    Int. J. Radiat. Biol.

    (1986)
  • M.J. Edwards, R.A. Wanner, in: J.G. Wilson, F. Clark, (Eds.), Handbook of Teratology, Vol. 1. General Principles and...
  • M.J. Edwards

    Congenital effects due to hyperthermia

    Adv. Vet. Comp. Med.

    (1978)
  • D. Poswillo et al.

    Hyperthermia as a teratogenic agent

    Ann. R. Soc. Coll. Surgeons

    (1974)
  • M.E. O'Connor

    Mammalian teratogenesis and radiofrequency fields

    Proc. IEEE

    (1980)
  • H. Lai et al.

    Acute low-intensity microwave exposure increases DNA single-strand breaks in rat brain cells

    Bioelectromagnetics

    (1995)
  • H. Lai et al.

    Single- and double-strand DNA breaks in rat brain cells after acute exposure to radiofrequency electromagnetic radiation

    Int. J. Radiat. Biol.

    (1996)
  • H. Lai, M. Carino, N. Singh, Naltrexone blocks RFR-induced DNA double strand breaks in rat brain cells, (1997) in...
  • H. Lai

    Research on the neurological effects of non-ionizing radiation at the university of Washington

    Bioelectromagnetics

    (1992)
  • O.M. Garson et al.

    A chromosomal study of workers with long-term exposure to radio-frequency radiation

    Med. J. Aust.

    (1991)
  • J.W. Allis et al.

    Temperature-specific inhibition of human cell Na+/K+ATPase by 2450 MHz microwave radiation

    Bioelectromagnetics

    (1987)
  • Cited by (139)

    • A meta-analysis of in vitro exposures to weak radiofrequency radiation exposure from mobile phones (1990–2015)

      2020, Environmental Research
      Citation Excerpt :

      Biological effects due to electromagnetic radiation from mobile communication systems may depend on a number of signal properties including the mean power level, frequency, and modulation of the electromagnetic signal, as well as polarity and underlying nutritional and health status of exposed hosts. For several decades concerns have been raised about the safety of extended use of mobile phones (Vijayalaxmi et al., 2014; Leszczynski et al., 2012; Marino et al., 2011; Gaestel, 2010; Paffi et al., 2010; McNamee and Chauhan, 2009; Verschaeve, 2001, 2005, 2009; Vijayalakshmi and Prihoda, 2009; Ruediger, 2009; Vijayalaxmi and Prihoda, 2008; Tusch et al., 2006; Moulder et al., 2005; Cotgreave, 2005; Vijayalaxmi and Obe, 2004; Meltz, 2003; Ahlbom et al., 2003; Heynick et al., 2003; Brusick et al., 1998; Verschaeve and Maes, 1998; Hermann and Hossmann, 1997; Leonarda et al., 1983). The recommendations of standard bodies ICNIRP (International Commission on Non-Ionizing Radiation Protection (ICNIRP), 1998), IEEE (IEEE C95.1-2005, 2005), CENELEC (CENELEC, 1995) for exposure limits are based exclusively on measurements of health effects due to elevating tissue temperatures that affect the absorption of energy during exposure and also do not take into account variations in BMF, nor the importance of cell types or signal properties.

    • Radio frequency electromagnetic fields: Health effects

      2019, Encyclopedia of Environmental Health
    • Effects of pre- and postnatal exposure to 1880–1900 MHz DECT base radiation on development in the rat

      2016, Reproductive Toxicology
      Citation Excerpt :

      The reproductive and teratogenetic effects of EMF were investigated very early from 1961 to 1991. The majority of these experimental studies dealt with exposure of animals to 2450-MHz EMF, while few studies investigated the effects of 915- and 970-MHz EMF on embryonic development [3,4], and have been reviewed by Verschaeve and Maes in terms of the genetic, carcinogenic, and teratogenic effects of radiofrequency (RF) fields (300 MHz–300 GHz) [5]. Later on, other researchers have shown that RF fields were teratogenic when the specific absorption rate (SAR) level was high enough to raise considerably maternal body temperature (cf review [6]), but only a few have found effects on animal reproduction (cf reviews [7,8]), as well as on growth and development [6,9,10] after exposure of animals to SAR values below the ICNIRP limit, i.e., at a whole body SAR of 0.08 W/kg [11].

    • Oxidative and genotoxic effects of 900MHz electromagnetic fields in the earthworm Eisenia fetida

      2013, Ecotoxicology and Environmental Safety
      Citation Excerpt :

      Although the majority of experiments demonstrate negative effects, positive findings are found also (Rüdiger, 2009; Speit et al., 2007; Verschaeve et al., 2010). Quite often the observed effects of RF-EMFs are associated with its ability to increase the temperature of the biological material (Brusick et al., 1998; Verschaeve and Maes, 1998; Verschaeve et al., 2010). Nevertheless, some studies documented non-thermal biological effects upon RF-EMF exposures (Friedman et al., 2007; Leszczynski et al., 2002; Panagopoulos and Margaritis, 2010; Velizarov et al., 1999), including genotoxic endpoints (Campisi et al., 2010).

    View all citing articles on Scopus
    1

    This is the second in a series of four papers, the first of which was published in Mutation Res. 387 (1997) pp. 165–171.

    View full text